LATIN AMERICAN JOURNAL OF AQUATIC RESEARCH

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Pontificia Universidad Catlica de Valparaso
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Escuela de Ciencias del Mar Centro de Cincias Tecnolgicas, da Terra e do Mar
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Valparaso, Chile Itajai, Santa Catarina, Brasil
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Estacin de Fotobiologa Playa Unin Escuela de Ciencias del Mar
Rawson, Chubut, Argentina Pontificia Universidad Catlica de Valparaso
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Universidad de Los Lagos Escuela de Biologa
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Facultad de Ciencias Biolgicas Asociacin Brasilea de Oceanografa
Pontificia Universidad Catlica de Chile Centro Balneario Cambori, Brasil
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 LATIN AMERICAN JOURNAL OF AQUATIC RESEARCH
Lat. Am. J. Aquat. Res., 39(2) 2011

CONTENTS

Research Articles

Joseph Selvin, Aseer Manilal, Suganthan Sujith, George Seghal Kiran & Aron Premnath Lipton
Efficacy of marine green alga Ulva fasciata extract on the management of shrimp bacterial diseases. Eficacia del extrac-
to del alga marina verde Ulva fasciata sobre el manejo de las enfermedades bacterianas en camarones197-204

Luciano N. Padovani, Mara D. Vias & Marcelo Pjaro

Importance of the Ro de la Plata estuarine front (southwestern Atlantic Ocean) in the feeding ecology of Argentine
anchovy, Engraulis anchoita (Clupeiformes, Clupeidae). Importancia del frente estuarial del Ro de la Plata (Ocano Atln-
tico sudoccidental) en la ecologa trfica de la anchota argentina, Engraulis anchoita (Clupeiformes, Clupei-
dae)......205-213

Susana Mara Velurtas, Ana Cristina Daz, Anala Vernica Fernndez-Gimenez & Jorge Lino Fenucci
Influence of dietary starch and cellulose levels on the metabolic profile and apparent digestibility in penaeoid shrimp.
Influencia del nivel de almidn y celulosa en la dieta sobre el perfil metablico y digestibilidad aparente en camarones penaeoi-
deos..214-224

Ral Prez-Gonzlez
Catch composition of the spiny lobster Panulirus gracilis (Decapoda: Palinuridae) off the western coast of Mexico.
Composicin de la captura de la langosta espinosa Panulirus gracilis (Decapoda: Palinuridae) en la costa oeste de Mxi-
co.........225-235

Mauricio F. Landaeta, Claudia A. Bustos, Pamela Palacios-Fuentes, Pablo Rojas & Fernando Balbontn
Distribucin del ictioplancton en la Patagonia austral de Chile: potenciales efectos del deshielo de Campos de Hielo
Sur. Ichthyoplankton distribution in South Patagonia, Chile: potential effects of ice melting from the Southern Ice Field...236-249

Jess Rodrguez-Romero, Laura del Carmen Lpez-Gonzlez, Felipe Galvn-Magaa, Francisco J. Snchez-Gutirrez, Roxana
B. Inohuye-Rivera & Juan C. Prez-Urbiola
Seasonal changes in a fish assemblage associated with mangroves in a coastal lagoon of Baja California Sur, Mexico.
Cambios estacionales de la comunidad de peces asociada a zonas de manglar en una laguna costera de Baja California Sur,
Mxico ....250-260

Douglas Fernando Peir, Paulo Ricardo Pezzuto & Fernando Luis Mantelatto
Relative growth and sexual dimorphism of Austinixa aidae (Brachyura: Pinnotheridae): a symbiont of the ghost shrimp
Callichirus major from the southwestern Atlantic. Crecimiento relativo y dimorfismo sexual en Austinixa aidae (Barchyura:
Pinnotheridae): un simbionte del camarn fantasma Callichirus major del Atlntico sudoccidental ...261-270

Joan Sebastin Salas-Leiva & Enrique Dupr

Cryopreservation of the microalgae Chaetoceros calcitrans (Paulsen): analysis of the effect of DMSO temperature and
light regime during different equilibrium periods. Criopreservacin de las microalgas Chaetoceros calcitrans (Paulsen):
anlisis del efecto de la temperatura de DMSO y rgimen de luz durante diferentes perodos de equil-
brio.......271-279

Paulina Soto, Hernn Gaete & Mara Eliana Hidalgo

Assessment of catalase activity, lipid peroxidation, chlorophyll-a, and growth rate in the freshwater green algae Pseu-
dokirchneriella subcapitata exposed to copper and zinc. Evaluacin de la actividad de la catalasa, peroxidacin lipdica,
clorofila-a y tasa de crecimiento en la alga verde de agua dulce Pseudokirchneriella subcapitata expuesta a cobre y
zinc. .....280-285

www.scielo.cl/imar.htm www.lajar.cl
Luis Fernando Payn, Andrs Felipe Navia, Efran A. Rubio & Paola Andrea Meja-Falla
Biologa de la raya guitarra Rhinobatos leucorhynchus (Gnther, 1867) (Rajiformes: Rhinobatidae) en el Pacfico co-
lombiano. Biology of the guitar ray Rhinobatos leucorhynchus (Gnther, 1867) (Rajiformes: Rhinobatidae) in the Colombian
Pacific...................................................................................................................................................................................286-296

Alfredo C. Barretto, Margarita B. Sez, Mara R. Rico & Andrs J. Jaureguizar

Age determination, validation, and growth of Brazilian flathead (Percophis brasiliensis) from the southwest Atlantic
coastal waters (34-41S). Determinacin de edad, validacin y crecimiento del pez palo (Percophis brasiliensis) de
aguas costeras del Atlntico sudoccidental (34-41S) ......297-305

Santiago Andrs Echaniz & Alicia Mara Vignatti

Seasonal variation and influence of turbidity and salinity on the zooplankton of a saline lake in central Argentina. Va-
riacin estacional e influencia de la turbidez y la salinidad sobre el zooplancton de un lago salino de la regin central de Argen-
tina........................................................................................................................................................................................306-315

Rodrigo Wiff, Juan Carlos Quiroz, Vilma Ojeda & Mauricio A. Barrientos
Estimacin de mortalidad natural e incertidumbre para congrio dorado (Genypterus blacodes Schneider, 1801) en la
zona sur-austral de Chile. Estimation of natural mortality and uncertainty in pink cusk-eel (Genypterus blacodes Schneider,
1801) in southern Chile.....316-326

Christopher Concha, Emilio Figueroa & Federico M. Winkler

Asociacin entre la tasa de autofecundacin y la frecuencia de larvas malformadas en poblaciones cultivadas del os-
tin del norte Argopecten purpuratus (Lamarck, 1819). Association between self-fertilization rates and the frequency of mal-
formed larvae in farmed populations of the northern scallop Argopecten purpuratus (Lamarck, 1819)..327-337

Andrea Ubilla & Ivn Valdebenito

Use of antioxidants on rainbow trout Oncorhynchus mykiss (Walbaum, 1792) sperm diluent: effects on motility and
fertilizing capability. Uso de antioxidantes en el diluyente espermtico para trucha arcoiris Oncorhynchus mykiss (Walbaum,
1792): efecto en la motilidad y capacidad fecundante.........................................................................338-343

Mara Alejandra Romero, Silvana Dans, Ral Gonzlez, Guillermo Svendsen, Nstor Garca & Enrique Crespo
Solapamiento trfico entre el lobo marino de un pelo Otaria flavescens y la pesquera de arrastre demersal del golfo
San Matas-Patagonia, Argentina. Trophic overlap between South American sea lion Otaria flavescens and trawl demersal
fishery in San Matas gulf-Patagonia, Argentina...344-358

Viviana Bravo, Sergio Palma & Nelson Silva

Seasonal and vertical distribution of medusae in Aysn region, southern Chile. Distribucin estacional y vertical de me-
dusas en la regin de Aysn, sur de Chile.359-377

Short Communications

Mauricio Ibarra & Patricio M. Arana

Crecimiento del camarn excavador Parastacus pugnax (Poeppig, 1835) determinado mediante tcnica de marcaje.
Growth of burrowing crayfish Parastacus pugnax (Poeppig, 1835) determined by marking technique......378-384

Subramanian Bragadeeswaran, Sangappellai Thangaraj, Kolandhasamy Prabhu & Solaman Raj Sophia Rani
Antifouling activity by sea anemone (Heteractis magnifica and H. aurora) extracts against marine biofilm bacteria. Ac-
tividades anti-incrustantes de las extractos de las anmonas marinas Heteractis magnifica y H. aurora frente a biofilm de
bacterias marinas........................385-389

Miguel Avendao & Marcela Cantillnez

Reestablecimiento de Choromytilus chorus (Molina, 1782) (Bivalvia: Mytilidae) en el norte de Chile. Reestablishment of
Choromytilus chorus (Molina, 1782) (Bivalvia: Mytilidae) in northern Chile.....390-396

www.scielo.cl/imar.htm www.lajar.cl
Lat. Am. J. Aquat. Res., 39(2): 197-204, 2011 Efficacy of marine green alga Ulva fasciata 197
DOI: 10.3856/vol39-issue2-fulltext-1

Research Article

Efficacy of marine green alga Ulva fasciata extract on the management of

shrimp bacterial diseases

Joseph Selvin1, Aseer Manilal2, Suganthan Sujith3, George Seghal Kiran4 & Aron Premnath Lipton5
1-4
Department of Microbiology, Bharathidasan University
Tiruchirappalli 620 024, India
5
Centre for Marine Science and Technology, M.S. University
Rajakkamankalam Kanyakumari District, India

ABSTRACT. Secondary metabolites of the green algae, Ulva fasciata, were tested to determine the efficacy
of controlling shrimp bacterial pathogens. Exploratory experiments indicated that an intermediate dose
(1 g kg-1 of shrimp) of Ulva in the diet was highly effective at controlling bacterial pathogens of shrimp, as
compared to lower (500 mg kg-1) and higher (1.5 g kg-1) doses. The pilot experiments evaluated the percent of
relative protection afforded shrimps treated with Ulva diet and faced with various concentrations of bacterial
pathogen. The survival of shrimps treated with Ulva diet was significant (P < 0.01). The present findings
indicate that the green U. fasciata may be an excellent source for developing a potent medicated feed for
shrimp disease management.
Keywords: Penaeus monodon, bacterial diseases, Vibrio, shell disease, proactive management, Ulva fasciata.

Eficacia del extracto del alga marina verde Ulva fasciata sobre el manejo de las
enfermedades bacterianas en camarones

RESUMEN. Metabolites secundario de algas verdes Ulva fasciata fue probado para determinar la eficacia de
controlar el camarn pathogens bacterial. Las conclusiones de experimentos exploratorios indicaron que la
dosis mediana (1 g kg-1 de camarn) de dieta Ulva era sumamente eficaz en el control de pathogens bacterial
de camarn cuando comparado al ms abajo (500 mg kg-1) y ms alto (1,5 g kg-1) dosis. En los experimentos
pilotos, la proteccin de pariente de por ciento de camarones trat con la dieta Ulva y desafi con varias
concentraciones de bacterial patgeno fueron evaluados. La supervivencia de camarones trat con la dieta
Ulva era significativo (P < 0,01). Basado en las conclusiones presentes, podra ser deducido que U. verde
fasciata puede ser una fuente excelente para desarrollar la comida potente medicinal para la direccin de
enfermedad de camarn.
Palabras clave: Penaeus monodon, enfermedades bacteriales, Vibrio, enfermedad de cscara, direccin
proactiva, Ulva fasciata.
___________________
Corresponding author: Aseer Manilal (aseermanilal@gmail.com)

INTRODUCTION (Karunasagar et al., 1997; Selvin & Lipton 2003a;

Bacterial disease outbreaks particularly vibriosis and
black shell disease impose a significant constraint on
the sustainable production of shrimp (Bachere et al.,
1995; Verschuere et al., 2000; Selvin et al., 2005;
Manilal et al., 2010b). In Asia, among the pathogenic
Vibrio group, 11 species were reported from the
shrimp culture systems (Lavilla-Pitogo, 1995). V.
alginolyticus and V. harveyi poses a serious disease
problem in cultured black tiger shrimp in India
Manilal et al., 2010b). Vibrio species are considered to
be members of the normal bacterial flora of shrimp
and the culture environment (Jiravanichpaisal et al.,
1994; Otta et al., 1999). Often acting as opportunistic
pathogens or secondary invaders, they may cause total
mortality of reared shrimps (Lightner, 1988; Nash et
al., 1992).
Although few reports evidenced the efficacy of
algae-based products in shrimp health management
(Furusawa et al., 1991; Yamasaki et al., 1997), the
198 Lat. Am. J. Aquat. Res.
role of marine natural product in shrimp disease
management has been realized recently (Selvin &
Lipton, 2003, 2004; Selvin et al. 2004b; Huang et al.,
2006; Manilal et al., 2009). It was found that marine
secondary metabolites are promising resources for the
development of eco-friendly management practices for
shrimp diseases (Selvin & Lipton, 2003; Selvin et al.,
2004, 2004b; Manilal et al., 2009, 2009a). Moreover,
secondary metabolites of green algae Ulva fasciata
elicited the non-specific defense factors of shrimp
against pathogenic invaders (Selvin, 2002; Selvin et
al., 2004b). In addition, medicated feed formulated
with polysaccharides isolated from the Indian green
algae, Acrosiphonia orientalis were found to be
effective in control of White Spot Syndrome Virus
(Manilal et al., 2009). Recently, Huang et al. (2006)
envisages the effect of Sargassum fusiforme
polysaccharide extracts on vibriosis resistance and
immune activity of the shrimp, Fenneropenaeus
chinensis.
Southwest coast of India is a unique marine habitat
infested with diverse variety of seaweeds. The
biological activity of seaweeds from the southwest
coast of India (Kollam coast) is already reported
(Manilal et al., 2009, 2009a, 2009b, 2010, 2010a,
2011, 2011a). In this background, the present study
aims to establish the effect of algal-based medicated
feed on the survival of experimentally infected
shrimps.
MATERIALS AND METHODS
Collection of marine algae
The mature plants of Ulva fasciata was handpicked
from the intertidal and subtidal habitat of the Kollam
(0854'N, 7638'E) area located on the southwestern
coast of India. The collection was performed during
the period from June 2007 to August 2007 when algal
biomass remains dominant. Live and healthy plants
were harvested manually and washed thoroughly in
running water. Cleaned plant materials were shade
dried under an air jet to prevent photolysis and thermal
degradation. The completely dried material was
weighed and ground coarsely in a mechanical grinder
(Manilal et al., 2010).
Extraction of algae
For extraction, 500 g of finely powdered algal material
was refluxed three times in a 5 L capacity round
bottom flask in a water bath at 65C for about 6 h
using dichloromethane: methanol (1:1) as a binary
azeotropic solvent (Manilal et al., 2009b). The
extracts were filtered and concentrated to recover the
excess solvents in another distillation system. The
concentrated extract (about 100 mL) was again filtered
through a Whatman N1 filter paper fitted with a
Buchner funnel using suction pressure.
Finally, it was reduced to thick oily natured crude
extract in a rotary vacuum evaporator (Yamato) at
40C, collected in airtight plastic vials and stored in
the refrigerator for further activity studies.
Determination of median lethal dose (MLD) of
algal extract
Primary exploratory (dose selecting) experiments were
conducted with broad range of the test compounds.
Chosen concentrations such as: 100, 1000 and 2000
mg kg-1 shrimp of U. fasciata extract were prepared in
5% EtOH in normal saline to ensure complete
solubility. Ten shrimps (abw = 8.5 g) per group
(triplicates) were injected intra-muscularly with 0.1
mL of appropriate dose or 5% EtOH in normal saline
(control). The immediate reflexes and mortality were
observed every hour for the first 6 h and every 24 h
for 7 days. Based on the exploratory experiments,
narrow ranges were administered to the experimental
shrimp to determine the median lethal dose (LD50).
Preparation of medicated diet
Top-coated medicated feed was prepared with
appropriate quantity of Ulva extract on the surface of
the feed at a rate of 3.2% of the shrimp body weight
daily. To prepare the medicated feed, 30, 60 and 80 g
of Ulva extract was incorporated in medicated diet.
The shrimp were fed with a commercially formulated
shrimp feed with the following proximate
composition: 35.6% crude protein, 3.5% lipids, 5.9%
fibre, 45.7% nitrogen-free extract and 11.21% ash.
Commercial pellet shrimp grower feed No. 1 (C.P.
feeds, Cochin) was used for preparing medicated feed
for the experiments on leaching of Ulva extract in the
water. The extract was dissolved in 50 mL of 4%
gelatin water and sprayed on 1 kg of pellet feed using
a TLC sprayer. The sprayed medicated feed was dried
in a hot air oven at 40C.
Pathogenicity and LD50 value of shrimp pathogens
Initially, the slant culture of shrimp pathogens (V.
fischeri, V. alginolyticus, V. harveyi and Aeromonas
sp.) was activated and 1 mL of 18 h culture was
inoculated in 25 mL nutrient broth. This was kept
overnight at 30 2C in a shaker at 180 5 rpm. An
18 h shake culture was centrifuged at 4800 x g for 15
min at 40C (Eppendorf). Cell pellets were washed
twice with normal saline (NS), re-suspended and
 Efficacy of marine green alga Ulva fasciata
serially diluted in NS and enumerated using a Petroff-
Hausser counting chamber by plating on nutrient agar
supplemented with 2% NaCl (Himedia). This was also
plated on nutrient agar to get the colony forming units
(cfu) values. The black tiger shrimp Penaeus monodon
post-larvae (PL-20) obtained from the Matsyafed
hatchery, Kollam and were reared in a 1000 L fiber
reinforced plastic tanks provided with constant
aeration and 50% daily water exchange. They were
reared at optimum hydrological conditions such as
salinity (35 ppt), temperature (30 2C) and pH (7.8).
Healthy juveniles (average body weight = 5.4 2.2 g)
were segregated and maintained at 20 shrimps/tank in
200 L high-density plastic (HDP) tanks before starting
the experiment. The challenged shrimps were
maintained at 10 shrimps/tanks in glass aquaria.
Shrimps were intramuscularly injected with 0.1 mL of
bacterial inoculums using a 1 mL tuberculin syringe at
ventral side between the second and third segment.
Preliminary examinations revealed that challenge dose
of 103 colony forming unit (cfu) per shrimp could not
kill the injected shrimp (Manilal et al., 2010b).
Therefore the concentrations of 105 to 108 cfu of the
appropriate single (V. fischeri, V. alginolyticus, V.
harveyi and Aeromonas sp.) and combined culture (V.
alginolyticus + V. harveyi) of bacteria per shrimp were
used. Parallel control groups received 0.1 mL of
normal saline (NS) only. Ten shrimps were used for
each inoculation level. The mortality and reflexes of
the shrimps were observed for every 15 min in the
first hour of post-inoculation and every 1 h until the
6th h (Manilal et al., 2010b). Subsequent monitoring
was done every 12 h for a period of seven days
(Tendencia & Dureza, 1997). The appropriate
concentration of pathogens (105 to 108 cfu), which
causes mortality within 24 h or within 7 days, was
considered as LD50 whereas which causes infection or
abnormalities was considered as ID50 (Infectivity
Dose) (Manilal et al., 2010b). The LD50 dose was
calculated by the probit method, after Wardlaw
(1985).
Effect of different dose of algal extracts in the
survival of experimentally infected shrimps
The shrimps with an average body weight of 5.6 1.8
g range were reared in the circular high density plastic
(HDP) tanks at a stocking density of 60 individuals
per 600 L of seawater. They were fed with Ulva diet
(1 g kg-1 shrimp) in three equal installments at a rate
of 3.2% of their body weight for a period of 15 days.
On the 16th day, three duplicate groups each of treated
shrimps (10 numbers/group) were grouped in to three
and intramuscularly injected with LD50 (106
199
cfu/shrimp) challenge dose and higher challenge dose
(107 to 108 cfu/shrimp) of single culture of bacterial
pathogens such as V. fischeri, V. harveyi, V. algino-
lyticus and Aeromonas sp., and combined culture of
pathogen (V. harveyi, 5 x 105 + V. alginolyticus, 5 x
105 = 106 cfu/shrimp) and transferred to the 100 L
glass aquaria. They were observed for a period of 15
days for mortality and external clinical symptoms
(Austin & Austin, 1989). The Ulva diet was continued
after challenge for 15 days. Parallel control shrimps
(10 numbers) received 0.1 mL normal saline only. The
mortality/infectivity percentages were estimated
according to Sung et al. (1994). The Percent Relative
Protection (PRP) was determined by the following
expression:
% of mortality (treated)
PRP = 1- x 100
% of mortality (control)
To determine if significant differences existed
between the treated and control shrimps, all results
were analyzed using ANOVA. The significant
differences were indicated at P < 0.01.
RESULTS
The Median Lethal Dose (MLD) of Ulva extract in P.
monodon was determined to be 1120 mg kg-1 shrimp.
During the preliminary experiment, the infection
(pathogenicity range) was obtained at a higher dose of
108 cfu/shrimp after 5 days of inoculation with
luminescent V. fischeri type culture. The LD50 values
of bacterial pathogens were ranged as 2.8 x 107
cfu/shrimp for V. fischeri and 106 cfu/shrimp for V.
harveyi, V. alginolyticus and Aeromonas sp. The
external clinical symptoms were characterized as
shell necrosis and black spots on the shell,
necrotised chelate legs, anorexia, feeble movement
and mortality.
The effect of different algal extracts in the survival
of experimentally infected shrimp is presented in
Table 1. The shrimp fed with the dose rate of 500-mg
kg-1 shrimp had the lowest protection against bacterial
infection. At this dose, the shrimp challenged with V.
fischeri produced infection in 60% of challenged
shrimp, whereas the shrimp challenged with V.
harveyi and V. alginolyticus caused infection to the
extent of 80%. The experimental group, fed with
median (1 g kg-1 shrimp) and higher (1.5 g kg-1
shrimp) doses of medicated feed exhibited more or
less similar level of protection. At these treatment
levels, no mortality was noticed in the shrimps
challenged with V. harveyi and Aeromonas sp.
whereas V. fischeri and V. alginolyticus caused 20%
200 Lat. Am. J. Aquat. Res.
Table 1. Efficacy of Ulva diet on protection and survival of experimentally infected Penaeus monodon.
Tabla 1. Eficacia de Ulva dieta sobre la proteccin y la supervivencia experimentalmente se infectan Penaeus monodon.
Percentage of infection within 15 days*
Medicated feed dose rate (g kg-1)
V. fischeri
0.5 60
1.0 20
1.5 10
*100% mortality was observed in the control treatments
infection. The infected shrimps showed external
clinical symptoms such as shell necrosis and black
spots on the shell. Subsequent symptoms such as
necrotised chelate legs, anorexia, feeble movement
were culminated in mortality, particularly in control
and lower treatments. Based on these findings, it could
be envisaged that shrimp fed with 1 g kg-1 will provide
high protection compared to other doses.
The survival rate of treated and control shrimp
against various bacterial pathogens is depicted in
Figures 1 to 4. The shrimps challenged with
potentiated pathogen produced more infection or
mortality in the treated group than those caused by the
LD50 value of individual pathogen. In the case of V.
fischeri, the LD50 did not cause mortality in the treated
group while all the control shrimp died (Fig. 1). Ulva
diet elicited significant survival (60 in terms of PRP)
against the lethal dose (108 cfu/shrimp) of V. fischeri.
However 20% infection was observed among the
surviving shrimp of Ulva fed group (Table 2). The
Ulva diet elicited complete protection (100% survival)
against the infection of V. harveyi and V.
alginolyticus. The inoculation of a higher dose (107
cfu/shrimp) of Aeromonas sp. caused 40% infection in
the Ulva treated group (Table 2). It was found that the
Ulva diet produced a higher level of protection (80%
survival) against the infection caused by the combined
pathogens. Invariably, the survival of treated shrimp
against the bacterial infection was significant at P <
0.01 level (Table 2).
DISCUSSION
Based on the findings, shrimp fed with Ulva-based
medicated feed at a dose rate of 1 g kg-1 could
effectively control the bacterial pathogens challenged
in this study. Invariably the shrimp treated and
challenged subsequently with the LD50 of appropriate
bacteria gave higher survival than the control group.
In the control group, early high mortality was
observed than the actual LD50. It may be due to the
V. alginolyticus V. harveyi Aeromonas sp.
80 80 40
20 0 0
20 10 0
enhanced virulence obtained by the pathogenic
isolates passed through the host, prior to the in
captivity control experiments. The treated group
challenged with higher dose (107 to 108 cfu/shrimp) of
bacterial inoculum had low survival. The survival rate
of Ulva treated shrimp was 100% against the infection
caused by the shrimp bacterial pathogens. Selvin et al.
(2004b) reported that inhibition of bacterial
propagation was a possible mechanism by which Ulva
medication provided protection from infection.
Shrimp disease management using Ulva diet was
proven to be an effective eco-friendly management
strategy for sustainable shrimp farming (Selvin, 2002;
Selvin & Lipton, 2003). Ulva diet was found to be a
potent immunomodulator and therefore it was
considered as a proactive drug (Selvin et al., 2004b).
As per our earlier finding, 88% of viable V. fischeri
cells were cleared-off from the haemolymph within 1
h in the Ulva treated group. These findings suggest the
quick production of bactericidins in the haemolymph
of Ulva treated group. The rapid bacterial clearance
rate of shrimp haemocytes was stimulated by Ulva
treatment. Therefore it was conjectured that
bacteridins found in shrimp plasma might be inducibly
released from haemocytes by Ulva medication.
Recently Huang et al. (2006) reported the effect of
seaweed Sargassum fusiforme polysaccharide extracts
on vibriosis resistance and immune activity of the
treated shrimp. Literature also evidenced the in vivo
antiviral (WSSV) potency of seaweed-based
medicated feed in Penaeus monodon (Manilal et al.,
2009). Satoh et al. (1987) investigated the effect of
Ulva on susceptibility of infectious disease in red sea
bream Pagrus major fed with 5% Ulva pertusa meal
supplementation diet. The Ulva meal increased the
resistance against infection caused by Pasteurella
piscicida. A spray-dried preparation of micro-algae
Tetraselmis suecica was reported to control a variety
of fish pathogens such as A. salmonicida,
Staphylococcus liquifaciens, V. anguillarum, V.
salmonicida and V. ruckeri (Austin & Day, 1990).
 Efficacy of marine green alga Ulva fasciata 201

Control inoculated with 10E+8 cfu/shrimp

Control inoculated with 10E+7 cfu/shrimp

Treated inoculated with 10E+7 cfu/shrimp

Treated inoculated with 10E+8 cfu/shrimp

Figure 1. Survival of shrimp fed with and without Ulva incorporated medicated diet following challenge with V. fischeri.
Figura 1. Supervivencia de camarones alimentados con y sin Ulva incorporada como dieta medicinal para combatir el
Vibrio fischeri.

Control inoculated with 10E+6 cfu/shrimp of

V. harveyi

Ulva inoculated with 10E+6 cfu/shrimp of

V. harveyi

Ulva inoculated with 10E+6 cfu/shrimp of

V. alginolyticus

Control inoculated with 10E+6 cfu/shrimp of

V. alginolyticus

Figure 2. Survival of shrimp fed with and without Ulva incorporated diet following challenge with Vibrio sp.
Figura 2. Supervivencia de camarones alimentados con y sin Ulva incorporada a dietas para combatir el Vibrio sp.

Control inoculated with 10E+7 cfu/shrimp

Control inoculated with 10E+6 cfu/shrimp

Treated inoculated with 10E+7 cfu/shrimp

Treated inoculated with 10E+6 cfu/shrimp

Figure 3. Survival of shrimp fed with and without Ulva incorporated medicated diet following challenge with Aeromonas
sp.
Figura 3. Supervivencia de camarones alimentados con y sin Ulva incorporada a dietas medicinales para combatir
Aeromonas sp.
202 Lat. Am. J. Aquat. Res.

Control inoculated with 10E+7 cfu/shrimp

Ulva inoculated with 10E+7 cfu/shrimp

Figure 4. Survival of shrimp fed with and without Ulva diet following combined pathogenic challenge (V. harveyi and V.
alginolyticus).
Figura 4. Supervivencia de camarones alimentados con y sin Ulva en dietas para combatir en forma combinada (V.
harveyi y V. alginolyticus).

Table 2. Efficacy of Ulva diet (1000 mg kg-1) on the percent relative protection (PRP) of Penaeus monodon against
bacterial infections.
Tabla 2. Eficacia de la dieta de Ulva (1000 mg kg-1) sobre el porcentaje de proteccin relativa de Penaeus monodon
contra las infecciones bacterianas.

Dose Cumulative Mortality within % shell necrosis in the

Bacterial pathogens PRP
(cfu/shrimp) 15 days (%)*(Treated n = 20) treated shrimp (n = 20)
V. fischeri 108 40 60 20
107 0 100 0
V. harveyi 106 0 100 0
V. alginolyticus 106 0 100 0
Aeromonas sp. 107 0 100 40
106 0 100 0
Combined pathogen 106 20 80 0
i. V. harveyi, 5 x 105
ii. V. alginolyticus 5 x 105
*Based on the cumulative mortality the calculated survival rate was significant at P < 0.01.
100% mortality was observed in the control treatments, except Aeromonas sp. which was 80%

Based on the present study, therapeutic formulation
(Ulva diet) can be easily prepared with crude extract.
Therefore purification strategies and consequent
synthetic analogue development process need not be
undertaken. As the extract was prepared from the
dried material, such source material can easily be
stored for 12 months. To sustain the host-defense
system and relative protection against pathogenic
invaders, the Ulva medication can be used as a
prophylactic agent for the entire culture period at low
cost. Based on the present findings, it could be
inferred that the secondary metabolites of U. fasciata
form an excellent source for developing potent
formulations as a package of proactive management
practice for sustainable shrimp farming.
ACKNOWLEDGEMENTS
The author Aseer Manilal is gratefully acknowledged
Council of Scientific and Industrial Research (CSIR),
New Delhi for providing Senior Research Fellowship.
This work is funded by Department of Biotechnology,
New Delhi (BT/PR8064/AAQ/03/290/2006).
 Efficacy of marine green alga Ulva fasciata
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Lat. Am. J. Aquat. Res., 39(2): 205-213, 2011 Anchovy feeding in an estuarine front, Argentine 205
DOI: 10.3856/vol39-issue2-fulltext-2

Research Article

Importance of the Ro de la Plata estuarine front (southwestern Atlantic Ocean)

in the feeding ecology of Argentine anchovy, Engraulis anchoita
(Clupeiformes, Clupeidae)

Luciano N. Padovani1,2,3, Mara D. Vias1,2,3 & Marcelo Pjaro1

1
Instituto Nacional de Investigacin y Desarrollo Pesquero, P.O. Box 175, B7602HSA
Mar del Plata, Argentina
2
Consejo Nacional de Investigaciones Cientficas y Tcnicas, P.O. Box 175, B7602HSA, Argentina
3
Universidad Nacional de Mar del Plata, P.O. Box 175, B7602HSA, Argentina

ABSTRACT. The feeding of Engraulis anchoita was studied in the coastal reproductive habitat of the
northern population during the spawning period. Stomach contents of anchovy adults and plankton samples
taken during a research cruise were examined. The highest stomach fullness values were found in the Rio de la
Plata estuary, particularly at stations close to the surface salinity front. Copepods, particularly those < 1 mm
total length, represented by Paracalanus spp. and Oithona spp., were the most abundant prey. The dominance
of small copepods in the Argentine anchovy diet is noted for the first time. Ecological implications of this fact
are discussed. Other abundant preys were appendicularians, cladocerans, and fish eggs. The species
composition of the zooplankton samples coincided roughly with that found in the stomach contents. However,
selective feeding was observed on preys > 1 mm total length. This might be explained by a low gill rakers
efficiency of adult anchovies to retain small prey. In the Rio de la Plata front, both the reported large
biomasses of zooplankton and the observed intense anchovy feeding revealed the ecological significance of
this front, especially when compared with the contiguous poor in food coastal areas.
Keywords: Engraulis anchoita, feeding, stomach content, estuarine front, copepods, southwestern Atlantic,
Argentina.

Importancia del frente estuarial del Ro de la Plata (Ocano Atlntico sudoccidental)

en la ecologa trfica de la anchota argentina, Engraulis anchoita
(Clupeiformes, Clupeidae)

RESUMEN. Se estudi la alimentacin de la poblacin nortea de Engraulis anchoita en el hbitat

reproductivo costero durante su periodo de desove. Se analizaron los contenidos estomacales de adultos de
anchota y muestras de zooplancton tomados durante un crucero de investigacin. Los mayores valores de
replecin estomacal se encontraron en el estuario del Ro de la Plata, particularmente en estaciones cercanas al
frente salino de superficie. Los coppodos fueron las presas ms abundantes, particularmente especmenes < 1
mm de longitud total, representados por Paracalanus spp. y Oithona spp. Este dominio de pequeos
coppodos en la dieta de la anchota argentina se destaca por primera vez. Se discutieron las implicancias
ecolgicas de este hecho. Otras presas abundantes fueron: apendicularias, cladceros y huevos de peces. La
composicin de especies en las muestras de zooplancton coincidi a grandes rasgos con las encontradas en los
contenidos estomacales. Sin embargo, se observ seleccin sobre presas > 1 mm de longitud total. Esto se
puede explicar por la baja eficiencia del aparato branquial de anchotas adultas para retener pequeas presas.
En el frente del Ro de la Plata, las altas biomasas de zooplancton reportadas y la intensa alimentacin
observada, evidencian su significancia ecolgica, especialmente cuando se compara con aguas costeras
adyacentes pobres en alimento.
Palabras clave: Engraulis anchoita, alimentacin, contenido estomacal, frente estuarial, coppodos, Atlntico
sudoccidental, Argentina.
___________________
Corresponding author: Luciano Padovani (lucianopadovani@inidep.edu.ar)
206 Lat. Am. J. Aquat. Res.
INTRODUCTION
Engraulis anchoita is the most abundant and wide-
spread pelagic fish in the southwest Atlantic. It plays a
key role in the pelagic ecosystem of the Argentine
Sea, being an important component in the diet of
commercial species such as hake, squid and mackerel
(Angelescu, 1982). Two distinct populations are rec-
ognized south of 34S: the northern stock, between 34
and 41S; and the Patagonian stock between 41 and
48S (Hansen et al., 1984). The northern stock, object
of this study, performs seasonal migrations between
coastal and shelf waters. In spring and early summer
the schools migrate into the coastal reproductive habi-
tat (hereafter CRH) off the Buenos Aires Province (<
50 m depth), where massive spawning takes place
(Snchez & Ciechomski, 1995). Larvae and juveniles
remain in coastal waters during their growing period.
After spawning, in summer and early autumn, schools
disperse into outer shelf waters to feed, accumulating
a large amount of energy for the next reproductive
cycle (Angelescu, 1982; Hansen & Madirolas, 1996).
E. anchoita adults are opportunistic predators on
meso and macrozooplankton. They exhibit, like other
engraulids, two different feeding mechanisms: filtra-
tion for smaller prey, and capture or biting for larger
ones (Leong & OConnell, 1969; Angelescu, 1982).
Previous studies indicate that anchovy feeding in
the CRH was negligible when compared with the in-
tense feeding occurring in shelf waters (Angelescu &
Anganuzzi, 1981; Angelescu, 1982; Schwingel &
Castello, 1994; Capitanio et al., 1997; Pjaro, 2002).
In the former, individuals feed almost exclusively on
small zooplankters (e.g. small copepods species, ap-
pendicularians and cladocerans) while in shelf waters
large zooplankters constitute their food (e.g. Calanidae
copepods, euphausiids and hyperiid amphipods). This
feeding pattern seems to reflect the food availability
found in zooplankton studies with lower biomass in
the CRH than in shelf waters (Pjaro, 2002; Vias et
al., 2002; Marrari et al., 2004). However, in northern
sector of the CRH high zooplankton biomasses have
been reported (Vias et al., 2002; Marrari et al.,
2004). This sector is strongly influenced by the Rio de
la Plata (RdP), the second most important river of
South America. Its estuarine front plays a central role
in the biological production, and zooplankton aggrega-
tions are a recurrent feature in this area probably be-
cause of retention and accumulation process (Madi-
rolas et al., 1997; Acha et al., 2008).
The presence of zooplankton aggregations together
with the fact that high densities of anchovy schools
occur frequently in RdP front (Hansen & Madirolas,
1996; Martos et al., 2005) suggest that this may be a
potential anchovy feeding area into the CRH. This is
not surprising since other estuarine fronts in the world
have been related to important anchovy spawning and
feeding grounds (Palomera, 1992; Motos et al., 1996;
Peebles, 2002). However, previous studies in the CRH
have not been addressed to this question. Moreover,
the characterization of anchovy diet (e.g. taxonomic
identification and quantification of ingested prey
items) was inaccurate in these studies, especially re-
garding small prey.
In this work, anchovy stomach contents were
analysed in order to assess differences in the feeding
activity between RdP front and the rest of the CRH.
Characterization of anchovy diet in the CRH was
carried out and prey composition in stomach contents
was compared with the prey availability in the field.
MATERIALS AND METHODS
Study site
Subantarctic coastal waters of the Buenos Aires
Province (< 50 m depth) are vertically homogeneous
all over the year because they are mixed by winds and
tides. They are poorer in nitrate and less productive
than subantarctic shelf waters (> 50 m depth) which
are stratified during the warmer season. Both are
separated by a semi-permanent temperature front
(Carreto et al., 1995). North of 38S the coastal waters
are modified by the RdP estuary (Fig. 1). This
estuarine front shows a high primary productivity,
driven by the nutrient input from the river and by the
vertical stability of the water column (Carreto et al.,
1986). It is characterized by a salt wedge structure and
strong horizontal salinity gradients. More saline and
dense marine waters penetrate into the estuary on the
bottom, whereas more dilute and less dense river
waters flows toward the sea at the surface (Guerrero et
al., 1997). The estuarine dynamics and the strong
pycnoclines of the salt wedge would favor the
accumulation and retention of plankton (Acha et al.,
2008).
Sample collection, treatment and data analysis
The material used in this study was obtained on board
the R/V Oca Balda on a cruise performed in coastal
areas of the Buenos Aires Province between 34 and
41S (Fig. 1). The sampling period (16 October-2
November 2004) was coincident with the peak of
anchovy spawning in the study area (Snchez &
Ciechomski, 1995).
Oceanographic data were obtained in 70 stations
with a CTD system (Kiel Multisonde Compact Sys-
tem, ME Meerestechnik Elektronic, Kiel, Germany).
The salinity CTD data were calibrated by salinometer
 Anchovy feeding in an estuarine front, Argentine
Figure 1. Study area and location of the sampling
stations. (X) trawls, (O) zooplankton. Dashed line
divides northern and southern sectors of study area
(38S).
Figura 1. rea de estudio y ubicacin de las estaciones
de muestreo. (X) lances de pesca, (O) zooplancton. La
lnea de guiones divide los sectores norte y sur del rea
de estudio (38S).
measurements of discrete water samples. Surface sa-
linity distribution was drawn to locate the RdP estua-
rine front.
Anchovies were collected using a Nichimo midwa-
ter trawl net with a 10 mm mesh size and immediately
fixed in 10% formaldehyde. Stomach contents of 240
adult fishes of both sexes (110 to 194 mm total length)
randomly selected from sixteen trawl stations (n = 15
per trawl) were examined (Fig. 1). Tows were per-
formed both during the day and night (Table 1). Each
stomach was weighed with and without food content
in order to determine the weight of the ingested prey,
expressed as the difference between both weights. To
assess the feeding activity, mean Stomach Fullness
Index (mSFI) was calculated for each trawl as the
ratio between ingested prey and whole animal
weights. According to Angelescu (1982), this index
indicates the stage of satiety and ranges from empty
stomach (< 0.5% of anchovy total weight) to full
stomach (> 6% of anchovy total weight).
Anchovies and stomachs were weighed using a
digital balance to nearest 0.01 g. No correction was
applied to the weight values for fixation effect on the
individuals. The dilated stomachs found empty for
regurgitation during trawling, were discarded.
207
Zooplankton samples (n = 13) were collected with
a 200 m meshed 61 cm diameter Bongo net, using
oblique tows in the whole water column (Fig. 1). The
samples were fixed in 4% formaldehyde.
In the laboratory, both zooplankton and stomach
content samples were sub-sampled into aliquots in
order to quantify the zooplankters. The individuals
were identified to the lowest possible taxonomic level
and their total length (TL) was measured. They were
placed in three size classes, < 1 and 1-2 mm TL for the
mesozooplankton and > 2 mm TL for the macrozoo-
plankton.
Anchovy feeding selectivity in relation to food
availability was calculated as the alpha selectivity
index (i) of Chesson (1978), using the formula:
where; ri = the percentage of food item i in the stom-
ach content; pi = the percentage of the same item in
zooplankton; n = the total number of food items as-
sessed.
RESULTS
Hydrography
Surface salinity values in the study area were ranged
between 19.5 and 33.9 (Fig. 2). The lowest values
corresponded to the RdP estuary. The isohaline of 30,
considered the boundary of estuarine waters (Guer-
rero, 1998), showed a south-eastward extension indi-
cating a river discharge in this direction whose influ-
ence reaches 3750S. A well-defined frontal zone was
observed with highest salinity gradients south of Sam-
borombn Bay. In the rest of the study area, out of the
river influence, the salinity values were above 33.
Feeding index
Mean Stomach Fullness Index (mSFI) of anchovy in
the CRH showed a well-defined pattern with the four
highest values located in RdP frontal area (Fig. 2).
This highest values were observed in specimens
collected from trawl stations close to the surface salin-
ity front, (away from the 30 isohaline): station N4
(mSFI: 2.49), N5 (mSFI: 2.01), N7 (mSFI: 1.34) and
N8 (mSFI: 1.33). Some individuals reached SFI val-
ues about 6, which mean a full stomach. In the re-
maining stations, the mSFI were smaller than 1.00
indicating empty or partially empty stomachs.
Prey composition
The total bulk of anchovy diet was made up of zoo-
plankton (Table 1). Mesozooplankton < 1 mm TL fol
208 Lat. Am. J. Aquat. Res.

Calanoida copepodites) and to a lesser extent by

Figure 2. Mean Stomach Fullness Index (mSFI) of
Engraulis anchoita adults at each trawling position in
relationship with surface salinity distribution. Isohaline
30 is shown thicker.
Figura 2. ndice de Replecin Estomacal promedio
(IREp) de adultos de Engraulis anchoita para cada lance
de pesca en relacin con la distribucin de salinidad
superficial. La isohalina de 30 se muestra engrosada.
appendicularians. Anchovy eggs and unidentified fish
eggs were less numerous. The least abundant
macrozooplankton > 2 mm was dominated by decapod
larvae and the Calanoides carinatus copepod.
From the application of the feeding selectivity
index to different prey size classes, high selectivity
was observed for mesozooplankton 1-2 mm TL and
macrozooplankton > 2 mm TL at the expense of
mesozooplankton < 1 mm (Fig. 3a). Furthermore,
unidentified fish eggs showed high index in the
northern sector of the study area (north of 38S) while
the appendicularians were in the southern part (south
of 38S) (Fig. 3b); what happened due to the high
number of specimens found in stomach from stations
4 and 12 for unidentified fish eggs and appendicu-
larians respectively (Table 1).
DISCUSSION
High feeding activity was detected in anchovies
from the proximity of RdP surface salinity front, in
contrast with a lower activity recorded in the rest of
the CRH. Moreover, it is worth mentioning that during
the cruise high anchovy biomasses were recorded in

lowed by the 1-2 mm TL fraction were dominant.

Copepods were the most important group reaching
almost 50% of prey items (PI). Other important groups
were appendicularians (22.1% PI), cladocerans
(14.7% PI), represented by Evadne nordmanni and
Podon spp., and fish eggs (12.6% PI), including
unidentified fish eggs and anchovy eggs. To a lesser
extent veliger stages of lamellibranchs, unidentified
nauplii, decapod larvae and amphipods were found.
The more abundant copepods in stomachs
belonged to the < 1 mm TL fraction (Paracalanus spp.
+ Calanoida copepodites and Oithona spp.). Copepods
size class 1-2 mm TL (Ctenocalanus vanus,
Clausocalanus brevipes, Centropages brachiatus +
Calanoida copepodites) was less abundant and
individuals > 2 mm TL (Calanoides carinatus) were
fairly rare.

Zooplankton composition and food selectivity

Mesozooplankton < 1 mm TL fraction was the most
abundant in study area (Table 2). Copepods
(Paracalanus spp. + Calanoida copepodites and
Oithona spp.) constituted the bulk of this fraction
followed by cladocerans (Evadne nordmanni and
Podon spp). The 1-2 mm TL size class was
represented by copepods (Ctenocalanus vanus,
Clausocalanus brevipes, Centropages brachiatus +
Figure 3. Feeding selectivity index values according to
Chesson (1978). a) prey size classes; b) main anchovy
prey items (north and south of 38S).
Figura 3. Valores del ndice de selectividad de Chesson
(1978). a) por clases de tamao de presa; b) por
principales tems presa (al norte y sur de 38S).
Table 1. Stomach contents of Engraulis anchoita adults in its coastal reproductive habitat (CRH). Average number of specimens of each prey item from each trawl is
indicated. (n: number of anchovies examined). * Ctenocalanus vanus, Clausocalanus brevipes, Centropages brachiatus and Calanoida copepodites.
Tabla 1. Contenido estomacal de adultos de Engraulis anchoita en su hbitat reproductivo costero (HRC). Se indica el nmero promedio de especimenes de cada tem presa
para cada lance. (n: nmero de anchotas analizadas) * Ctenocalanus vanus, Clausocalanus brevipes, Centropages brachiatus y copepoditos de Calanoida.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
Trawl Total
(n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15) (n=15)
Time 10:57 10:35 20:14 23:55 8:34 20:51 22:53 20:44 0:27 16:35 16:16 18:47 10:19 20:57 10:40 18:08
Mesozooplankton (< 1 mm) 49.50 242.71 108.75 199.24 1259.24 112.03 179.29 87.65 143.16 55.22 136.33 1020.11 61.50 1813.81 87.89 606.67 6163.08
Copepods 44.05 206.43 99.75 159.41 1083.24 29.92 149.18 53.62 80.77 45.11 81.66 805.91 38.83 775.16 86.82 536.33 4276.20
Euterpina acutifrons 13.85 0.89 2.01 1.06 14.26 0 5.92 0 0.83 0.91 3.19 0.07 0.67 0 0 1.12 44.80
Oithona spp. 8.50 92.38 19.71 117.03 733.14 12.91 48.70 29.68 38.78 9.94 29.23 155.20 6.17 422.77 68.67 71.86 1864.66
Paracalanus spp. +
Calanoida copepodites 21.70 113.15 78.03 41.31 335.84 17.02 94.56 23.94 41.16 34.26 49.24 650.63 32.00 352.40 18.15 463.35 2366.73
Unidentified nauplii 0 1.89 0.33 10.17 0 0.22 1.33 0.33 1.33 0.56 0.50 0 0.50 0 0 0 17.16
Cladocerans 0.95 28.20 1.67 27.33 120.33 78.67 14.78 30.72 50.33 7.17 52.83 214.20 21.50 1038.64 1.07 70.33 1758.72
Evadne nordmanni 0 17.00 0.56 16.17 65.89 55.83 4.83 11.79 37.51 2.33 13.54 180.93 0.35 531.89 0 9.07 947.69
Podon spp. 0.95 11.20 1.11 11.16 54.44 22.84 9.95 18.93 12.82 4.84 39.29 33.27 21.15 506.75 1.07 61.26 811.03
Veliger stages of
Lamellibranchs 4.50 6.20 7.00 2.33 55.67 3.22 14.00 2.97 10.72 2.39 1.33 0 0.67 0 0 0 111.00
Mesozooplankton (1-2 mm) 3.50 133.74 24.85 1202.98 253.76 31.30 141.41 93.40 51.34 35.53 36.29 3114.25 19.00 280.82 26.64 46.98 5495.77
Copepods* 2.05 7.99 20.51 9.65 77.76 1.41 35.07 27.96 11.90 3.80 16.12 980.58 3.00 131.33 0.71 33.31 1363.16
Fish eggs 0.50 2.73 2.33 1192.17 24.67 10.11 7.11 43.05 5.94 0.33 19.17 0 15.67 142.82 24.60 7.33 1498.54
Anchovy eggs 0 1.93 0.67 132.33 24.67 10.11 7.11 41.76 5.94 0.33 19.17 0 15.33 142.82 17.46 7.33 426.97
Unidentified fish eggs 0.50 0.8 1.66 1059.84 0 0 0 1.29 0 0 0 0 0.34 0 7.14 0 1071.57
Appendicularians 0.95 123.01 2.00 1.17 151.33 19.78 99.22 22.39 33.50 31.39 1.00 2133.67 0.33 6.67 1.33 6.33 2634.07
Anchovy feeding in an estuarine front, Argentine

Macrozooplankton (> 2 mm) 0 0 1 1.55 0 0 3 235 0 0 1 20 0 9 0 1 272.42

Copepods 0 0 0.40 0.21 0 0 2.96 234.00 0 0 0.93 20.37 0 2.59 0 0.22 261.69
Calanoides carinatus 0 0 0.40 0.21 0 0 2.96 234.00 0 0 0.93 20.37 0 2.59 0 0.22 261.69
Decapod larvae 0 0.47 0.33 1.33 0 0.33 0.22 0.44 0 0 0 0 0 6.67 0 0.80 10.60
Amphipods 0 0 0 0 0 0 0 0.07 0.07 0 0 0 0 0 0 0 0.13

Total 53.00 376.92 134.33 1403.77 1513.00 143.66 323.88 415.56 194.56 90.74 173.54 4154.73 80.50 2103.88 114.53 654.67 11931.28

Copepods (%) 86.98 56.89 89.83 12.06 76.73 21.81 57.80 75.94 47.63 53.90 56.88 43.49 51.97 43.21 76.43 87.05 49.46
Appendicularians (%) 1.79 32.64 1.49 0.08 10.00 13.77 30.63 5.39 17.22 34.59 0.58 51.36 0.41 0.32 1.16 0.97 22.08
Cladocerans (%) 1.79 7.48 1.24 1.95 7.95 54.76 4.56 7.39 25.87 7.90 30.44 5.16 26.71 49.37 0.93 10.74 14.74
Fish eggs (%) 0.94 0.73 1.74 84.93 1.63 7.04 2.20 10.36 3.06 0.37 11.04 0 19.46 6.79 21.48 1.12 12.56
209
210 Lat. Am. J. Aquat. Res.

Table 2. Taxonomic composition and abundance (ind m-3) of zooplankton in coastal reproductive habitat (CRH) of
anchovy. (SD: standard deviation). *Ctenocalanus vanus, Clausocalanus brevipes, Centropages brachiatus and
Calanoida copepodites.
Tabla 2. Composicin taxonmica y abundancia (ind m-3) de zooplancton en el hbitat reproductivo costero (HRC) de la
anchota (SD: desviacin estndar). *Ctenocalanus vanus, Clausocalanus brevipes, Centropages brachiatus and
Calanoida copepodites.

Taxa Mean SD Abundance range

Mesozooplankton < 1 mm 988.92 1233.54 134.23 - 4546.16
Copepods 736.61 1164.65 61.13 - 4408.57
Euterpina acutifrons 10.38 34.42 0 - 124.77
Oithona spp. 156.10 154.92 13.37 - 518.67
Paracalanus spp. + Calanoida copepodites 570.13 1107.14 46.98 - 4173.52
Unidentified nauplii 27.20 68.94 0 - 254.44
Cladocerans 212.08 324.92 2.44 - 1206.41
Evadne nordmanni 130.83 235.38 0 - 820.55
Podon spp. 81.25 115.03 0 - 385.86
Veliger stages of Lamellibranchs 13.03 22.74 0 - 74.52
Mesozooplankton 1-2 mm 144.42 116.86 25.84 - 396.03
Copepods* 76.92 86.97 3.25 - 286.64
Fish eggs 9.88 11.50 0 - 33.76
Anchovy eggs 9.59 11.05 0 - 31.93
Unidentified fish eggs 0.29 0.56 0 - 1.83
Appendicularians 57.63 87.41 0 - 327.77
Macrozooplankton > 2 mm 7.81 13.36 0.58 - 50.31
Copepods 1.52 2.83 0 - 10.7
Calanoides carinatus 1.52 2.83 0 - 10.7
Decapod larvae 1.97 5.69 0 - 20.80
Amphipods 0.04 0.09 0 - 0.27
Chaetognaths 3.30 4.91 0 - 16.88
Pteropods 0.97 3.39 0 - 12.23

this area (Hansen, 2004), which agrees with the cited
preference of this species for salinity frontal regions
(Martos et al., 2005).
Although the low number of samples does not
allow to be conclusive, these results support the
hypotheses that this area could be a preferred site of
intense food intake by anchovy within less productive
coastal waters.
The different time of the day when samples were
collected might reduce the significance of this finding,
taking into account that a diel feeding cycle has been
described for E. anchoita (Angelescu, 1982).
However, this cycle was observed mainly in shelf
waters where two periods of feeding activity at sunset
and sunrise were reported. On the contrary, in the
CRH this pattern was weak probably due to lower
food availability. Under these conditions of limited
food availability an extended feeding period has been
observed in E. anchoita and several other anchovy
species (Angelescu, 1982; Tudela & Palomera, 1997;
Pjaro, 2002).
In this study, most of items ingested by anchovies
belonged to < 1 mm and 1-2 mm TL mesozooplankton
fractions. According to Angelescu (1982), these prey
size (< 2 mm) would correspond to a filtration feeding
mechanism in argentine anchovy. The prey spectrum
found is in accordance with the taxonomic groups
mentioned by other authors in the CRH where the
copepods were the main prey of anchovy followed by
appendicularians and cladocerans (Capitanio et al.,
1997; Mianzan et al., 2001; Pjaro et al., 2007).
However, the large incidence of small copepods (<
1 mm TL) in Argentine anchovy diet is highlighted in
this work because they were, for the first time,
accurately identified and quantified. These results
agree with those frequently reported for European
 Anchovy feeding in an estuarine front, Argentine
anchovy (Tudela & Palomera, 1997; Plounevez &
Champalbert, 1999, 2000; Borme et al., 2009).
The main small copepod species found in stomach
content were Paracalanus spp., Oithona spp. and
copepodite stages of Calanoida. It is known that these
copepods form dense aggregations associated with
saline discontinuities of the estuarine front (Vias et
al., 2002; Marrari et al., 2004).
Small copepods are important links in marine food
webs, acting not only as major grazers of small
phytoplankton but also preying upon heterotrophic
protists which are components of the microbial loop
(Turner, 2004). Thus, they might play a significant
role in the energy transfer to anchovy by an alternative
pathway to the traditional herbivorous food web of
shelf waters: spring diatom bloom-herbivorous
calanoid copepods-fish.
The species composition and relative abundance
observed in zooplankton samples coincided roughly
with the stomach contents. However, despite of the
large abundance of small copepods in anchovy diet, a
clear selectivity for prey greater than 1 mm TL was
observed in this work. This might be explained by a
decrease in retention efficiency of small prey by the
filtering apparatus of larger fishes. In fact, an increase
in gill-raker spacing with anchovy size has been
previously shown (Angelescu, 1981).
Intensive predation on patches of unidentified fish
eggs and appendicularians was observed in two
specific hauls in northern and southern sectors of the
study area respectively. Fish eggs aggregations are
frequently found in the RdP estuary, belonging of
about twenty fish species including anchovy that
spawn pelagic eggs there (Madirolas et al., 1997;
Berasategui et al., 2004). On the other hand,
appendicularians are known to form dense breeding
patches near the surface water during the sexual
maturity period (Fenaux, 1985; Capitanio et al., 1997).
Anchovy predation on these occasional prey patches
confirms its opportunistic feeding habits.
Some authors suggest that the planktivorous fishes
spawn in zooplankton-rich locations, which is
reasonable due to the high energetic cost of
reproduction (Hunter & Leong, 1981; Peebles et al.,
1996; Peebles, 2002). In fact, Patagonian anchovy
stock spawns in a frontal area where high biomass of
copepods has been detected (Ramrez et al., 1990).
However, in the CRH of the northern stock it has been
widely mentioned that feeding conditions are
unfavourable for anchovy adults (Angelescu, 1982;
Ciechomski & Snchez, 1983; Pjaro, 2002; Pjaro et
al., 2007). Pjaro (2002) proposed that favourable
conditions for the adults might not be the same for
211
eggs and larvae, due to the fact that greatest amounts
of large zooplankton also mean higher amounts of
potential predators. According to this, the strategy of
the fishes could consist in feeding in shelf waters,
which is dominated by high concentrations of large
zooplankton, and subsequently migrate into the CRH
where dominant small zooplankton is suitable for
feeding larvae (Pjaro, 2002).
The present findings, although based on few
samples, would suggest that in RdP front, the above
mentioned strategy should be revised since intense
feeding occurs in this sector of the CRH. The
coincidence of both feeding and spawning grounds
could have important implications. It might be
expected an increased reproductive potential of E.
anchoita in the estuarine front as it was reported for
other anchovy species spawning in food rich areas
(Peebles et al., 1996). Further studies are required to
confirm this observation.
ACKNOWLEDGEMENTS
The authors are indebted to Dr. Jorge Hansen,
Director of the Anchovy Project of INIDEP, and the
Oceanography Laboratory of INIDEP for providing
the environmental data. This study was partially
funded by CONICET-PIP5009; PICT 15227-03 and
UNMdP 15/E269.
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DOI: 10.3856/vol39-issue2-fulltext-3

Research Article

Influence of dietary starch and cellulose levels on the metabolic profile and
apparent digestibility in penaeoid shrimp

Susana Mara Velurtas3, Ana Cristina Daz2,3, Anala Vernica Fernndez-Gimenez1,3

& Jorge Lino Fenucci1,3
1
Consejo Nacional de Investigaciones Cientficas y Tcnicas
2
Comisin de Investigaciones Cientficas
3
Departamento de Ciencias Marinas, Facultad de Ciencias Exactas y Naturales
Universidad Nacional de Mar del Plata, Funes 3350, B7602AYL, Mar del Plata, Argentina

ABSTRACT. The present study compared the effect of different starch/cellulose ratios (30/0, 20/10, 10/20,
0/30) on the metabolic response and apparent digestibility in two species of penaeoids: Artemesia longinaris
and Pleoticus muelleri. Adult animals were used in order to obtain sufficient quantities of haemolymph and
faecal material for analysis. No significant differences were found in levels of plasma metabolites in P.
muelleri, but in A. longinaris, a significant increase was observed in glucose, total protein, and cholesterol in
correlation with increased dietary starch. The apparent digestibility coefficients decreased from 83.7% to
51.2% (A. longinaris) and from 71.9% to 7.6% (P. muelleri) as the dietary starch levels increased. The ratio of
amylase activity to protease activity (A/P ratio) declined in A. longinaris when the percentage of dietary starch
increased. In contrast, the A/P ratio for P. muelleri increased with higher starch concentrations. These results
demonstrated a close relationship between the feeding habits and digestive physiology of the two species
studied; they also suggest a more herbivorous behavior for A. longinaris and more omnivorous habits for P.
muelleri.
Keywords: Artemesia longinaris, Pleoticus muelleri, apparent digestibility, carbohydrate metabolism,
cellulose, starch, haemolymph, Argentina.

Influencia del nivel de almidn y celulosa en la dieta sobre el perfil metablico y

digestibilidad aparente en camarones penaeoideos

RESUMEN. En el presente estudio se compar el efecto de diferentes concentraciones de almidn/celulosa

(30/0; 20/10; 10/20; 0/30) sobre la respuesta metablica y la digestibilidad aparente en dos especies de
peneidos, Artemesia longinaris y Pleoticus muelleri. Se utilizaron animales adultos a fin de obtener cantidades
suficientes de hemolinfa y heces para los anlisis. No hubo diferencias significativas en los niveles de
metabolitos plasmticos en P. muelleri, en cambio en A. longinaris se observ un incremento significativo de
la glucosa, protenas totales y colesterol en relacin con el aumento del almidn en la dieta. Los coeficientes
de digestibilidad aparente disminuyeron de 83,7% a 51,2% (A. longinaris) y de 71,9% a 7,6% (P. muelleri) a
medida que los porcentajes de almidn en la dieta aumentaron. El cociente entre la actividad de amilasa y
proteasa (A/P) se redujo en A. longinaris con los mayores porcentajes de almidn dietario; por el contrario, el
cociente A/P en P. muelleri aument cuando la concentracin fue ms alta. Estos resultados demostraron que
existe una estrecha relacin entre los hbitos alimentarios y la fisiologa digestiva de las dos especies
estudiadas; sugiriendo un comportamiento ms herbvoro para A. longinaris y ms omnvoro para P. muelleri.
Palabras clave: Artemesia longinaris, Pleoticus muelleri, digestibilidad aparente, metabolismo de
carbohidratos, celulosa, almidn, hemolinfa, Argentina.

___________________
Corresponding author: Ana Cristina Daz (acdiaz@mdp.edu.ar)
215 Influence of dietary cellulose level in penaeoid shrimp
INTRODUCTION
The major achievements in crustacean nutrition
include the identification of a protein sparing effect of
dietary carbohydrates and lipids, leading to
considerably lower protein requirements than those
originally suggested. The proteins are the higher
reserve substrate in shrimp, which can be converted to
carbohydrates following the gluconeogenic pathway
(Campbell, 1991). The carbohydrates are not essential
for crustaceans; shrimp appear to be able to utilize
complex carbohydrates better than simple ones such as
glucose, which is quickly absorbed and released into
the haemolymph, resulting in a physiologically
abnormal elevation of plasma glucose levels (New,
1976, 1990; Shiau & Peng, 1992). Starch is nowadays
the typical carbohydrate in formulated feeds for
crustaceans; it is well hydrolyzed by shrimp such as
Fenneropenaeus indicus and Litopenaeus vannamei
but poorly hydrolyzed by lobsters (Verri et al., 2001).
The rate of nutrient absorption depends on the rate
at which nutrients come into contact with the
absorptive epithelium. Dietary fibers, such as
cellulose, are associated with the delay in stomach
emptying and contribute to the efficient utilization of
dietary protein (Gomez Daz & Nakagawa, 1990).
Determination of digestibility can be used to select
ingredients that optimize the nutritional value and
reduce costs of formulated feeds. Among the methods
employed in feed digestibility studies in crustaceans,
the use of chromic oxide as an inert indicator is
recommended with procedural steps to insure
accuracy (Fenucci et al., 1980, 2009; Lee &
Lawrence, 1997; Divakaran et al., 2002).
The carbohydrates are incorporated in aquaculture
feeds to reduce costs and for their binding properties
during feed manufacturing. Waste management has
become a prime concern for shrimp farming in many
countries. It is generally accepted that a better
understanding of feed utilization by the shrimp is
essential to reduce environmental pollution through
both ammonia excretion and feces egestion;
carbohydrate utilization can be achieved and
consequently lead to a decrease in the amount of
nitrogen waste.
Haemolymph is the prime component involved in
the defense mechanism of crustaceans; several
metabolic variables of haemolymph, such as proteins,
glucose, and cholesterol have been proposed to
monitor the effect of environmental conditions on wild
and cultured shrimp (Hall & Van Ham, 1998; Snchez
et al., 2001; Pascual et al., 2003). Fluctuations in
biochemical variables are also associated with the
physiological response to stress, but these variables
levels can only be properly interpreted if the
nutritional state of the shrimp is carefully controlled.
The present study was designed to compare the
dietary effect of different ratio starch/cellulose on
selected physiological, metabolic, and hematological
responses and the apparent digestibility in two species
of penaoids (Artemesia longinaris and Pleoticus
muelleri). Both species present seasonal and yearly
fluctuations in catches; it is therefore important to
establish the feasibility of culturing them on
commercial basis to keep a continue supply of these
species to the market. The Aquaculture group from the
University of Mar del Plata has been working with
both species, but mainly with P. muelleri, on different
aspects of the biology, nutrition, maturation, massive
larval culture, and growth out in ponds. Some studies
have demonstrated good survival and growth under
culture conditions (Fenucci et al., 1983, 1990;
Petriella et al., 1984; Daz et al., 1996), and
determined the nutritional requirements (Fernndez-
Gimenez & Fenucci, 2002; Romanos-Mangialardo &
Fenucci, 2002) as well as gonadal maturation in
captivity (Daz et al., 1997, 2001; Daz & Fenucci,
2004), and characterized the digestive proteinases in
relation to the molting cycle (Fernndez-Gimenez et
al., 2002).
MATERIALS AND METHODS
Feed and feeding trials
Artemesia longinaris and Pleoticus muelleri were
obtained from a commercial fisherman in the coastal
waters of Mar del Plata, Argentina (38S). Large adult
animals were used in these experiments to obtain
sufficient quantities of faecal material for the analysis
of feed digestibility. All individuals were kept in 150
L glass aquaria with continuous aeration during four
weeks. Filtered seawater (to 5m) was exchanged at a
rate of 50% per day. Shrimp were exposed to constant
conditions of photoperiod (11 h light-13 h dark),
temperature (18C), pH 7, and salinity (31 ppt). The
ammonium concentration never exceeded 0.2 mg L-1.
All groups were fed ad libitum once a day (09:30 h).
Formulated feeds were tested in triplicate groups for
both species, each A. longinaris group consisted of 6
shrimp (2.7 0.9 g mean weight) and P. muelleri
groups had 4 shrimp (9.7 2.0 g mean weight),
randomly chosen.
The treatments consisted of four dry formulated
feed prepared to contain different ratios
starch/cellulose (30/0; 20/10; 10/20; 0/30), with 0.5%
chromic oxide as an inert indicator (to calculate the
apparent protein digestibility coefficients). Formu-
 Lat. Am. J. Aquat. Res.
lations were made according to the chemical
composition results of the by-products meal in order
to obtain isoproteic and isolipidic diets. The chemical
composition of the formulated feeds was confirmed
through proximate analysis (Table 1) according to
AOAC (1997). All ingredients, from a local feed
manufacturer, were mixed and cold pelleted (< 50C)
by extrusion (Fenucci & Zein-Eldin, 1976) and were
oven-dried for 24 h at 50C.
Apparent digestibility
After a 7-day period of adjustment to the new
conditions and diets was beginning of fecal collection.
To determine the apparent digestibility for crude
protein, before each feeding, feces were collected
during two weeks by siphoning and rinsed with
distilled water to eliminate the excess of salts. The
fecal material from each tank was pooled and frozen at
-20C for analysis.
Proximate analyses of faecal samples were carried
out using AOAC methods (1997). The chromic oxide
levels were measured with a spectrophotometer (540
nm) (Shimadzu UV-2102 PC, UV-visible Scanning
Spectrophotometer). The apparent digestibility
coefficient (ADC) was estimated according to Fenucci
et al. (1980): ADC (% protein digestibility) = 100 -
(Ia/Ib . IIb/IIa . 100) where: Ia = %Cr2O3 feed; Ib = %
Cr2O3 feces; IIa = % protein food; IIb = % protein feces.
Sampling and analyses of metabolic variables
At the end of the experiments (four weeks), shrimp
were anaesthetized in ice water for approximately 5
min, then the haemolymph was extracted and midgut
gland was removed. All shrimp used in the analysis
were in the intermolt stage (Petriella, 1984; Daz &
Petriella, 1990). Samples collected from eight
individuals (n = 8) of each treatment group were
analyzed separately.
Approximately 200-300 L of haemolymph were
extracted from the arthrodial membrane of the fifth
pereiopod of each organism; using a 1 mL syringe
rinsed with a 10% cooled anticoagulant solution of
sodium citrate. The haemolymph was centrifuged at
800 g for 5 min, and plasma transferred into a new
tube and stored at -20C for further analysis.
Midgut glands were carefully dissected and
immediately frozen at -20C and homogenized in
chilled distilled water and centrifuged for 30 min
(10,000 g at 4C), the upper aqueous phase was stored
at -20C.
Glucose, total protein and cholesterol concen-
trations in plasma and supernatants from homogenate
were measured using commercial kits for medical
216
diagnosis (Wiener Laboratories SAIC, Argentina),
according to the manufacturers protocols and
quantified in a Metrolab 1600DR (Wienerlab
Instrument). The extracts were analyzed in triplicate.
Enzyme assays
The amount of soluble protein in the homogenized
midgut glands used for enzyme analysis was
determined by the Bradford method (1976). Albumin
from chicken egg white (Sigma) was used as the
standard.
Total proteinase determination was performed with
1% azocasein in 50 mM Tris-HCl, pH 7.5 as substrate.
Triplicates of 5 L of enzyme extracts were mixed
with 0.5 mL of buffer and 0.5 mL of substrate
solution. The reaction mixtures were incubated for 10
min at 25C. Proteolysis was stopped by adding 0.5 ml
of 20% trichloroacetic acid TCA, and the mixture was
centrifuged in Eppendorf tubes for 5 min at 14 000 g.
The supernatants were separated from the undigested
substrate and the absorbance at 366 nm was recorded
for the released dye (Garca-Carreo, 1992).
Total -amylase activity was determined using
commercial kits for medical diagnosis (Wiener
Laboratories SAIC, Argentina), according to the
manufacturers protocols and quantified in a Metrolab
1600DR (Wienerlab Instrument).
Total cellulase activity was determined according
to Martnez et al. (1999) modified method. A solution
of crystalline cellulose was prepared in substrate
buffer sodium acetate 0.05 M; pH 5. A 24 mL volume
of this substrate solution was then mixed with 1 mL of
midgut gland extract, incubated with gentle agitation,
for 2 h at 30C. The reaction mixture was centrifuged,
2 ml of supernatant was separated and added 0.1 mL
starch solution (100 mg mL-1) and 2 mL of 3.5-
dinitrosalicilic acid. Then, the extract was incubated
for 5 min at 100C and the absorbance was recorded at
490 nm. The extracts were analyzed in triplicate.
Statistical Analysis
One-way ANOVA and Duncans multiple
comparisons of means were preformed to compare the
data obtained. Homogeneity of variances was verified
with Cochrans test. An arcsine transformation was
applied before processing percentages data. Protein
digestibility among different treatments was evaluated
through regression analyses. A correlation coefficient
was used to describe the fit of the data on the
regression line. ANCOVA was used to test differences
among regression lines. To find out the relationships
among different ratio starch/cellulose in the diet and
metabolic variables, Pearson's rank correlation
217 Influence of dietary cellulose level in penaeoid shrimp

Table 1. Ingredient composition of formulated feeds.

Tabla 1. Composicin de las dietas formuladas.

Ingredient Formulated feed (g 100 g-1 dry feed)

D1 D2 D3 D4
a
Fish meal 48 48 48 48
Soybean mealb 15.5 15.5 15.5 15.5
Manioc starchc 30 20 10 0
Cellulose microcrystallined 0 10 20 30
Fish oil 2 2 2 2
Lecithin 0.5 0.5 0.5 0.5
Cholesterol 0.5 0.5 0.5 0.5
Vitamin supplemente 0.5 0.5 0.5 0.5
Mineralsf 0.5 0.5 0.5 0.5
Fish soluble 1 1 1 1
Chromic oxide 0.5 0.5 0.5 0.5
Na alginate 1 1 1 1
Proximate composition (% dry matter)
Dry matter 99.3 97.6 98.2 99.2
Crude protein 37.9 38.2 38.2 37.8
Total lipid 12.4 13.2 12.0 12.7
Ash 11.0 11.6 10.8 10.2
a
Agustinier S.A. Mar del Plata, Argentina. bMelrico S.A. Argentina.
c
Molinos Chacabuco, Argentina. d Merck, Germany.
e
Vitamin premix (mg kg-1 of premix): cholecalciferol 35; thiamin 163;
rivoflavin 156; pyridoxine 213; calcium pantothenate 250; biotin 250; niacin
500; folic acid 25; B12 HCL 20; ascorbic acid Rovimix STAY C 781;
menadione 34; inositol 300; choline chloride 200; a-tocopherol acetate 1750;
vitamin A acetate 180 (Roche, Argentina).
f
Mineral premix: calcium 1,000 mg; magnesium 500 mg; potassium 99 mg;
zinc 30 mg; 10 mg; iron 10 mg; copper 2 mg; iodine 150 g; selenium 200
g; chromium 200 g; molybdenum 500 g (Twin Laboratories, Inc. USA).

coefficient was done. A probability level of 0.05 was
used to assess significance in all measured parameters.
(Sokal & Rohlf, 1995).
RESULTS
Metabolic variables
Mean values of metabolic variables for each species
are shown in Figure 1. There were no significant
differences in levels of plasma metabolites in P.
muelleri when shrimp were fed with different ratio
starch/cellulose. Significant variations were observed
in the metabolic variables of A. longinaris, a
significant increase in glucose, total protein, and
cholesterol was noted in correlation with the increase
in starch.
The analysis of the midgut gland from shrimp fed
with different levels of starch/cellulose showed that
concentration of metabolites was different in both
species. The highest level of cholesterol was observed
in A. longinaris fed with D1 (30/0, starch/cellulose),
whereas concentrations of glucose and total protein
were not significantly different. In contrast, in P.
muelleri glucose was significantly higher in shrimp
fed with D1 than in those fed with diet containing
lower starch levels.
Enzyme assays
Soluble protein content of the midgut gland was 15.3
1.68 mg mL-1 in A. longinaris and 17.3 2.30 mg
mL-1 in P. muelleri. No significant differences were
observed in proteinase and -amylase activity in
midgut gland extracts from the four dietary groups in
both species (Table 2). No specific cellulase activity
was observed in the midgut gland extracts.
The ratio of amylase activity to protease activity
(A/P ratio) decreased in A. longinaris when the
 Lat. Am. J. Aquat. Res. 218

Figure 1. Metabolic variables in haemolymph and midgut gland of A. longinaris and P. muelleri fed with different ratio
starch/cellulose in the diet. Error bars indicate standard deviation. Different letters indicate statistical differences (P <
0.05).
Figura 1. Variables metablicas en hemolinfa y hepatopncreas de A. longinaris y P. muelleri alimentados con diferentes
niveles de almidn/celulosa en la dieta. La barra indica la desviacin estndar. Letras distintas indican diferencias
estadsticas significativas (P < 0,05).

percentage of dietary starch increased. In contrast, the
A/P ratio for P. muelleri increased when starch
concentration was high (Fig. 2).
Apparent Digestibility
The apparent protein digestibility coefficients
decreased from 83.7% to 51.2% in A. longinaris) and
from 71.9% to 7.6% in P. muelleri with the increase in
dietary cellulose levels, and was significantly different
among treatments. In vivo apparent protein
digestibility was related to dietary cellulose contents
as shown by the regression analysis (y = 0.095x2 -
4,2647x + 88,671; R2 = 0.7198 for A. longinaris, and y
= 97,476 e-0, 0829x, R2 = 0.724 for P. muelleri) (Fig. 3).
Pearsons Correlation
Pearson correlation coefficients showed that all
variables exhibited a greater degree of correlation with
the cellulose rate, except glucose in haemolymph for
A. longinaris (Table 3) and glucose in midgut gland
for P. muelleri (Table 4). Metabolic variables were
correlated with each other.
DISCUSSION
Dietary nutritional requirements of two species of
penaeoids were investigated on the basis of their
haemolymph metabolic contents and the apparent
digestibility analysis to determine which the dietary
components that were better assimilated are. The
penaeoids shrimp do not present a dietary glucose
requirement since this compound can come from the
gluconeogenesis from the amino acids. Nevertheless,
these organisms own a complete enzymatic structure
for the digestion of proteins and polysaccharides, such
219 Influence of dietary cellulose level in penaeoid shrimp

Table 2. Specific enzyme levels ( SEM) recorded from midgut gland at four levels of dietary starch/cellulose in A.
longinaris and P. muelleri.
Tabla 2. Niveles enzimticos ( ESM) especficos registrados en hepatopncreas de A. longinaris y P. muelleri alimenta-
dos con cuatro niveles dietarios de almidn/celulosa.

Protease Amylase
Formulated feed
A. longinaris P. muelleri A. longinaris P. muelleri
a a a
D1 0.11 0.007 0.25 0.117 2.06 0.007 3.78 0.410a
D2 0.11 0.056a 0.24 0.009a 2.30 0.007a 2.99 0.183a
D3 0.09 0.011a 0.32 0.019a 2.56 0.084a 2.20 0.128a
D4 0.05 0.024b 0.47 0.066a 2.56 0.275a 3.69 0.134a
Specific protease activity expressed as Abs/mg protein/min. Specific amylase activity
expressed as mg starch hydrolyzed/mg protein/min. Different superscripts are significantly
different, P < 0.05.

Figure 2. The effect of dietary starch levels on ratio of
amylase specific activity to protease specific activity on
polynomial regression analysis in A. longinaris and P.
muelleri (y = 0.051x2 2.602x + 50.80, R = 0.969 for A.
longinaris, and y = 0.009x2 + 0.001x + 7.387, R = 0.867
for P. muelleri).
Figura 2. Regresin polinomial del efecto de los niveles
de almidn en la dieta sobre el cociente entre la actividad
especfica de amilasa y la de proteasa en A. longinaris y
P. muelleri (y = 0,051x2 2,602x + 50,80; R = 0,969
para A. longinaris; y = 0,009x2 + 0,001x + 7,387; R =
0,867 para P. muelleri).
as starch, glycogen, laminarin, and chitin that are
natural components of their diet. (Tacon, 1990). The
starch is a straight-chain consisting of glucose
molecules linked together by (1-4) bonds,
conformed by two units amylose and amylopectin.
The starches rich in amylose are poorly digestible
because -amylase cannot hydrolyze the amylase, in
contrast, the starch rich in amylopectin is relatively
well digested (Gaxiola et al., 2006). The cellulose is
also a polymer of glucose but it differs in its glycoside
Figure 3. Apparent protein digestibility at four levels of
dietary starch/cellulose in A. longinaris and P. muelleri.
Values are means of three observations. Error bars
indicate standard deviation.
Figura 3. Digestibilidad aparente de protenas con cuatro
niveles de almidn/celulosa en la dieta de A. longinaris y
P. muelleri. Los valores representan la media de tres
observaciones. La barra indica la desviacin estndar.
bonds, which are (1-4). The inclusion of starch in
the shrimps diet represents the greater source of
energy. The incorporation of cellulose was used to
compensate the amount of carbohydrates added to the
experimental diet or to increase stomach emptying
(Shiau, 1997).
The type of food is a dominant factor affecting
shrimp haemolymph metabolites (Pascual et al.,
2003). Baseline levels of the haemolymph metabolites
were obtained by Rosas et al. (2002) in Litopenaeus
vannamei to be used as reference parameters. Glucose
is the major component of circulating carbohydrates in
crustaceans, but its concentration varies markedly
 Lat. Am. J. Aquat. Res. 220

Table 3. Correlation matrix of metabolic variables and cellulose in feed for Artemesia longinaris.
Tabla 3. Matriz de correlacin de las variables metablicas y el nivel de celulosa en la dieta para Artemesia longinaris.

C GH PH ChH GMG PMG ChMG APD

C 1
GH -0.983 1
PH -0.919* 0.901* 1
ChH -0.941* 0.928* 0.998 1
GMG -0.432* 0.445* 0.042* 0.106* 1
PMG -0.865* 0.941* 0.749* 0.785* 0.524* 1
ChMG -0.866* 0.940* 0.842* 0.865* 0.313* 0.973 1
APD -0.874* 0.889* 0.983 0.980 -0.014* 0.786* 0.893* 1
*P < 0.05. C-Cellulose feed; GH -Glucose Haemolymph; PH- Total Protein Haemolymph; ChH -
Cholesterol Haemolymph; GMG -Glucose Midgut Gland; PMG -Total Protein Midgut Gland; ChMG -
Cholesterol Midgut Gland; APD - Apparent Protein Digestibility

Table 4. Correlation matrix of metabolic variables and cellulose in feed for Pleoticus muelleri.
Tabla 4. Matriz de correlacin de las variables metablicas y el nivel de celulosa en la dieta para Pleoticus muelleri.

C GH PH ChH GMG PMG ChMG APD

C 1
GH -0.775* 1
PH -0.866* 0.871* 1
ChH -0.445* 0.751* 0.346* 1
GMG -0.954 0.913* 0.868* 0.674* 1
PMG 0.245* -0.536* -0.753* -0.960 -0.478* 1
ChMG -0.252* -0.340* -0.232* -0.138* 0.063* 0.025* 1
APD -0.947* 0.620* 0.661* 0.471* 0.886* -0.346* 0.515* 1
*P < 0.05. C-Cellulose feed; GH -Glucose Haemolymph; PH - Total Protein Haemolymph; ChH
-Cholesterol Haemolymph; GMG -Glucose Midgut Gland; PMG -Total Protein Midgut Gland;
ChMG - Cholesterol Midgut Gland; APD -Apparent Protein Digestibility

among the species (Chang & OConnor, 1983).
Increases in haemolymph glucose are also associated
with the physiological response to stress in shrimp, but
levels can only be properly interpreted if the
nutritional state of the shrimp is carefully controlled
(Hall & Van Ham, 1998). Furthermore, the glucose in
haemolymph is an indicator of the carbohydrates
metabolism and the level of this nutrient in the diet. In
the present study, the glucose levels were similar to
those reported in juvenile L. setiferus, L. vannamei
and L. stylirostris (Rosas et al., 2000). In A.
longinaris, the glucose in haemolymph was no
correlated with cellulose level in the diet (Table 3);
shrimp could activate its compensation mechanism
that allowed the recovery of haemolymph metabolites
to maintain the homeostasis. This mechanism could
involve the use of reserves stored in digestive gland,
such as demonstrated in other species (Pascual et al.,
2003).
From the entire set of metabolites studied in A.
longinaris plasma, glucose, total protein, and
cholesterol were the most affected by the increase of
starch in diet. But in P. muelleri there were no
significant variations under the same conditions.
In P. muelleri, cholesterol in midgut gland showed
slight fluctuations, however in A. longinaris,
significant differences were observed among dietary
treatments (Fig. 1). The shrimps midgut gland is
considered the main storage organ, mainly
accumulating lipids, and to a lesser degree, glycogen.
It has been proposed in crustaceans, that cholesterol is
conserved due to their role as structural component of
cell membranes, and is also an essential nutrient for
crustaceans since they are incapable of de novo
synthesis of the steroid ring (Rabid et al., 1999). The
dependence of haemolymph cholesterol on dietary
lipids levels is related to the ability of shrimp to store
and synthesize lipids. Mourente & Rodrguez (1991)
and Teshima (1998) showed that because of the
221 Influence of dietary cellulose level in penaeoid shrimp
limited space in shrimps digestive gland, lipids must
be processed rapidly and delivered into the
haemolymph, where they are transported to the
different tissues to be metabolized. With regards to P.
muelleri, this species will be using cholesterol of the
diet quicker than A. longinaris. Probably for that
reason it is observed higher levels of cholesterol in A.
longinaris haemolymph and midgut gland and in P.
muelleri only in the haemolymph. As all supplied diets
had the same cholesterol level, it was evident that P.
muelleri presented a greater requirement of this
nutrient, which was demonstrated by a smaller level of
reserve. P. muelleri would be more carnivorous and
require cholesterol from animal sources. This is in
agreement with the results of digestibility, which
decreased with increasing cellulose inclusion
Borrer & Lawrence (1989) observed that the level
of dietary cellulose affected apparent protein
digestibility in Farfantepenaeus aztecus, by lowering
digestibility values as cellulose levels increased. A
similar result was observed in Macrobrachium
rosenbergii (Gonzlez-Pea et al., 2002). On the other
hand, in L. vannamei the protein digestibility did not
change with the different levels of cellulose (Borrer &
Lawrence, 1989; Guo et al., 2006). It was evident that
A. longinaris fed with diets poor in cellulose content
(D1 and D2) assimilated better the nutrients than P.
muelleri and this fact was reflected by an increase of
circulating metabolites and the apparent digestibility
(Fig. 3). In both species, the digestibility values
decreased from D1 to D4, nevertheless the values of
apparent digestibility in A. longinaris were higher than
in P muelleri. This fact would be related to the rate of
nutrient absorption that depends on the time at which
nutrients come into contact with the absorptive
epithelium. According to other authors, the relative
influence of dietary fiber on the movement of
nutrients along the gastrointestinal tract affects
nutrient absorption (Shiau, 1997). So, it is possible
that the dietary fiber with high viscosity reduces the
interaction between the enzymes and substrates,
reducing absorption rates. The binding capability of
the dietary fiber is another possible factor that can
reduce the availability of nutrients (Gonzlez-Pea et
al., 2002).
The proteins are essential nutrients for the
penaeoids shrimps because they are basic for growth,
the regulation of the internal osmotic pressure, the
gluconeogenesis and the immune system (Rosas et al.,
2002). Therefore variations of this nutrient in
haemolymph can be used as good indicator of general
physiological state. The increment in haemolymph
proteins observed in A. longinaris feed D1 and D2
(high levels starch) could be related with amino acids
synthesis from the transamination pathway, and its
posterior storing (Rosas et al., 2001). The values of
proteins in haemolymph and digestibility for the
different treatments in P. muelleri did not adjust to a
same pattern. Whereas digestibility was greater in D1
and D2, there were no differences in the circulating
proteins. From the analysis of the proteins data it can
be postulated that P. muelleri employs these absorbed
proteins for muscular development or growth.
Penaeid shrimp adapt quite well to changes in diet
composition by the induction of digestive enzymes
synthesized and secreted in midgut gland. These
enzymes hydrolyze a variety of substrates and various
factors are involved in their regulation, including diet
(Gamboa-Delgado et al., 2003). Therefore, the
digestive enzyme profile can be used to illustrate the
capacity of shrimp to exploit diet in order to meet
nutritional requirements. Carnivorous species
generally have a wide range of proteolytic enzyme at
high concentrations, which is consistent with their
ability to hydrolyze high levels of dietary protein
(Johnston & Yellowlees, 1998). However, omnivores
and herbivores have a wide range and higher
concentration of carbohydrases, consistent with their
ability to hydrolyze plant and animal dietary
carbohydrate (Wigglesworth & Griffith, 1994). The
decline in the ratio of amylase to protease observed in
A. longinaris in our study, confirms that carbohydrate
digestion and its utilization change with the increase
in dietary starch levels. In contrast, in P. muelleri the
A/P ratio was correlated with dietary starch level. This
shift in relative importance of carbohydrate and
protein highlights the strategy outlined above,
whereby carbohydrate energy reserves are used
initially, while protein becomes important once
carbohydrate reserves are depleted.
In the current study, there was no cellulase activity
in the midgut gland of both species. It is now clear
that cellulases are produced endogenously in a number
of invertebrate taxa that includes crustaceans; genes
for cellulose enzymes (-glucosidase and endo--1,4-
glucanase) are present in the genome of crayfish
(Cherax sp.) (Linton et al., 2006). However, in
penaeoid species cellulose digestion has not been
unequivocally demonstrated (Shiau, 1997). More
suitable substrates and assays for the determination of
cellulase activity are required to clarify matters.
Although the bibliography indicates that both
species studied in this work present a similar
nourishing regime (Boschi, 1989; Gavio & Boschi,
2004), studies in culture conditions showed that both
species have a 92% apparent digestibility of proteins
with diets having fish meal as the main ingredient;
when this ingredient is replaced by soybean meal, the
 Lat. Am. J. Aquat. Res.
digestibility is 83% for A. longinaris and 47.7% for P.
muelleri (Fenucci et al., 2009). This difference in
digestibility can be related to the more carnivorous
behavior of the latter species. The present study shows
that apparent protein digestibility was influenced by
the levels of dietary starch and cellulose in both
species; increasing cellulose levels caused significant
reduction in protein digestibility. The inclusion of
starch as source of carbohydrates in the diet seems to
be more suitable than cellulose.
ACKNOWLEDGEMENTS
This research was funded by a grant PIP. N112-
200801-02585 from CONICET (Consejo Nacional de
Investigaciones Cientficas y Tcnicas) Argentina.
Special thanks to Dra. Liliana Sousa by the revision of
the English language of the manuscript. The authors
also thanks anonymous reviewers and editor for
critically reviewing the manuscript.
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Lat. Am. J. Aquat. Res., 39(2): 225-235, 2011 Population structure of Panulirus gracilis 225
DOI: 10.3856/vol39-issue2-fulltext-4

Research Article

Catch composition of the spiny lobster Panulirus gracilis (Decapoda: Palinuridae)

off the western coast of Mexico

Ral Prez-Gonzlez
Universidad Autnoma de Sinaloa, Facultad de Ciencias del Mar
P.O. Box 610, Mazatln, Sinaloa, Mxico

ABSTRACT. The lobster fishery in the Gulf of California and the south-central region of the western coast of
Mexico consists of small-scale artisanal activity supported by Panulirus gracilis and P. inflatus, with an
annual average catch of 132 ton. The present study analyzes the landing composition of this fishery and the
population structure of P. gracilis. Carapace lengths (CL) for this species ranged from 35 to 125 mm, and the
most frequent sizes were between 60 and 85 mm. The size distribution was approximately normal. This
implies that the fishery is composed of several size classes, with annual recruitment to the fishing areas. For
the 1989-1990 and 1990-1991 fishing seasons, the mean monthly sizes of males were between 70.18 11.74
and 81.11 6.76 mm CL, whereas females averaged from 73.60 8.95 to 80.28 7.53 mm CL. Power-law
relationships between carapace length (CL in mm) and total weight (TW in g) were determined, resulting in
the following equations: PT = 0.0021 CL2.7689 for males and PT = 0.0009 CL3.0038 for females. During certain
periods of the year, males dominated the catch; however, the overall annual male:female ratio was near 1:1.
Keywords: population structure, spiny lobster, Panulirus gracilis, Gulf of California, Mexico.

Composicin de la captura de la langosta espinosa Panulirus gracilis

(Decapoda: Palinuridae) en la costa oeste de Mxico

RESUMEN. La pesquera de langosta en el golfo de California y en el centro-sur de la costa occidental de

Mxico es una actividad artesanal a pequea escala y es sostenida por Panulirus gracilis y P. inflatus, con una
captura promedio anual de 132 ton. En este estudio se analiza la composicin de los desembarques de esta
pesquera y la estructura de la poblacin de P. gracilis. El intervalo de talla de esta especie fue de 35 a 125
mm de longitud del cefalotrax (LC) y el ms frecuente se encontr entre 60 y 85 mm. La distribucin de
tallas fue aproximadamente normal. Esto implica que la pesquera est compuesta por varias clases de tallas,
con un reclutamiento anual a las reas de pesca. La talla media mensual de machos fue entre 70,18 11,74 y
81,11 6,76 mm LC y en hembras de 73,60 8,95 a 80,28 7,53 mm LC, durante las temporadas de pesca
1989-1990 y 1990-1991. Se determin la relacin entre la LC (en mm) y el peso total (PT, en g), obtenindose
las siguientes ecuaciones: PT = 0.0021 LC2.7689 en machos y PT = 0.0009LC3.0038 en hembras. Durante ciertos
perodos del ao los machos son dominantes en las capturas, pero la proporcin machos:hembras durante todo
el ao es cercana a 1:1.
Palabras clave: estructura poblacional, langosta, Panulirus gracilis, golfo de California, Mxico.
___________________
Corresponding author: Ral Prez-Gonzlez (raulp@ola.icmyl.unam.mx)

INTRODUCTION The annual landings of these species were estimated at

On the Mexican coast of the Pacific Ocean and Gulf
of California, Panulirus gracilis and P. inflatus are
locally important fishery resources and their
harvesting is exclusively a small-scale artisanal
activity, developed mainly on the continental shelf.
approximately 500-650 t during the 15-year period
from 1990-2005. This production includes the catches
of these species obtained in Baja California (A. Vega-
Velzquez, pers. comm.).
Traditionally, P. gracilis and P. inflatus were
captured in traps and sometimes by divers (Prez-
226 Lat. Am. J. Aquat. Res.
Gonzlez et al., 2002a). A major change in the
exploitation strategy of these species took place during
the 1980s and early 1990s with the progressive
introduction of tangle nets, which have almost totally
replaced other fishing methods. These tangle nets
(called chinchorros langosteros in the region)
usually have stretched meshes of 101.6 and 114.3 mm,
lengths between 75.0 and 200.0 m and a height
between 0.9 and 1.8 m. In general, the nets are left in
the water for 24 h (one fishing day). A longer set time
leads to better catches of spiny lobster, as they are
attracted by fishes, crustaceans, mollusks and other
invertebrates caught in the nets (Olabarra, 1999;
Plascencia-Gonzlez & Van der Heiden, 2002; Prez-
Gonzlez, 2006; Prez-Gonzlez et al., 2002b, 2006).
Panulirus gracilis (called gera, verde, arenera or
playera spiny lobster) is distributed along the coastline
of the eastern Pacific from Baja California, Mexico, to
Paita, Peru and the Galapagos Islands (Holthuis, 1991;
Hendrickx, 1995). P. inflatus is endemic to Mexico,
but P. gracilis is also fished in Panama (Butler &
Pease, 1965), on the continental coast of Ecuador
(Loesch & Lpez, 1966; Bez, 1983), and in the
Galapagos Islands (Holthuis & Loesch, 1967). Most
studies on the two spiny lobsters coexisting along the
western coast of Mexico have considered them both;
only a few have been performed on the latter species
specifically.
The catch composition, population structure, sex
ratio, and fishery characteristics of both species have
been described on the Mexican Pacific (Weinborn,
1977; Briones et al., 1981; Jurez-Carrillo et al.,
2006) and Gulf of California coasts (Prez-Gonzlez
et al., 1992a, 1992b; Valadez-Manzano et al., 2003;
Arzola-Gonzlez et al., 2007). Here we report these
characteristics for P. gracilis off the western coast of
Mexico in the lower part of the Gulf of California.
MATERIALS AND METHODS
Commercial lobster fishing on the western coast of the
Gulf of California occurs in the south, primarily at the
state of Sinaloa. Therefore, the study area in this
region was located from the north of Punta Piaxtla to
the south in Mazatlan Bay, between 2310-2348N
and 10624-10654W (Fig. 1). The coast presents
extensive sand beaches with some gravel-sand
patches, while large areas offshore are rocky or
covered with gravel-sand.
The target species was determined according to the
catalogues of Holthuis (1991) and Hendrickx (1995)
catches were weighed monthly. To determine the
population structure of P. gracilis, catches were
sampled by accompanying fishermen in the field.
Lobsters caught with tangle nets from depths of
approximately 0.5-35 m were sampled at random
every month from September, 1989 to November,
1991.
To determine the relationships among total length
(TL), carapace length (CL), total weight (TW) and
carapace width (CW), regression equations for TL vs
CL, TW vs CW and CW vs CL were calculated from
sample of whole male and female P. gracilis caught in
the same study area. The TL was measured from
between the rostral horns to the posterior end of the
telson with a modified ichthyometer ( 1 mm). CL and
CW were measured with a vernier caliper ( 0.01
mm), with the former being measured along the mid-
dorsal line, from the transverse ridge between the
postorbital spines to the posterior edge of the
carapace, and the latter at the greatest width of the
carapace. TW was measured with a field balance ( 1
g).
Additionally, to obtain CL and TW to the nearest
mm and g, respectively, selected individuals were
transported to the laboratory each month to be
measured with a digital caliper ( 0.1 mm) and
weighed on an electronic balance ( 0.01 g). These
data were used to estimate the parameters of the
relationship between TW and CL by a linear
regression analysis of the log-transformed data:
TW= aCLb Ln (CL) + Ln(a)
where a and b are constants.
Data were grouped into 5-mm class intervals, weighed
for each landing and compiled into annual
distributions. The size distribution and sex ratio were
obtained from the pooled sample (catch obtained by
accompanying fishermen in the field plus commercial
landings).
RESULTS
From September, 1989 to November, 1991, a total of
13,834 spiny lobster were caught, of which 5,799
(41.92%) belonged to the species P. gracilis and 8,035
(58.08%) to P. inflatus. The observed relative
proportions of these lobster species showed an
inversion during the study period (Fig. 2). P. inflatus
predominated from September 1989 to September
1990, whereas P. gracilis was more abundant from
October 1990 to November 1991, except in February
and October of 1991.
Morphometric relationships
TL vs CL and CW vs CL exhibited linear
relationships, while TW vs CW was potential, and
their equations appear in Table 1. The determination
coefficient (R2) values were high.
 Population structure of Panulirus gracilis 227

Figure 1. Map of the study area in the lower part of the Gulf of California, western coast of Mexico.
Figura 1. Mapa del rea de estudio en la parte baja del golfo de California, costa occidental de Mxico.

TW-CL relationship
Data from 279 specimens (159 males; size range 42-
92 mm CL, weight range 60-580 g, and 120 females;
size range 48-86 mm CL, weight range 100-580 g),
were used to determine the relationship between TW
and CL (Fig. 3). The relationships between carapace
length (CL in mm) and total weight (TW in g) were as
follows: for males, TW = 0.0021 CL2.7689; for females,
TW = 0.0009 CL3.0038. The male relationship was
allometric (b 3, P < 0.05), whereas for females it
was isometric (b = 3, P > 0.05).

Figure 2. Panulirus inflatus and P. gracilis landings
between September 1989 and November 1991 in the
lower part of the Gulf of California, Mexico.
Figura 2. Capturas de Panulirus inflatus and P. gracilis
desembarcadas entre septiembre de 1989 y noviembre de
1991 en la parte baja del golfo de California, Mxico.
Size distribution
The size of the landed P. gracilis individuals
ranged from 40 to 120 mm CL in 1990, with most of
the individuals sized from 65 to 90 mm CL; the mode
was 75 mm CL (Fig. 4). In 1991, the specimens
ranged from 35 to 125 mm CL, with most of the
individuals sized from 60 to 85 mm CL; the mode was
228 Lat. Am. J. Aquat. Res.

Table 1. Regression equations for the relationships between total length (TL) and carapace length (CL), total weight
(TW) and CL and carapace width (CW) and CL estimated for both sexes of Panulirus gracilis in the lower part of the
Gulf of California, Mexico.
Tabla 1. Ecuaciones de las relaciones entre la longitud total (TL) y longitud del cefalotrax (CL), peso total (TW) y CL, y
ancho del cefalotrax (CW) y CL estimadas tanto para ambos sexos como separados de Panulirus gracilis en la parte baja
del golfo de California, Mxico.

Relationship Equation R2 n
Males + females
TL vs CL TL = 2.5027 CL + 16.036 0.898 271
TW vs CW TW = 0.0017 CW 2.973 0.886 271
CW vs CL CW = 0.7458 CL + 4.271 0.930 271
Males
TL vs CL TL = 2.3714 CL + 22.037 0.898 159
TW vs CW TW = 0.002 CW 2.9241 0.890 159
CW vs CL CW = 0.7403 CL + 4.4196 0.930 159
Females
TL vs CL TL = 2.8109 CL + 0.0933 0.949 112
TW vs CW TW = 0.0012 CW 3.0784 0.896 112
CW vs CL CW = 0.7616 CL + 3.57 0.934 112

75 mm CL (Fig. 5). No change in the modal size

Figure 3. Relationship between carapace length and total
weight in the spiny lobster Panulirus gracilis from the
lower part of the Gulf of California, Mexico.
Figura 3. Relacin entre la longitud del cefalotrax y el
peso total en la langosta espinosa Panulirus gracilis en la
parte baja del golfo de California, Mxico.
classes was found between the 1989-1990 and the
1990-1991 fishing seasons.
The sample mean and standard deviation were
analyzed for the 1989-1990 and 1990-1991 fishing
seasons. The monthly mean size, standard deviation
and size range of the sample, as a whole and by sex,
are presented in Table 2; the corresponding weight
data are given in Table 3. In the 1989-1990 fishing
season, the monthly mean sizes and weights of males
were between 70.18 11.74 and 81.11 6.76 mm CL
and 317.28 142.59 and 427.73 98.61 g TW,
respectively, and for females they were between 75.06
6.51 and 80.28 7.53 mm CL and 371.86 90.15
and 437.76 109.91 g TW. For the 1990-1991 fishing
season, the monthly mean sizes and weights of males
were between 71.09 11.31 and 79.30 6.99 mm CL
and 300.61 150.38 and 417.33 105.71 g TW,
respectively, and for females, they were between
73.60 8.95 and 77.23 6.62 mm CL and 355.00
124.12 and 431.67 136.05 g TW.
Sex ratio
A total of 5,799 P. gracilis lobsters were examined.
Of these, 56.4% were males (3,272) and 43.6% were
females (2,527). The overall sex ratio (M:F) was
1:1.3. However, the sex ratio varied monthly (Fig. 6).
The catch rates of male lobsters were consistently
higher in summer and autumn than those of females,
 Population structure of Panulirus gracilis
Figure 4. Size-frequency distributions of Panulirus
gracilis for a) both sexes, b) males and c) females by 5-
mm-CL size classes during 1990 in the lower part of the
Gulf of California, Mexico.
Figura 4. Frecuencia de tallas (intervalo cada 5 mm de
LC) de a) machos+hembras, b) machos y c) hembras de
Panulirus gracilis durante 1990 en la parte baja del golfo
de California, Mxico.
229
Figure 5. Size-frequency distributions of Panulirus
gracilis for a) both sexes, b) males and c) females by 5-
mm-CL size classes during 1991 in the lower part of the
Gulf of California, Mexico.
Figura 5. Frecuencia de tallas (intervalo cada 5 mm de
LC) de a) machos+hembras, b) machos y c) hembras de
Panulirus gracilis durante 1991 en la parte baja del golfo
de California, Mxico.
Figure 6. Percentage of males and females of Panu-
lirus gracilis in monthly samples from September
1989 to November 1991 in the lower part of the Gulf
of California, Mexico.
Figura 6. Porcentajes mensuales de machos y
hembras de Panulirus gracilis entre septiembre de
1989 y noviembre de 1991 en la parte baja del golfo
de California, Mxico.
230 Lat. Am. J. Aquat. Res.

Table 2. Monthly mean size, standard deviation and size range whole and by sex of the carapace length (CL, in mm) of
Panulirus gracilis, during 1989-1990 and 1990-1991 fishing seasons in the lower part of the Gulf of California, Mexico.
Tabla 2. Nmero de hembras y machos de Panulirus gracilis e intervalos de talla, medias y desviacin estndar mensua-
les de la longitud del cefalotrax (CL, en mm), durante las temporadas de pesca 1989-1990 y 1990-1991 en la parte baja
del golfo de California, Mxico.

Season 1989-1990
Total Males Females
Month n CL n Range CL n Range CL
X SD CL (mm) X SD CL (mm) X SD
Sep 132 76.38 5.48 100 64.8-99.1 75.90 4.88 32 64.1-93.8 77.86 6.91
Oct 143 77.19 5.96 105 65.8-87.1 76.06 4.86 38 63.1-94.2 80.28 7.53
Nov 158 76.96 7.60 93 60.6-113.1 76.69 6.71 65 61.2-98.6 77.35 8.76
Dec 174 77.68 7.76 90 53.1-101.8 79.06 7.88 84 57.5-93.9 76.19 7.38
Jan 142 79.39 6.52 72 68.0-93.2 80.14 6.21 70 63.5-96.0 78.62 6.78
Feb 125 78.69 7.56 66 62.7-98.2 81.11 6.76 59 63.1-95.5 75.98 7.54
Mar 178 76.03 8.75 67 47.6-109.7 77.64 11.44 111 56.0-95.0 75.06 6.51
Apr 267 78.17 7.53 87 55.8-109.3 80.31 9.16 180 65.2-96.3 77.14 6.37
May 272 75.17 10.25 69 39.2-95.3 70.18 11.74 203 47.0-100.0 76.87 9.11

Season 1990-1991

Total Males Females

Month n CL n Range CL n Range CL
X SD CL (mm) X SD CL (mm) X SD
Sep 47 76.46 7.94 34 61.3-96.9 76.73 7.78 13 60.2-88.1 75.76 8.63
Oct 168 78.22 8.26 99 43.9-106.3 79.12 7.75 69 56.9-102.6 76.93 8.84
Nov 153 76.98 5.17 98 68.9-90.1 77.43 4.35 55 67.6-98.4 76.18 6.35
Jan 261 75.70 7.86 146 49.0-98.8 76.11 8.70 115 60.5-101.4 75.19 6.65
Feb 237 76.25 7.87 108 52.6-107.4 75.95 8.40 129 51.3-100.6 76.49 7.43
Mar 278 77.93 6.80 94 66.4-104.6 79.30 6.99 184 67.1-96.1 77.23 6.62
Apr 176 74.82 8.43 32 46.8-107.0 71.38 13.64 144 51.1-94.1 75.59 6.59
May 190 72.96 9.65 49 53.5-107.7 71.09 11.31 141 53.4-100.3 73.60 8.95

which were more abundant in spring; however, the
overall sex ratio exhibited a significantly equal
distribution (1:1, P > 0.05) during the winter months.
DISCUSSION
Catch composition
Nets are the main fishing method used in the study
area and are deployed in rocky and gravel-sandy areas.
Prez-Gonzlez et al. (2002a) indicated that the
periodically inverse proportions of P. gracilis and P.
inflatus observed in commercial catches during the
fishing season or annually is due to their different
behaviors and the meteorological conditions related to
the habitat occupied by each species. In this study, we
observed that the fishermen set their nets close to the
coast over rocky bottoms, the preferred habitat of P.
inflatus (0.5-8.0 m depth), during periods of calm
water, whereas the nets were deployed offshore over
gravel-sandy bottoms at depths between 8.0 and 25-
35.0 m (the habitat of P. gracilis) in periods of strong
ocean swells, coinciding with the observations
recorded by Prez-Gonzlez et al. (1992a).
The periodic inversion in the proportions of P.
gracilis and P. inflatus in commercial catches has
previously been observed along the Mexican Pacific
coast (Briones-Fourzn & Lozano-lvarez, 1992;
Valadez-Manzano et al., 2003; Arzola-Gonzlez et al.,
2007). Tangle nets and SCUBA diving are the fishing
methods utilized in the south of this region of the
Pacific Ocean and are associated with the different
proportions of these species obtained in the
commercial catches. Briones-Fourzn & Lozano-
lvarez (1992) and Valadez-Manzano et al. (2003)
suggested that this pattern is related to the habitats of
 Population structure of Panulirus gracilis 231

Table 3. Monthly mean size, standard deviation and size range whole and by sex of the total weight (W, in g), Panulirus
gracilis, during 1989-1990 and 1990-1991 fishing seasons in the lower part of the Gulf of California, Mexico.
Tabla 3. Nmero de hembras y machos de Panulirus gracilis e intervalos de talla, medias y desviaciones estndar
mensuales del peso total (W, en g), durante las temporadas de pesca 1989-1990 y 1990-1991 en la parte baja del golfo de
California, Mxico.

Fishing season 1989-1990

Total Males Females
Month n W n Range W n Range W
X SD W (g) X SD W (g) X SD
Sep 132 355.0 85.1 100 205-780 338.2 73.8 32 220-630 407.4 97.3
Oct 143 369.7 87.3 105 230-590 345.1 61.8 38 230-695 437.8 109.9
Nov 158 377.4 115.1 93 175-1075 361.7 102.5 65 230-795 399.9 128.6
Dec 168 395.3 114.3 90 195-755 394.2 104.5 78 165-700 396.6 125.3
Jan 142 405.5 102.7 72 220-630 402.4 94.3 70 200-790 408.6 111.4
Feb 125 410.4 106.0 66 205-655 427.7 98.6 59 220-695 391.0 111.4
Mar 178 378.2 116.5 67 84-960 388.7 150.7 111 135-720 371.9 90.2
Apr 267 414.3 113.4 87 150-960 426.4 139.2 180 230-735 408.4 98.5
May 272 396.6 139.8 69 47-730 317.3 142.6 203 105-840 423.6 128.5

Fishing season 1990-1991

Total Males Females
Month n W n Range W n Range W
X SD W (g) X SD W (g) X SD

Sep 46 413.5 119.5 34 200-780 407.1 114.6 12 205-650 431.7 136.1

Oct 168 421.4 123.2 99 75-850 417.3 105.7 69 175-975 427.1 145.3
Nov 153 390.9 75.1 98 280-550 388.1 62.6 55 270-725 396.0 93.7
Jan 261 365.1 106.2 146 105-730 360.3 111.6 115 195-860 371.1 99.0
Feb 237 377.8 112.4 108 110-850 360.9 110.5 129 120-770 391.9 112.5
Mar 278 400.7 104.6 94 240-870 401.9 110.9 184 270-725 400.2 101.5
Apr 176 364.5 110.7 32 90-870 318.1 171.3 144 100-640 374.8 89.7
May 190 341.0 133.1 49 130-860 300.6 150.4 141 140-790 355.0 124.1

each species. These authors indicated that fishermen Size distribution

deployed their nets on the type of bottom where P.
gracilis is more abundant to select for this species,
whereas divers prefer rocky bottoms, where visibility
is better, thus obtaining larger proportions of P.
inflatus.
Additionally, Prez-Gonzlez et al. (2002b)
reported that the abundance of P. gracilis and P.
inflatus varies as a function of depth. In the study area
(see Fig. 1), the bottoms are rocky between 0.5 and
10-15 m and gravel-sandy from 12-15 to 35-40 m.
Therefore, P. inflatus is found inshore (0.5-15 m
depth), whereas the abundance of the P. gracilis
increases with depth. The two species coexist in a
similar proportion at depths between eight to
approximately 18 m.
The modal size of P. gracilis landed in this study (75
mm CL) during the 1989-1990 and 1990-1991 fishing
seasons was smaller than that reported by Salazar-
Navarro (2000) (85 mm CL) but similar to that
recorded by Prez-Gonzlez et al. (1992a) and Flores-
Campaa et al. (1993). However, the mean size found
contrasts with other studies performed in study area or
in adjacent zones. For example, during the 1977
fishing season, the mean sizes were higher than the
minimum legal size (MLS) of 82.0 mm CL, with the
catchable stock in the range of 75.0-110 mm CL
(Wiedfeldt, 1997), whereas, beginning in the early
1980s, the mean sizes have been lower that the MLS.
Prez-Gonzlez (1986), Quintero-Montoya (1999) and
Valadez-Manzano et al. (2003) recorded mean sizes of
232 Lat. Am. J. Aquat. Res.
72.0 < 70 and 70 mm CL during the 1983-1984, 1996-
1997/1997-1998 and 2001-2002 fishing seasons,
respectively.
Prez-Gonzlez et al. (2002a) reported that, as a
consequence of the high fishing mortality in sublegal
sizes, the stock-turnover rate has increased, with an
equivalent decrease in the age at first maturity and an
increase in mean fecundity, suggesting a low rate of
compliance with fishery regulations due to a lack of
strict enforcement. Fishing pressure on sublegal sizes
of the spiny lobsters P. gracilis and P. inflatus,
including a high proportion of immature individuals,
has increased since the early 1990s. Similarly, in the
present study, we observed that ovigerous females
were also being captured.
Yallonardo et al. (2002) did not find changes in the
size frequency in the spiny lobster P. guttatus between
1986-1988 and 1998-99, suggesting that fishing
pressure on this resource had not yet been increased to
the point that it negatively affected the size structure
of the population. Montgomery (1995) and Padilla-
Ramos & Briones-Fourzn (1997) indicated that the
fishing locality and/or pattern of movement of lobsters
along the shore could be additional factors influencing
the size composition of the catch and should be taken
into account when analyzing the mean monthly size of
the catch.
Sex ratio
As found in the present study, a P. gracilis sex ratio
close to unity has been reported by Weinborn (1977);
Briones et al. (1981); Prez-Gonzlez et al. (1992b);
Flores-Campaa et al. (1993) and Salazar-Navarro
(2000). However, Arzola-Gonzlez et al. (2007) found
that the sex ratio favored males over females in the
1995 (2.6:1), 1996 (1.6:1) and 1997 (2.4:1) fishing
seasons.
MacDiarmid & Sainte-Marie (2006) suggested that
many fisheries appear to have the potential to alter
population sex ratio and sexual size dimorphism, and
they noted a number of factors that could result in sex-
biased exploitation. For example, one sex may be
more vulnerable to capture due to its greater spatial
and/or temporal exposure to fishing gear. Goi et al.
(2001) reported that the scarcity of males in February
may indicate a substantial sex segregation of the
Palinurus elephas population at this time, but the
presence of recent postmolt males in the samples also
suggested reduced activity and, thus, catchability,
related to ecdysis. A decrease of approximately 70%
in catchability has been estimated for late-postmolt
Panulirus argus (Lipcius & Herrnkind, 1982) and P.
cygnus (Morgan, 1974). In several species, males are
more catchable than females, and larger males are
more catchable than smaller males (e.g., Tremblay &
Smith, 2001; Ziegler et al., 2002).
The seasonal disparity in the sex ratio of P. gracilis
has been associated with the differential male and
female movements associated with their reproductive
activity, which occurs in summer and autumn (Prez-
Gonzlez et al., 1992b; Briones-Fourzn & Lozano-
lvarez, 1992; Arzola-Gonzlez et al., 2007). This
timing of the main reproductive period in P. gracilis is
evidenced by the higher abundance of larvae
phyllosoma found in the study area from June to
October (Muoz-Garca et al., 2000, 2004), as well as
by the observations of a higher value of the
gonadosomatic index and the most females with
mature gonads during these months (Puga-Lpez,
2004).
The catch rates of male lobsters were higher during
the reproductive period (summer and autumn) than
those of females, which were more abundant during
spring (the nonreproductive period). After mating and
oviposition, the bulk of the female population is
expected to migrate to deeper waters during egg
development and to return to inshore areas prior to egg
hatching. This suggests that P. gracilis females are
less catchable than males during their reproductive
period because the bulk of the female population
probably migrates to deeper waters and/or presents
decreased activity. This pattern of movement of the
females toward deeper waters has been observed in P.
argus in the northern Caribbean and Bahamas
(Herrnkind, 1980, 1985; Kanciruk, 1980), south of
Florida (Gregory & Labisky, 1986), on the continental
shelf of the Quintana Roo, Mexico (Lozano-lvarez et
al., 1991), and in the northwest islands of the Cape
Verde Archipelago (east-central Atlantic) (Freitas &
Castro, 2005); it has also been observed in P. ornatus
in the Gulf of Papua (Bell et al., 1987, Pitcher et al.,
1992), in P. guttatus on the Caribbean coast of Mexico
(Padilla-Ramos & Briones-Fourzn, 1997), and in
Palinurus elephas in the western region of the
Mediterranean Sea (Goi et al., 2001).
Panulirus inflatus presents similar patterns of
reproductive activity and male and female movements
related to mating, oviposition, egg development and
egg hatching (Prez-Gonzlez et al., 1992b, Briones-
Fourzn & Lozano-lvarez, 1992; Arzola-Gonzlez et
al., 2007). This species coexists with P. gracilis along
the Mexican Pacific coast and in the lower part of the
Gulf of California.
Kanciruk (1980) indicated that differences between
male and female movements appear to cause these
unbalanced sex ratios in a number of other spiny
lobster species. Maturing adults of most well-studied
palinurid species exhibit either an incremental
 Population structure of Panulirus gracilis
ontogenetic migration that culminates in mating and
spawning in distinct adult habitats or seasonal inshore-
offshore movements for mating or foraging (Butler et
al., 2006).
There are other factors that could result in sex-
biased exploitation. For example, the male-skewed sex
ratio observed for P. guttatus (Losada-Tosteson et al.,
2001) has been associated with the method of capture
(traps vs handpicking, Briones-Fourzn, 1991), lower
catchability (Evans & Lockwood, 1994), differential
male and female movements associated with their
reproductive activity (Briones-Fourzn & Contreras-
Ortiz, 1999), and lower abundance due to differential
mortality (Evans et al., 1995; Sharp et al., 1997).
Furthermore, Losada-Tosteson et al. (2001) indicated
that the evolutionary mechanics of skewed sex ratios
in P. guttatus, if they exist, require further study.
Thus, obtaining information on the quantity and
size composition of individuals harvested and changes
in the abundance of species is fundamental for the
effective management of fishery resources. Such data
provide knowledge about the impact of harvesting on
the population and on the temporal and spatial
distributions of individuals of different sizes
(Montgomery, 1995). For this reason, periodic
evaluations of the lobster fishery should be conducted
to improve monitoring of the status of this fishery on
the Mexican Pacific and Gulf of California coasts.
ACKNOWLEDGEMENTS
The author thanks Luis M. Valadez and Martn I.
Borrego for their help in field (sampling) activities.
Commercial samples were obtained from catches of
the Sociedades Cooperativas Punta Tiburn and
Jos Mara Canizalez. This project was supported by
the Secretara de Educacin Pblica, Mxico.
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Lat. Am. J. Aquat. Res., 39(2): 236-249, 2011 Lat. Am. J. Aquat. Res. 236
DOI: 10.3856/vol39-issue2-fulltext-5

Research Article

Distribucin del ictioplancton en la Patagonia austral de Chile: potenciales efectos

del deshielo de Campos de Hielo Sur

Mauricio F. Landaeta1,, Claudia A. Bustos2, Pamela Palacios-Fuentes1, Pablo Rojas3 &

Fernando Balbontn1
1
Facultad de Ciencias del Mar y de Recursos Naturales, Universidad de Valparaso
P.O. Box 580, Reaca, Via del Mar, Chile
2
Programa Doctorado en Acuicultura, Universidad Catlica del Norte, P.O. Box 117, Coquimbo, Chile
3
Divisin de Investigacin en Acuicultura, Centro de Maricultura Hueihue
Instituto de Fomento Pesquero, Ancud, Chile

RESUMEN. Durante octubre-noviembre de 2009 se realiz un crucero oceanogrfico entre 50 y 53S de

Chile austral, en las cercanas del glaciar Campos de Hielo Sur. Las estaciones cercanas al glaciar presentaron
baja temperatura (1-3C) y salinidad (< 25), y alta estabilidad (frecuencia de Brunt-Visl N > 0,1 ciclos s-1).
Los principales taxa del ictioplancton fueron huevos y larvas de sardina fueguina Sprattus fuegensis, pez hacha
Maurolicus parvipinnis, Macrouridae y merluza austral Merluccius australis. El desove principal de S.
fuegensis (~ 8000 huevos 10 m-2) ocurri en zonas mezcladas de la plataforma continental adyacente, mientras
que el desove de M. parvipinnis ocurri en canales intermedios asociado a valores intermedios de estabilidad
(N~0,06 ciclos s-1). Se observ una nula o baja abundancia de huevos y larvas de peces en las cercanas del
glaciar, y la abundancia de huevos de M. parvipinnis estuvo relacionada positivamente con la temperatura y
salinidad de la columna de agua y negativamente con la estabilidad de la columna de agua. Adems, hubo una
relacin negativa entre la densidad del agua de mar y el dimetro de los huevos de S. fuegensis. La relacin
entre deshielo e ictioplancton podra tener consecuencias en el transporte advectivo y mortalidad masiva de
huevos y larvas de peces y el acople pelgico-bentnico en la Patagonia austral de Chile. Como el cambio
climtico global ha incrementado los deshielos de glaciares en latitudes altas, y el aumento del ingreso de
aguas de baja temperatura y salinidad podra tener consecuencias en el ictioplancton de la Patagonia chilena.
Palabras clave: estratificacin, distribucin, ictioplancton, Campo de Hielo Sur, sur de Chile.

Ichthyoplankton distribution in South Patagonia, Chile: potential effects of ice

melting from the Southern Ice Field

ABSTRACT. In October-November 2009, an oceanographic survey was carried out between 50 and 53S off
southern Chile, near the Southern Ice Field. The stations near the glacier showed low temperatures (1-3C) and
salinity (< 25), and high stability (Brunt-Visl frequency N > 0.1 cycles s-1). Main ichthyoplankton taxa
were eggs and larvae of southern sprat Sprattus fuegensis, lightfish Maurolicus parvipinnis, Macrouridae, and
southern hake Merluccius australis. The main spawning area of S. fuegensis (~8000 eggs 10 m-2) occurred in
mixed zones of the adjacent continental shelf, whereas the spawning of M. parvipinnis occurred in
intermediate channels associated with medium stability values (N~0.06 cycles s-1). Fish egg and larval
abundances were null or scarce near the glacier, and the abundance of M. parvipinnis eggs was positively
related to the temperature and salinity of the water column, and negatively related to water column stability.
Moreover, a negative relationship was observed between seawater density and the diameter of S. fuegensis
eggs. The relation between ice melting and ichthyoplankton may have consequences for advective transport
and mass mortality of fish eggs and larvae, as well as pelagic-benthic coupling in the Chilean South Patagonia.
Global climate change has increased glacier ice melting at high latitudes, and the increased entry of colder,
less saline waters in coastal areas may have consequences for the ichthyoplankton in the Chilean Patagonia.
Keywords: stratification, distribution, ichthyoplankton, Southern Ice Field, southern Chile.

___________________
Corresponding author: Mauricio F. Landaeta (mauricio.landaeta@uv.cl)
237 Deshielos y distribucin de ictioplancton en la Patagonia, Chile
INTRODUCCIN
La zona sur austral de Chile (4130S-56S) se
caracteriza por presentar una geometra costera
compleja, caracterizada por fiordos, islas, canales y
archipilagos, con una longitud de 1600 km y un rea
superficial de aproximadamente 240.000 km2 (Palma
& Silva, 2004). A lo largo de esta zona tambin hay
numerosos aportes de agua dulce, provenientes de
descargas de ros de rgimen pluvial, nival y mixto
(Dvila et al., 2002), de lluvias (2000-5000 mm ao-1,
Strub et al., 1998) y deshielos de glaciares, que
generan una capa superficial de agua de baja densidad
con una fuerte picnoclina a aproximadamente 20-30 m
de profundidad y una capa profunda de mayor
densidad. Como consecuencia de esto, el sistema se
comporta como un estuario, con una capa superficial
de mayor velocidad que se mueve hacia fuera de la
costa y una capa profunda que ingresa al sistema con
menor velocidad (Silva et al., 1997).
Este sistema estuarino presenta fuertes variaciones
estacionales en la incidencia de radiacin solar que
afectan significativamente la variabilidad de la
biomasa fitoplanctnica y la produccin primaria en la
capa de mezcla (Iriarte et al., 2007), produciendo
cambios en la estructura del ecosistema desde una
clsica trama trfica pelgica en primavera a una
trama microbiana en invierno (Gonzlez et al., 2010).
Acoplado al aumento de fitoplancton coincide una
mayor actividad reproductiva en primavera de
crustceos decpodos (Mujica & Medina, 2000;
Mujica & Nava, 2010) y peces marinos (Landaeta &
Castro, 2006a; Landaeta et al., 2009), cuando se
presenta mayor oferta alimenticia y menor cantidad de
predadores gelatinosos (p.e., Chaetognatha, Sagitta
spp., Eukrohnia hamata, Villenas et al., 2009).
Por otra parte, a lo largo de Chile austral ocurren
cambios en los aportes de agua dulce, que generan dos
zonas de muy baja salinidad cerca de 44-46S (por
aportes de ros de alto caudal) y alrededor de 52-53S
(por efecto de deshielos, Dvila et al., 2002) y que no
slo incrementan la estabilidad de la columna de agua,
sino que aumentan los gradientes verticales y
horizontales de densidad. De esta forma ocurre
agregacin de partculas en estas zonas frontales,
desde parches de alimento planctnico (Landaeta &
Castro, 2006b) hasta macroalgas flotando a la deriva
(i.e., Macrocystis pyrifera y Durvillaea antarctica,
Hinojosa et al., 2010). Aunque se han postulado
relaciones positivas significativas entre la abundancia
de estados tempranos de peces y la estabilidad en la
zona norte de la Patagonia Chilena (Bustos et al.,
2007, 2008a, 2008b), que podran tener consecuencias
positivas para la alimentacin larval (Landaeta &
Castro, 2006b), recientemente, se ha detectado que en
zonas donde ocurren deshielos (i.e., baja temperatura
y salinidad), tanto la diversidad como la abundancia
de huevos y larvas de peces es baja (Bustos et al.,
2010).
Los deshielos de glaciares pueden causar
mortalidad masiva de zooplancton, particularmente
durante verano, con estimaciones de biomasa muerta
de 0,17 gC m-2 (Wslawski & Legezyska, 1998). Los
mecanismos que generan mortalidad asociados a una
fuente de agua dulce se deben a la incapacidad del
zooplancton de evadir el agua de baja salinidad por la
mezcla turbulenta y morir por estrs osmtico
(Kaartvedt & Aksnes, 1992; Eiane & Daase, 2002).
Por lo tanto, es posible hipotetizar que la distribucin
espacial y la abundancia de estados tempranos de
peces para aquellas especies que usan esta rea como
zona de desove y crianza larval temprana podran ser
afectados por los deshielos de Campo de Hielo Sur en
la zona austral de Chile (50-53S). El objetivo del
presente trabajo es establecer la distribucin espacial
del ictioplancton en la zona de influencia del glaciar
Campos de Hielo Sur durante la poca de primavera
austral, relacionar la abundancia con variables
ambientales y sugerir posibles consecuencias del
incremento del deshielo producto del cambio
climtico global en la Patagonia Chilena.
MATERIALES Y MTODOS
Durante octubre y noviembre de 2009 se realiz un
crucero oceanogrfico entre 5006S y 5245S a
bordo del buque cientfico AGOR Vidal Gormaz (Fig.
1), que comprendi el muestreo de 40 estaciones. En
cada una de ellas se midieron las variables
hidrogrficas de la columna de agua con un CTD
Seabird SB-19 desde la superficie hasta 500 m de
profundidad o hasta 10 m por sobre el fondo. El
zooplancton fue capturado mediante lances doble
oblicuos con una red Tucker trawl (1 m2 de boca,
mallas de 300 m de apertura), con sistema de dos
redes y flujmetro para estimar el volumen filtrado de
cada red. Una vez a bordo, las redes fueron lavadas y
las muestras de los lances de bajada (p.e., 0-200 m)
fueron preservadas en formalina al 4% tamponeada
con borato de sodio, y las muestras de los lances de
subida (p.e., 200-0 m) fueron fijados con etanol al
75%, para anlisis de otolitos (no incluidos). Los
volmenes filtrados variaron entre 22,74 y 897,20 m3
lance-1 (promedio desviacin estndar, 221,94
150,94 m3 lance-1).
En laboratorio, se separaron los huevos y larvas de
peces de las muestras preservadas en formalina. El
 Lat. Am. J. Aquat. Res. 238

Figura 1. Zona de estudio, indicando la posicin de las estaciones de muestreo y transectas.

Figure 1. Study area, showing location of sampling stations and transects.

ictioplancton fue identificado hasta el nivel
taxonmico ms bajo posible basado en las
descripciones de Ciechomski (1971); Moser (1996);
Balbontn et al. (2004); Uribe & Balbontn (2005);
Bustos & Landaeta (2005) y Landaeta et al. (2008).
Los huevos fueron contados y separados en tres
estados: (a) estado I, sin embrin, (b) estado II, con
embrin temprano y (c) estado III, pre-eclosin. Se
tomaron aleatoriamente huevos de sardina fueguina
Sprattus fuegensis para medir su dimetro. Se
realizaron tres medidas de dimetro de cada huevo -
independiente de su estado de desarrollo- bajo una
lupa estereomicroscpica Olympus SZ-61 con cmara
digital Moticam 2000 (2.0M Pxel), usando el
software Motic Images Plus 2.0 y se calcul el
promedio de las tres mediciones de tamao de cada
huevo. Se comprob la normalidad de los datos de
tamao de los huevos con una prueba de Shapiro-
Wilks. La abundancia de huevos y larvas de peces fue
estandarizada en individuos por 10 m2 (ind 10 m-2).
Con la informacin del CTD, se calcul como
estimador de la estabilidad de la columna de agua para
cada una de las estaciones oceanogrficas, la
frecuencia de Brunt-Visl (N = [(g/) x (/z)]1/2),
donde g es la gravedad (9,8 m s-2), es la densidad del
agua de mar, y z es la profundidad, que es la
frecuencia a la cual oscilar una partcula desplazada
verticalmente dentro de un ambiente estticamente
estable.
Se realizaron regresiones lineales simples por
mnimos cuadrados entre las variables ambientales
(temperatura, salinidad, estabilidad), el dimetro de
los huevos de S. fuegensis y la abundancia
estandarizada de huevos y larvas de algunos taxa
seleccionadas, calculando el 95% de intervalo de
confianza de los modelos lineales. Los valores de
temperatura y salinidad correspondieron al promedio
de los datos recolectados por el CTD en la columna de
agua muestreada por la red. El valor de estabilidad
corresponde al valor mximo obtenido en la columna
239 Deshielos y distribucin de ictioplancton en la Patagonia, Chile
de agua de cada una de las estaciones oceanogrficas.
Los valores de abundancia del ictioplancton y
frecuencia de Brunt-Visl fueron transformados con
logaritmo en base 10.
Para investigar la relacin entre las variables
oceanogrficas con la abundancia del ictioplancton se
utiliz el Anlisis de Componentes Principales (ACP)
(Jongmann et al., 1995). Este anlisis permite
identificar un mnimo de componentes funcionales
(variables oceanogrficas) que pueden explicar la
distribucin de las variables dependientes (huevos y
larvas de peces). Adicionalmente, se utiliz la prueba
de correlacin R de Spearman (Hays, 1981) para
investigar la relacin entre las diferentes variables
oceanogrficas con la abundancia de larvas y huevos
de las diferentes taxa.
RESULTADOS
Caractersticas hidrolgicas y estabilidad de la
columna de agua
Las condiciones hidrolgicas de la columna de agua
en la zona de estudio estuvieron influidas por los
deshielos del glaciar Campos de Hielo Sur (CHS)
(Tabla 1, Figs. 2 y 3). Se detectaron bajas
temperaturas (1,4C) y bajas salinidades (14,62) en las
cercanas al glaciar, generando aguas de baja densidad
del agua (t = 11,47 kg m-3) y alta estabilidad de la
columna de agua (0,16 ciclos s-1) (Tabla 1).
Espacialmente, se observ que en el seno Europa
ocurri una inversin trmica entre 5 a 20 m de
profundidad, con aguas de baja temperatura (1-3C) y
baja salinidad (< 25) provenientes de deshielos de
CHS, y un gradiente horizontal de densidad entre seno
Europa y canal Concepcin. Esto provoc una
columna de agua altamente estratificada y estable en
los primeros 40 m de la columna de agua del seno
Europa, con valores de frecuencia de Brunt-Visl
mayores a 0,1 ciclos s-1 (Fig. 2). En cambio, en la boca
del canal Concepcin y en la plataforma continental
adyacente, se detectaron valores de temperatura > 8C,
salinidad > 31 y una columna de agua altamente
mezclada (N < 0,025 ciclos s-1) (Fig. 2).
En el golfo Almirante Montt, con cierta influencia
de CHS, se detectaron aguas de baja temperatura
(~7C), salinidad (< 25), densidad (< 20 kg m-3) y
mayor estabilidad (N > 0,025 ciclos s-1) (Fig. 3). Se
observ que el Paso M. Vicua, una morrena que
reduce la profundidad mxima a ~55 m, impidi la
intrusin de aguas de origen ocenico (> 8C, > 31, >
24 kg m-3) al interior del golfo Almirante Montt.
Adems, a lo largo de los canales Smyth y Unin (Fig.
1), la picnoclina y la mayor estabilidad se encontraron
aproximadamente a 50 m de profundidad (Fig. 3).
Para el rea y periodo de estudio hubo una relacin
significativa entre la temperatura promedio de la
columna de agua muestreada y el valor mximo
estimado de la frecuencia de Brunt-Visl (F = 15,88;
g.l. 1, 33; P < 0,001), al igual que con la salinidad (F =
6,72; g.l. 1, 33; P = 0,014). Es decir, las zonas que
presentaron baja temperatura y baja salinidad (i.e.,
zonas de deshielo) fueron altamente estables, y por
tanto, N es un buen estimador del efecto de deshielo
en la zona de estudio.
Composicin y distribucin del ictioplancton
Durante el crucero oceanogrfico realizado en
primavera de 2009 se recolect un total de 5511
huevos y 676 larvas de peces, correspondientes a 22 y
19 taxa, respectivamente (Tablas 2 y 3). Los huevos
de sardina fueguina Sprattus fuegensis y el pez hacha
Maurolicus parvipinnis fueron los ms importantes
durante el periodo de estudio, con 64,6 y 28,1% de
dominancia, respectivamente. Otros taxa importantes
en el rea de estudio fueron los huevos de merluza
austral Merluccius australis, pejerrata (familia
Macrouridae) y lenguado austral (Hippoglossina sp.,
probablemente H. mystacium) (Tabla 2). Entre las
larvas de peces, los taxa ms importantes fueron M.
parvipinnis, S. fuegensis, Bathylagichthys parini,
Macrouridae, Sebastes oculatus y M. australis (Tabla
3). Cabe destacar la recoleccin por primera vez en
aguas chilenas de una postlarva de 12,4 mm de
Psychrolutes marmoratus (Psychrolutidae), carac-
terizada por un cuerpo globoso, fuertemente pig-
mentado, con presencia de estructuras espinosas en la
zona frontal de la cabeza, supraocular y dorsalmente a
la altura de la insercin de la aleta pectoral1.
Los huevos recientemente desovados (estado I) de
S. fuegensis fueron recolectados a lo largo del canal
Concepcin y en la plataforma continental adyacente,
a lo largo del estero Las Montaas (que no tiene
conectividad con CHS) y en el golfo Almirante Montt
(Fig. 4). Los huevos ms desarrollados y las larvas se
recolectaron en estas mismas reas, destacando las
mayores abundancias (~8000 huevos 10 m-2) sobre la
plataforma continental y su ausencia en las estaciones
ms cercanas al glaciar. Se detectaron bajas
abundancias (< 100 ind 10 m-2) de huevos y larvas en
las cercanas del Estrecho de Magallanes (Fig. 4). Un
patrn totalmente diferente present la distribucin
espacial de los estados tempranos del pez hacha M.
parvipinnis. En general, los canales (Concepcin,
Sarmiento, Unin, Smyth) fueron utilizados como
1
http://ictioplanctonenchile.blogspot.com/2010/05/postlarva-
de-psychrolutidae.html
 Lat. Am. J. Aquat. Res. 240

Tabla 1. Resumen de las condiciones hidrogrficas presentes durante el crucero CIMAR 15 en octubre-noviembre de
2009.
Table 1. Summary of hydrographic conditions found during the cruise CIMAR 15 in October-November 2009.

Temperatura (C) Salinidad t (kg m-3) Brunt-Visl (ciclos s-1)

Mnimo 1,428 14,626 11,479 0
Mximo 9,472 33,484 26,073 0,165
Promedio 8,260 31,586 24,549 0,012
Desviacin estndar 0,861 3,148 2,386 0,013
Mediana 8,595 33,017 25,595 0,007

Figura 2. Secciones verticales de condiciones oceanogrficas de la transecta con lnea continua indicada en la Figura 1.
Los puntos indican los datos extrados de los lances de CTD.
Figure 2. Vertical sections of oceanographic conditions of continuos line transect showed in Figure 1. Dots correspond to
data from CTD casts.

zonas de desove (Fig. 5), con abundancias totales de
los huevos entre 40 y 897 huevos 10 m-2 (Tabla 2), y
con una distribucin espacial similar de las larvas. La
abundancia fluctu entre 3 y 293 larvas 10 m-2 (Tabla
3). No obstante, en las estaciones ms cercanas al
glaciar no se detectaron huevos de esta especie y se
recolectaron bajas densidades (0-13 ind 10 m-2) de
larvas de M. parvipinnis (Fig. 5).
Aguas de deshielo y su relacin con el ictioplancton
Los huevos de sardina fueguina presentaron un rango
amplio de tamaos, variando entre 0,922 y 1,361 mm
(n = 127), con distribucin normal de los dimetros
(prueba de Shapiro-Wilks, W = 0,992, P = 0,719)
(Fig. 6a). Los huevos de mayor tamao (> 1,25 mm)
fueron recolectados en aguas de menor temperatura (<
7C) y salinidad (< 21), producto de los deshielos, que
generaron aguas de baja densidad (t = 16-17 kg m-3,
Fig. 6b). De hecho, el dimetro de los huevos de S.
fuegensis tuvo una relacin negativa y significativa (P
< 0,001) con la densidad del agua de mar (Fig. 6b).
De los otros componentes del ictioplancton, slo la
abundancia de los huevos del pez hacha Maurolicus
241 Deshielos y distribucin de ictioplancton en la Patagonia, Chile

Figura 3. Secciones verticales de condiciones oceanogrficas de la transecta con lnea segmentada indicada en la Figura
1. Los puntos indican los datos extrados de los lances de CTD.
Figure 3. Vertical sections of oceanographic conditions of dotted line transect showed in Figure 1. Dots correspond to
data from CTD casts.

Tabla 2. Composicin y abundancia (ind 10 m-2) de huevos de peces capturados durante primavera de 2009. DE:
desviacin estndar. Dominancia es el porcentaje de abundancia del taxon con respecto a la abundancia total. Ocurrencia
es el porcentaje de estaciones oceanogrficas con presencia positiva del taxon con respecto al total de estaciones
muestreadas.
Table 2. Composition and abundance (ind 10 m-2) of fish eggs collected in spring 2009. DE: standard deviation.
Dominance is the percentage of taxon abundance in relation to the whole abundance. Occurrence is the percentage of
oceanographic stations with positive presence of taxon respective to total sampled stations.

Taxa Media DE Mediana Dominancia Ocurrencia Rango de abundancia

(%) (%)
Sprattus fueguensis 946,60 2613,10 21,54 64,60 45,00 2,23 - 8163,38
Maurolicus parvipinnis 246,70 267,90 126,85 28,06 75,00 8,34 - 897,03
Merluccius australis 63,07 165,89 11,94 3,35 35,00 2,23 - 634,81
Normanichthys crockeri 15,87 - 15,87 0,06 2,50 15,87
Genypterus blacodes 7,47 0,51 7,54 0,08 7,50 6,93 - 7,94
Macroronus magellanicus 6,47 1,80 6,47 0,05 5,00 5,19 - 7,75
Lampanyctodes hectoris 4,46 - 4,46 0,02 2,50 4,46
Prolatilus jugularis 3,11 - 3,11 0,01 2,50 3,11
Hippoglossina sp. 25,98 22,56 24,02 0,30 7,50 4,46 - 49,45
Macrouridae 26,18 36,77 12,01 1,29 32,50 3,40 - 118,83
Pinguipedidae 6,18 - 6,18 0,02 2,50 6,18
Huevos no identificados 21,12 45,38 11,84 2,16 67,50 2,22 - 243,84
 Lat. Am. J. Aquat. Res. 242

Tabla 3. Composicin y abundancia (ind 10 m-2) de larvas de peces capturadas durante primavera de 2009. DE:
desviacin estndar. Dominancia es el porcentaje de abundancia del taxon con respecto a la abundancia total. Ocurrencia
es el porcentaje de estaciones oceanogrficas con presencia positiva del taxn con respecto al total de estaciones
muestreadas.
Table 3. Composition and abundance (ind 10 m-2) of fish larvae collected in spring 2009. DE: standard deviation.
Dominance is the percentage of taxon abundance in relation to the whole abundance. Occurrence is the percentage of
oceanographic stations with positive presence of taxon respective to total sampled stations.

Taxa Media DE Mediana Dominancia Ocurrencia Rango de abundancia

(%) (%)
Sprattus fuegensis 54,61 70,19 23,39 18,09 42,50 3,77 - 249,40
Bathylagichthys parini 53,91 75,41 15,09 17,86 42,50 5,68 - 222,79
Maurolicus parvipinnis 66,06 69,59 44,56 42,47 82,50 3,11 - 293,72
Merluccius australis 17,75 19,28 9,21 4,15 30,00 5,19 - 73,35
Macruronus magellanicus 24,02 - 24,02 0,47 2,50 24,02
Macrouridae 23,38 25,55 12,01 5,01 27,50 3,11 - 89,12
Genypterus blacodes 19,78 13,48 19,11 1,54 10,00 7,52 - 33,36
Cataetyx messieri 9,85 2,13 9,85 0,38 5,00 8,34 - 11,35
Sebastes oculatus 15,63 16,92 11,78 4,87 40,00 4,97 - 74,18
Helicolenus lenguerichi 3,11 - 3,11 0,06 2,50 3,11
Agonopsis chiloensis 3,11 - 3,11 0,06 2,50 3,11
Leptonotus blainvilleanus 10,16 - 10,16 0,20 2,50 10,16
Psychrolutes marmoratus 3,78 - 3,78 0,07 2,50 3,78
Notothenia sp. 1 9,49 5,43 9,33 0,92 12,50 3,78 - 17,03
Notothenia sp. 2 8,85 0,90 8,89 0,52 7,50 7,94 - 9,73
Seriolella caerulea 7,56 6,29 7,56 0,29 5,00 3,11 - 12,01
Sp. A 6,18 - 6,18 0,12 2,50 6,18
Sp. B 5,32 0,50 5,32 0,21 5,00 4,97 - 5,68
Sp. C 6,93 - 6,93 0,14 2,50 6,93
No identificado 16,45 13,20 14,14 2,57 20,00 5,29 - 44,28

parvipinnis se relacion significativamente con las
variables ambientales de la columna de agua (Fig. 7).
Se encontr una reduccin significativa de la
abundancia de sus huevos en zonas con menor
temperatura (relacin positiva, Fig. 7a, P = 0,0060),
menor salinidad (relacin positiva, Fig. 7b, P =
0,0007) y mayor estabilidad de la columna de agua
(relacin negativa, Fig. 7c, P = 0,0063), correspon-
dientes a las estaciones cercanas a CHS.
Los dos primeros componentes principales (ACP)
explicaron el 70% de la varianza. La contribucin de
las estaciones con mayor abundancia de ictioplancton
con las variables oceanogrficas de los dos primeros
componentes fue utilizada para realizar asociaciones
estadsticas entre ambos tipos de variables. Se
detectaron tres tipos de asociaciones entre las
diferentes estaciones de muestreo y las variables
oceanogrficas (Fig. 8). El primer grupo compuesto
por el 63% de las estaciones se asoci positivamente
con valores intermedios de estabilidad vertical (~ 0,06
ciclos s-1) de la columna de agua. Una importante
proporcin de la abundancia total del ictioplancton
(34% huevos; 51% larvas) se concentr en este grupo.
Un segundo conjunto, compuesto por diez estaciones
(25%) se asoci negativamente con valores de
temperatura del mar cercanos a 7C. A diferencia del
grupo anterior, ste congreg la mayor abundancia de
huevos de peces (66%) y, a un 47% del total de larvas
de peces. Finalmente, el tercer grupo compuesto por
cuatro estaciones (10%) se asoci positivamente con
valores de densidad del mar cercanos a 23 kg m-3. Esta
agrupacin slo represent a un 2% de la abundancia
total de larvas y, menos del 1% de la abundancia total
de huevos de peces (Fig. 8).
El anlisis de correlacin R de Spearman realizado
con las larvas de peces, mostr relaciones positivas
243 Deshielos y distribucin de ictioplancton en la Patagonia, Chile

Figura 4. Distribucin espacial de huevos por estado de desarrollo y larvas de sardina fueguina Sprattus fuegensis durante
primavera de 2009. Abundancia estandarizada a ind 10 m-2.
Figura 4. Spatial distribution of eggs by developmental stage and larval southern sprat Sprattus fuegensis during austral
spring 2009. Standardised abundance in ind 10 m-2.

estadsticamente significativas con un bajo coeficiente estadios tempranos de B. parini (Bathylagidae)

de correlacin (r = ~ 0,4) entre los estadios tempranos
de M. parvipinnis y las condiciones hidrolgicas de la
columna de agua (Tabla 4). Las larvas de Seriolella
caerulea (cojinoba del sur) presentaron relaciones
positivas significativas con la salinidad y densidad de
la columna de agua. Cabe destacar que solo los
mostraron relaciones positivas significativas con la
frecuencia de Brunt-Visl. Finalmente, el total de
larvas de peces mostr relaciones positivas
significativas con un bajo coeficiente de correlacin (r
= ~0,4) slo con valores de temperatura, salinidad y
densidad (Tabla 4).
 Lat. Am. J. Aquat. Res. 244

Figura 5. Distribucin espacial de huevos por estado de desarrollo y larvas de pez hacha Maurolicus parvipinnis durante
primavera de 2009. Abundancia estandarizada en ind 10 m-2.
Figura 5. Spatial distribution of eggs by developmental stage and larval lightfish Maurolicus parvipinnis during austral
spring 2009. Standardised abundance in ind 10 m-2.

Para los huevos de peces, el anlisis de correlacin
mostr relaciones positivas significativas entre los
huevos de Hippoglossina sp. y M. parvipinnis con
valores de temperatura, salinidad y densidad de la
columna de agua. Los huevos de merluza austral (M.
australis) mostraron relaciones positivas con un bajo
coeficiente de correlacin (r = ~0,3) con los valores de
salinidad y densidad. Los huevos de peces de la
familia Macrouridae mostraron relaciones positivas
significativas con las variables fsicas, al igual que el
total de huevos colectados en el ara de estudio (Tabla
4).
DISCUSIN
El anlisis del ictioplancton presente en la zona sur
austral de Chile cercana a uno de los glaciares ms
grandes del Hemisferio Sur, permiti establecer que
en primavera de 2009 las aguas de baja temperatura y
245 Deshielos y distribucin de ictioplancton en la Patagonia, Chile

Figura 6. a) Histograma de tamao de huevos (mm) de

sardina fueguina Sprattus fuegensis. b) Regresin lineal
entre dimetro (mm) de huevos de S. fuegensis y t (kg
m-3). Las lneas punteadas corresponden al intervalo de
confianza del 95%.
Figure 6. a) Histogram of southern sprat Sprattus
fuegensis egg size (mm). b) Linear regression between S.
fuegensis egg diameter (mm) and t (kg m-3). Dotted
lines correspond to 95% confidence level.

salinidad, y alta estabilidad provenientes de los

deshielos del glaciar afectan significativamente la
composicin y distribucin espacial de los estados
tempranos de peces marinos, el tamao de los huevos
de sardina fueguina S. fuegensis y la abundancia de
huevos de pez hacha M. parvipinnis.
Tanto los anlisis multivariados como el anlisis
individual de distribucin espacial de los taxa
mostraron que el ictioplancton se concentr en las
estaciones oceanogrficas con valores intermedios de
estabilidad (~0,06 ciclos s-1), y que hubo ausencia o
una baja abundancia de huevos y larvas en las zonas
cercanas al glaciar Campo de Hielo Sur. Los valores
de los datos ambientales (temperatura y salinidad)
Figura 7. Regresiones lineales entre el logaritmo de la
abundancia de huevos del pez hacha Maurolicus
parvipinnis y a) temperatura (C), b) salinidad y c) el
logaritmo de la frecuencia de Brunt-Visl (ciclos s-1).
Las lneas punteadas corresponden al intervalo de
confianza del 95%.
Figure 7. Linear regressions between logaritm of lighfish
Maurolicus parvipinnis egg abundance and a) tempe-
rature (C), b) salinity and c) logaritm of Brunt-Visl
frequency (cycles s-1). Dotted lines correspond to 95%
confidence level.
 Lat. Am. J. Aquat. Res.
Figura 8. Proyeccin de las variables fsicas con la
abundancia del ictioplancton mediante el anlisis de
componentes principales (ACP) en Chile austral durante
primavera de 2009.
Figure 8. Projection of physical variables and
ichthyoplankton abundance in the Principal Component
Analysis (PCA) in southern Chile during austral spring
2009.
utilizados en los anlisis de regresin correspondieron
a promedios de la columna de agua muestreada por la
red de plancton, por lo que los efectos directos de
intrusiones de aguas de baja salinidad y temperatura
estn suavizados por los valores ambientales de aguas
ms profundas, y por lo tanto es esperable que la
interaccin de las aguas superficiales con el
ictioplancton haya sido subestimada. No obstante, las
relaciones fueron significativas.
La zona austral de Chile se caracteriza por amplios
rangos de valores de estratificacin vertical (N) de la
columna de agua, entre 0,0003 y 0,539 ciclos s-1 en la
Patagonia norte (Bustos et al., 2008a) y entre 0,013 y
0,296 ciclos s-1 en la Patagonia sur (Bustos et al.,
2011), indicando una alta variabilidad espacial en las
condiciones ambientales. En la Patagonia norte se han
observado relaciones positivas entre la estratificacin
vertical y la abundancia de huevos y larvas de peces,
mientras que en la Patagonia sur se han detectado
relaciones negativas con el ictioplancton (Bustos et
al., 2008a, 2011). Esto sugiere que hay mecanismos
diferentes que generan la estratificacin vertical (p.e.,
pluviosidad versus deshielo) y que a su vez producen
diferentes respuestas en los estados tempranos de los
peces marinos.
246
El aporte de aguas fras, de baja salinidad (i.e., de
baja densidad) producto del deshielo del glaciar puede
afectar la salinidad superficial de la columna de agua
hasta 50 m de profundidad y hasta 75 km mar afuera,
generando una anomala positiva en salinidad cerca de
la costa entre 48 y 53S, e incrementa la circulacin
estuarina del sistema (Dvila et al., 2002),
transportando el zooplancton presente en la capa de
mezcla hacia los canales intermedios, ya sea en forma
pasiva o activamente en estados larvales ms
desarrollados, como se ha planteado para larvas de
cabrilla Sebastes oculatus (Landaeta & Castro,
2006b). Por otro lado, durante primavera en la zona
austral de Chile dominan vientos con direccin norte,
por lo que el transporte de Ekman resultante es hacia
el este, desacelerando la adveccin superficial fuera de
los canales (Dvila et al., 2002). Ambos mecanismos
fsicos podran explicar parcialmente el aparente
movimiento de los huevos de sardina fueguina desde
la plataforma continental hacia canal Concepcin (Fig.
4) o la mantencin de huevos y larvas de M.
parvipinnis dentro de los canales muestreados (Fig. 5).
Si el desove ocurre subsuperficialmente (p.e., bajo 50
m de profundidad), como lo realiza M. parvipinnis en
Chile central (Landaeta & Castro, 2002), el transporte
neto sera hacia el interior de los canales,
incrementando los tiempos de residencia de los
estados tempranos en la zona de estudio. En el
presente caso, es difcil establecer la posicin vertical
del desove, ya que los muestreos fueron integrados, y
M. parvipinnis ha mostrado una amplia variabilidad en
sus tcticas reproductivas en sistemas de fiordos
(Bustos et al., 2008b, 2011; Landaeta et al., 2009).
En cuanto a composicin del ictioplancton, sta fue
similar a la encontrada previamente durante la
primavera austral en otros cruceros para la zona de
estudio. Durante fines de la dcada de 1990, se
recolectaron altas densidades de larvas de merluza de
cola Macruronus magellanicus, pero sus abundancias
se redujeron considerablemente despus del 2008
(Bernal & Balbontn, 2003; Bustos et al., 2011). Otros
componentes del ictioplancton, como las larvas de M.
parvipinnis, S. fuegensis y Sebastes oculatus
mantuvieron su importancia relativa en ambos
periodos de tiempo (Bustos et al., 2011).
El tamao de los huevos de S. fuegensis present
un rango ms amplio que el descrito previamente por
Ciechomski (1971) para aguas argentinas (1,017-1,030
mm). Adems, se observ que los huevos de mayor
tamao (> 1,25 mm) se recolectaron en reas de baja
salinidad y densidad. La salinidad donde ocurre el
desove puede afectar varias propiedades de los huevos
de peces, incluyendo el dimetro y la flotabilidad
neutra (Kucera et al., 2002). Los huevos desovados en
247 Deshielos y distribucin de ictioplancton en la Patagonia, Chile

Tabla 4. Coeficientes de correlacin R de Spearman entre huevos y larvas de peces con valores promedio de temperatura
(Temp), salinidad (Sal), densidad (t) y Frecuencia Brunt-Visl (Frec. B-V) en Chile austral. *P < 0,05.
Table 4. Spearman R correlation coefficients between fish eggs and larvae with mean values of temperatura (Temp),
salinity (Sal), density (t) and Brunt-Visl frequency (Frec. B-V) in southern Chile. *P < 0.05.

LARVAS HUEVOS
Taxa Temp Sal t Frec. B-V Taxa Temp Sal Dens Frec. B-V
A. chiloensis -0,0347 0,2707 0,2707 -0,2013 G. blacodes 0,1739 0,1323 0,1241 -0,1097
B. parini 0,0784 -0,0705 -0,0696 0,3363* Hippoglossina sp. 0,3449* 0,4321* 0,4321* -0,2294
C. messieri -0,2393 -0,1578 -0,1578 0,0579 L. hectoris 0,2568 0,2291 0,2291 -0,0624
G. blacodes -0,0752 -0,2136 -0,2136 0,1098 M. magellanicus 0,0531 0,0430 0,0430 -0,0221
H. lenguerichi -0,0347 0,2707 0,2707 -0,2013 M. parvipinnis 0,5960* 0,5310* 0,5291* -0,1234
L. blainvilleanus 0,0347 -0,0347 -0,0208 0,2013 M. australis 0,1265 0,3710* 0,3856* -0,0857
M. magellanicus 0,2291 0,2568 0,2568 -0,1457 N. crockeri -0,1735 -0,2013 -0,2013 -0,1041
M. parvipinnis 0,4720* 0,3534* 0,3492* -0,1651 P. jugularis -0,0347 0,2707 0,2707 -0,2013
M. australis 0,1942 0,2308 0,2382 0,1971 S. fuegensis -0,0232 0,2157 0,2260 -0,1379
S. oculatus 0,2921 0,2300 0,2241 0,0439 Macrouridae 0,3668* 0,3377* 0,3497* 0,0557
S. caerulea -0,1160 0,2359* 0,2483* -0,1323 Pinguipedidae 0,1041 0,2429 0,2429 -0,1735
S. fuegensis -0,0641 -0,1134 -0,1134 -0,0168 Sp. A 0,2291 0,2568 0,2568 -0,1457
Nothotenia sp. 1 0,1439 0,3775 0,3775 -0,2475 Sp. B 0,0976 0,0584 0,0584 0,1287
Macrouridae -0,0763 -0,1319 -0,1319 0,1735 Sp. C 0,1180 0,0763 0,0763 0,1041
Nothotenia sp. 2 0,0322 0,2169 0,2216 -0,2570 Sp. D 0,2568 0,2291 0,2291 -0,0624
P. marmoratus -0,1324 0,0688 0,0797 -0,1452 Sp. E -0,0902 0,0208 0,0347 0,2152
Sp. A 0,1041 0,2429 0,2429 -0,1735 Sp. F 0,0134 0,1928 0,2025 0,0228
Sp. B -0,1715 0,0748 0,0942 -0,0390 Sp. G 0,1874 0,1319 0,1319 -0,0347
Sp. C 0,0208 0,0069 0,0069 0,0763 Sp. I 0,0782 0,2439 0,2504 -0,1089
Sp. No identif. 0,0634 0,0264 0,0201 -0,0588 Sp. K -0,0624 -0,0624 -0,0624 0,0485
Total larvas 0,4058* 0,4289* 0,4307* -0,0923 Sp. L -0,0208 0,0485 0,0485 0,0069
Sp. M 0,1225 0,1048 0,1134 0,0394
Total huevos 0,4628* 0,6111* 0,6207* -0,1444

reas de baja salinidad tienen mayor contenido de
agua, y Thorsen et al. (1996) sugieren que estos
huevos presentan mayor contenido de aminocidos
libres en su interior, que actan como efectores
osmticos incrementando el contenido de agua del
huevo durante la hidratacin. Sin embargo, un mayor
dimetro de los huevos asociados a zonas de baja
salinidad no est correlacionado con un mayor tamao
de eclosin larval (Kucera et al., 2002). Entonces, el
mayor dimetro de los huevos de S. fuegensis en zonas
de baja salinidad (o cercana a los deshielos del glaciar)
eventualmente no generara ventajas adaptativas a las
larvas recin eclosionadas (i.e., mayor tamao de
eclosin) y por lo tanto, no incrementara las
probabilidades de sobrevivencia en un rea de alto
stress ambiental.
La ausencia y escasa abundancia de algunos taxa
en las zonas ms cercanas al glaciar puede ser
explicada por las consecuencias fisiolgicas que
generan aguas de baja densidad en el zooplancton.
Durante la poca de deshielo (primavera y verano) se
incrementa el aporte de agua dulce al sistema, que
aumenta la mezcla turbulenta en la capa de mezcla.
Adicionalmente, procesos de vientos locales de fuerte
intensidad a lo largo de fiordos y canales puede
reducir la circulacin estuarina y atrapar plancton en
zonas cercanas a deshielos (Eiane & Daase, 2002).
Aunque los zooplancteres intentan evadir esta zona de
baja salinidad a travs de migraciones verticales, la
mezcla turbulenta puede reducir sus capacidades
natatorias, produciendo stress osmtico (Kaartvedt &
Aksnes, 1992) y muerte masiva (~1000 ind m-2, Eiane
& Daase, 2002), lo que parcialmente podra explicar la
ausencia o escasa abundancia de ictioplancton en
zonas cercanas a Campos de Hielo Sur.
 Lat. Am. J. Aquat. Res.
Las mortalidades masivas de zoo e ictioplancton
producto de los deshielos de glaciares generan como
consecuencia un acople pelgico-bentnico. El
zooplancton muerto (biomasa entre 0,01 y 2,8 g peso
hmedo m-2, 0,03-0,17 gC m-2, Wslawski &
Legezyska, 1998) sirve como importante entrada de
materia orgnica a excavadores bentnicos carnvoros;
por ejemplo, en fiordos rticos la liberacin de
juveniles de anfpodos excavadores Onisimicus
caricus est sincronizada con el mximo de
mortalidad de zooplancton en la poca de deshielos
(Nygrd et al., 2009).
Los deshielos incrementan tambin la turbidez de
la columna de agua (Bustos et al., 2011) e
indirectamente podran afectar las tasas de encuentro
predador-presa, incrementando la mortalidad por
inanicin en larvas de peces. Segn los patrones de
distribucin espacial y anlisis multivariados, la
mayora de las larvas de peces estuvo asociada a
valores intermedios de estratificacin vertical de la
columna de agua. Slo las larvas de Bathylagichthys
parini mostraron una correlacin significativa y
positiva con la frecuencia de Brunt-Vaisala,
sugiriendo una adaptacin a condiciones extremas de
gradientes verticales presentes en fiordos patagnicos,
donde se encuentran larvas, juveniles y adultos
(Pequeo & Matallanas, 2003; Bustos et al., 2008b).
Por lo tanto, la presencia de aguas lechosas en la
cabecera de fiordos y cercanos a glaciares sugiere
condiciones poco favorables para el desarrollo larval
temprano de la mayora de los peces marinos, por la
reduccin de la oferta ambiental de alimento,
alimentacin y crecimiento reciente.
Bajo este contexto, el presente estudio sugiere
algunas posibles consecuencias del incremento de los
deshielos en la Patagonia chilena producto del cambio
climtico global. Un aumento de la descarga de aguas
muy fras y de baja salinidad podra aumentar la
adveccin fuera de los canales del ictioplancton,
transportando huevos y larvas de peces hacia zonas
costeras ms mezcladas, reduciendo el uso de los
fiordos y canales del sur de Chile como reas de
desove y crianza larval temprana. Tambin generara
mayores mortalidades de ictio- y zooplancton, que
inicialmente podra beneficiar al bentos excavador
carnvoro. Es necesario realizar investigaciones sobre
las variaciones temporales (i.e., estacionales) de las
consecuencias biolgicas de los deshielos en esta zona
austral de la Patagonia chilena, estimar flujos de
carbono desde el plagos al bentos, y establecer los
efectos de las forzantes fsicas sobre la historia de vida
de algunos recursos de importancia comercial como la
sardina fueguina y merluza austral.
248
AGRADECIMIENTOS
Los autores agradecen a Mara Ins Muoz y la
tripulacin del Vidal Gormaz por la toma de las
muestras de plancton, a Carolina Rojas, quien apoy
en la separacin del ictioplancton y a los tres
evaluadores annimos. Este trabajo fue financiado por
el proyecto CIMAR C15F 09-03 adjudicado a C.
Bustos y el proyecto Fondecyt 11090020 adjudicado a
M. Landaeta. Durante el desarrollo del trabajo, C.
Bustos fue financiada por una beca doctoral de
CONICYT.
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Lat. Am. J. Aquat. Res., 39(2): 250-260, 2011 Lat. Am. J. Aquat. Res. 250
DOI: 10.3856/vol39-issue2-fulltext-6

Research Article

Seasonal changes in a fish assemblage associated with mangroves in a coastal

lagoon of Baja California Sur, Mexico

Jess Rodrguez-Romero1, Laura del Carmen Lpez-Gonzlez2, Felipe Galvn-Magaa3

Francisco J. Snchez-Gutirrez3, Roxana B. Inohuye-Rivera1 & Juan C. Prez-Urbiola1
1
Centro de Investigaciones Biolgicas del Noroeste, P.O. Box 128, La Paz, B.C.S. 23000, Mxico
2
Instituto Nacional de la Pesca, Pitgoras 1320, Col. Santa Cruz Atoyac, Mxico, D.F. 03310, Mxico
3
Centro Interdisciplinario de Ciencias Marinas, Av. Instituto Politcnico Nacional s/n
P.O. Box 592, La Paz, B.C.S. 23000, Mxico

ABSTRACT. The fish assemblage in a coastal lagoon with mangroves known as Rancho Bueno was
determined and associated with environmental parameters. We used an experimental otter trawl net to catch
the fish, and 62 fish species were identified from 48 genera and 30 families. The most abundant species were:
Etropus crossotus, Eucinostomus gracilis, Paralabrax maculatofasciatus, Sphoeroides annulatus, and
Eucinostomus dowii. The water temperature changed seasonally, being warm from July through December and
cold from January through June. We found more fish species during the warm season than during the cold
season. The southern area of the coastal lagoon had the highest diversity and species richness. The small size
of the fishes registered confirms the ecological role of coastal lagoons as nursery areas that offer protection
and feeding to commercially important fish near Baha Magdalena, Mexico.
Keywords: soft-bottom fish assemblage, environmental parameters, mangrove, Rancho Bueno, Baja
California Sur, Mexico.

Cambios estacionales de la comunidad de peces asociada a zonas de manglar en una

laguna costera de Baja California Sur, Mxico

RESUMEN. Se determin la estructura de peces asociada a factores ambientales en una laguna costera con
manglar denominada Rancho Bueno. Se utiliz una red de arrastre experimental para la captura y se
identificaron 62 especies de peces de 48 gneros y 30 familias. Las especies ms importantes fueron Etropus
crossotus, Eucinostomus gracilis, Paralabrax maculatofasciatus, Sphoeroides annulatus y Eucinostomus
dowii. La temperatura del agua vari estacionalmente, siendo clida de julio a diciembre y fra de enero a
junio. Se registr un mayor nmero de especies de peces durante la poca clida comparada con la poca fra.
La zona sur de la laguna costera present una mayor diversidad y riqueza especfica. El menor tamao de los
peces registrados, confirma el papel ecolgico de las lagunas costeras, consideradas como reas de crianza las
cuales proporcionan proteccin y alimentacin a los peces de importancia comercial cerca de Baha
Magdalena, Mxico.
Palabras clave: comunidad de peces de fondos suaves, parmetros ambientales, manglar, Rancho Bueno,
Baja California Sur, Mxico.

___________________
Corresponding author: Jess Rodrguez-Romero (jrodri04@cibnor.mx)

INTRODUCTION the tropical North Equatorial Current (Galvn-Magaa

et al., 2000; Bizzarro, 2008); this is a zone with
The western coast of the Baja California Peninsula is transitional marine conditions influenced by
influenced by the temperate California Current and by upwellings, which contribute to high primary
251 Fish assemblage in a coastal lagoon from Mxico
productivity almost year round. It is a biologically
active center (BAC), where many marine fish from
different trophic levels are found (Lluch-Belda, 2000).
The study area named Rancho Bueno is a coastal
lagoon located at the southern area of the Baha
Magdalena-Almejas lagoon complex, which is an
important fishing area, mainly for artisanal fisheries
(Ramrez & Gutirrez, 1987; Bizzarro et al., 2007;
Bizzarro, 2008) and sardine (Robinson, 2000).
In spite of this high natural productivity, there are
few published data on fish species taxonomy,
abundance and diversity from this important fishing
area (Galvn-Magaa et al., 2000; Rodrguez-Romero
et al., 2008, 2009). Also is poor known the relation
between the fish assemblages and environmental
parameters in this area, or how these parameters
determine the seasonal or spatial changes in the fish
structure. The objective of our study is to know the
influence of environmental parameters in the seasonal
and spatial changes of the fish assemblages in a
shallow coastal lagoon in the western coast of Baja
California peninsula.
MATERIALS AND METHODS
Study area
The coastal lagoon of Rancho Bueno is located
between 241730-242045N, and 1112030- in the coastal lagoon, averaging 21.0C at location 1
1112740W. It is 10.9 km long and 1.2 km wide.
The depth is shallow, from 1 to 6 m, with ~95% of its
perimeter bordered by mangrove (Rhyzophora
mangle, Laguncularia racemosa and Avicennia
germinans). The bottom includes sand, silt and clay,
and some stony areas (Mendoza & Lechuga, 1995).
From October 1993 through September 1994, we
did twelve surveys at ten locations. One tow was
carried out at each location using an experimental
otter trawl net of 6.0 m length and 4.0 m wide with
doors of 0.60 x 0.40 m and 3.15 cm mesh size. The
bottom temperature, salinity, water depth, and bottom
type were recorded. Specimens were fixed in 10%
formaldehyde solution for later identification using
specific keys for each fish species.
Using the weight data of each species, ecological
indexes were calculated. The relative abundance (RA)
and relative weight (RW) were calculated as follows:
RA(%) = (n / N) * (100) and RW(%) = (w / W) * (100),
where n is the number of species captured, N is the
total number of specimens, w is the weight of each
species, and W is the weight of all specimens.
The species richness index (D) proposed by
Margalef (1969) was calculated as follows: D = (S
1) / ln N, where S is the number of species and N is the
total number of individuals. The Shannon-Wiener
diversity index (H') was calculated as follows: H' =
(ni / N) log (ni / N), where: ni is the number of
individuals of species i and N is the total individuals
of all species in the sample. The evenness index
(Pielou, 1966) was calculated as follows: E = H' / ln
(S), where H' is the Shannon index and S is the
number of species. The dominance or Biological
Value Index (BVI) (Sanders, 1960) was calculated as
i
follows: BVI = j Puij, where i is the species, j is the
sample locality, and Puij is the point level of species i
at locality j.
A Principal Components Analysis (PCA) by
season and locations were used, including
environmental and ecological data.
RESULTS
The Rancho Bueno coastal lagoon was divided into
three zones: North (locations 1, 2, 3, 4), Central (5, 6,
7), and South (8, 9, 10) (Fig. 1). The warm season
went from July to December 1993, with average water
temperatures ranging from 22.6 to 27.9C; whereas
the cold season went from January through June 1994,
with average temperatures ranging from 18.8 to
22.0C. The temperature increased from north to south
(North) and 25.1C at location 10 (South). Salinity
changed little during the year, ranging from 34.6 to
35.5 psu. Spatial variations in salinity were small,
ranging from 34.3 psu at location 1 to 36.6 psu at
location 10 (Tables 1 and 2).
The depths and substrate types are shown in Table
2. The Northern Zone (locations 1 to 4), had sandy
bottoms and greater depths than the Southern Zone
(locations 8 to 10), which had higher salinity and
shallow depths.
We captured 3,082 fish, all juveniles, with a total
weight of 102.04 kg, belonging to 62 species in 48
genera and 30 families. The most important families
were: Haemulidae (ten species); Lutjanidae, Gerreidae
and Paralichthyidae (five species each), Serranidae
(four species), and Sciaenidae and Urolophidae (three
species each). The most common species were:
Etropus crossotus (688 specimens), Eucinostomus
gracilis (544), Paralabrax maculatofasciatus (253),
Sphoeroides annulatus (242), Eucinostomus dowii
(229), Orthopristis reddingi (133) and Diapterus
peruvianus (108).
Locations 9, 10 and 5 had the highest numbers of
fish. The months with highest organism numbers
were: September 1994 (937 fish from 32 species)
 Lat. Am. J. Aquat. Res. 252

Figure 1. Study area and sampling locations Rancho Bueno coastal lagoon in southern Baha Magdalena, Baja California
Sur, Mexico.
Figura 1. rea de estudio y localidades de muestreo en la laguna costera de Rancho Bueno ubicada al sur de Baha
Magdalena, Baja California Sur, Mxico.

Table 1. Average water temperature and salinity during The fish species better represented by relative
1993-1994 in Rancho Bueno, Mexico. abundance, in order of importance, were: E. crossotus,
Tabla 1. Temperatura y salinidad promedio durante E. gracilis, P. maculatofasciatus, S. annulatus, E.
1993-1994 en Rancho Bueno, Mxico. dowii, O. reddingi and D. peruvianus, composing
71.3% of the specimens and over 35% of the total
relative weight (Fig. 2). On each sampling, E.
Average Average crossotus and E. gracilis had the highest relative
Month
Temperature (C) Salinity (psu) abundance (22.3 and 17.6%); while P.
Oct. 27.6 34.8 maculatofasciatus had the highest relative weight
Nov. 25.2 35.0 (11.2%). It is important to mention that of 62 fish
Dec. 22.6 34.7 species, 38 (61.29%) are of commercial importance
Jan. 22.0 35.0
(species marked with an asterisk in Table 4).
Feb. 19.9 35.5 The highest seasonal and spatial species richness
according to species abundance occurred in October
Mar. 20.5 34.9
(3.9); whereas the lowest richness occurred in April
Apr. 18.8 35.0 (0.4). The lowest value was from the northern zone
May 18.9 35.2 during the cold months; whereas the highest value was
Jun. 21.0 35.5 from the southern zone during the period September
Jul. 22.7 35.0 through January.
Aug. 25.7 35.1 The diversity index ranged from 0.4 to 3.6 (bits
ind-1), with the minimum value at location 7 in April;
Sep. 27.9 35.0
whereas the maximum diversity was found at location
10 in October (both in the southern zone). Locations 1
and October 1993 (469 fish from 36 species). Six of to 4 in the northern zone had lower diversity than
the 62 species were found at all locations: E. locations 7 to 10 in the southern zone, which also had
crossotus, P. maculatofasciatus, Paralichthys cali- the highest diversity.
fornicus, S. annulatus, Symphurus atramentatus and The lowest evenness occurred in the cold season
Synodus lucioceps. (values below 0.6.); the minimum value (0.25) was at
253 Fish assemblage in a coastal lagoon from Mexico

Table 2. Characteristics of Rancho Bueno coastal lagoon, Mexico sampling sites.

Tabla 2. Descripcin de las localidades de muestreo en la laguna costera Rancho Bueno, Mxico.

Tow depth Temperature Salinity

Zone Site Substrate type
(m) (C) (psu)
North 1 Sand 2.9 21.04 34.36
2 Sand 2.5 21.17 34.10
3 Sand 3.6 21.26 34.13
4 Sand 3.5 21.34 34.44
Central 5 Sand-silt 2.1 21.59 34.61
6 Sand-silt 2.0 22.73 34.96
7 Sand-silt 2.2 24.17 35.40
South 8 Silt 1.4 24.24 35.87
9 Silt 1.8 24.63 36.12
10 Silt 1.6 25.07 36.58

Using PCA, we detected two main groups of fish

Figure 2. Relative abundance and weight of dominant
fish species at Rancho Bueno coastal lagoon.
Figura 2. Abundancia relativa y biomasa de las especies
dominantes de peces en la laguna costera de Rancho
Bueno.
location 4 in May, followed by location 7 in April
(0.39). The highest evenness (1.0) in some locations
was recorded in November, December, February, and
August. In general, the cold season had lower
evenness than the warm season (0.72 to 0.77). In table
3 are shown the monthly values of ecological indexes.
The fish species of highest importance according to
the Biological Value Index were: E. crossotus, E.
gracilis, S. annulatus, P. maculatofasciatus and E.
dowii, with index values of 94, 64, 62, 60 and 48,
respectively (Fig. 3).The monthly analyses of this
index are shown in Table 4.
(Fig. 4). In the first group were six species: P.
californica, O. cantharinus, U. halleri, S. ovale, E.
crossotus and P. maculatofasciatus, which were
associated to northern locations (1, 2, 3 and 4) in the
coastal lagoon, with higher biomass in deep locations
and close to the entrance to the open ocean.
The other group included 11 fish species at
locations 5 to 10, which are in the center and south
area, with lower biomass but higher organism
numbers and evenness, associated to shallow waters
with higher water temperature and salinity.
The seasonal PCA (Fig. 5) recorded two periods,
associated to cold waters during January-June (winter-
spring), and a warm period from July to December
(summer-fall). In this last period the diversity, species
number, and organism abundance showed the highest
affinity with 12 dominant fish species, including P.
maculatofaciatus, Sphoeiroides annulatus, Lutjanus
argentiventris, Hoplopagrus guntheri, Calamus
brachysomus, Balistes polylepis and others. During
the cold period, with highest biomass and salinity, the
most common species were: P. californicus, U.
halleri, E. crossotus, A. mazatlanus, O. cantharinus
and S. lucioceps.
DISCUSSION
The topographic and hydrographic characteristics of
the coastal lagoon of Rancho Bueno, provide optimal
conditions as a nursery, feeding, and reproduction area
for many fish species that are important as commercial
species. This ecosystem has high primary productivity
that promotes species richness. Mendoza & Lechuga
(1995), found higher accumulated organic matter in
Table 3. Monthly values of ecological indices by zone and sampling site. D: Species richness (Margalef, 1969), H: Diversity (Shannon-Wiener), E: Evenness (Pielou,
1966).
Tabla 3. Valores mensuales de los ndices ecolgicos por zona y localidades de muestreo. D: Riqueza de especies (Margalef, 1969), H: Diversidad (Shannon- Wiener), E:
Uniformidad (Pielou, 1966).

October November December January February March

Location
D. H' E D H' E D H' E D H' E D H' E D H' E
North 1 2.06 1.97 0.62 1.86 1.92 0.96 1.52 2.07 0.89 1.23 1.29 0.55
2 2.64 2.03 0.59 1.86 1.92 0.96 2.4 2.5 0.97 0.91 0.92 0.92 1.37 1.66 0.83
3 2 2.22 0.79 0.91 0.92 0.92 1.82 1.58 1 1.21 1.73 0.86
4 2.32 2.38 0.72 1.82 1.58 1 2.41 2.63 0.94 1.94 2.24 0.8 0.72 1 1 1.37 1.45 0.72
Central 5 2.72 2.8 0.88 0.72 0.81 0.81 2.59 2.82 0.89 1.64 2.01 0.78 0.56 0.92 0.92
6 2.34 2.62 0.93 0.62 0.97 0.97 1.12 1.46 0.92 1.21 1.42 0.71 1.24 1.52 0.96 1.2 1.77 0.76
7 0.87 0.86 0.43 1.44 1 1 1.5 1.72 0.66 1.44 1.55 0.77 2.12 2.13 0.71 0.72 0.67 0.42
South 8 2 1.78 0.59 2.16 2 1 2.73 2.41 0.73 2.16 2.53 0.9 1.82 2.36 0.79
9 2.72 2.11 0.55 3.47 3.29 0.8 1.64 1.65 0.55 1.44 1.5 0.95 2.23 2.25 0.97 1.62 1.87 0.72
10 3.96 3.62 0.85 0.91 1.33 0.66 2.32 1.82 0.53 3.44 2.99 0.75 2.06 2.24 0.96 1.94 2.29 0.72
Lat. Am. J. Aquat. Res.

April May June July August September

Location
D H' E D H' E D H' E D H' E D H' E D H' E
North 1 0.91 0.92 0.92 0.96 1.41 0.89 1.56 2.2 0.95 1.44 1.5 0.95
2 0.62 0.72 0.72 1.01 1.62 0.7 1.67 1.92 0.96 0.62 0.72 0.72
3 1 1.19 0.6 1.59 1.53 0.54 0.69 0.61 0.39 1.11 1.72 0.86 1.86 2.42 0.81
4 1.41 1.26 0.54 0.58 0.4 0.25 1.7 1.33 0.44 0.91 0.99 0.62 1.23 1.8 0.7
Central 5 1.12 1.46 0.92 1.31 1.38 0.53 3.07 2.82 0.68
6 0.94 1.06 0.53 2.4 2.11 0.67 1 1.32 0.66 0.91 0.92 0.92 0.91 0.92 0.92 3.55 3.26 0.77
7 0.39 0.39 0.39 0.91 0.92 0.92 0.91 0.99 0.62 1.24 1.37 0.86 2.93 3.3 0.83
South 8 0.62 0.97 0.97 0.91 0.92 0.92 3.34 2.91 0.76 1.12 1.46 0.92 1.44 1 1 2.4 3.04 0.88
9 2.39 2.26 0.65 1.86 1.97 0.66 2.09 2.3 0.89 2.01 2.52 0.98 2.39 2.86 0.75
10 1.69 2.31 0.82 1.44 1.5 0.95 1.8 1.94 0.69 1.61 2.05 0.88 1.03 1.15 0.72
254
255 Fish assemblage in a coastal lagoon from Mexico
Figure 3. Biological Value Index of the most common
fish species at coastal lagoon of Rancho Bueno, Mexico.
Figura 3. ndice de valor biolgico de las especies de
peces ms importantes de la laguna costera de Rancho
Bueno, Mxico.
the southern area, which also we found higher fish
abundance.
The number of fish species and marine organisms
was higher in the southern area of Rancho Bueno,
where average water temperature was higher and the
bottom was muddy. In contrast to northern locations,
the southern locations had fewer fish species and
organisms, with sandy bottoms and lower water
temperatures. In months with low temperatures, the
number of fish species and other organisms was low.
During February, we found fewer fish (55) belonging
to 15 families; whereas during warmer months, mainly
September, we found 937 fish belonging to 19
families. The main species were: P. maculato-
fasciatus, S. annulatus, E. dowii, O. reddingi and D.
peruvianus. Of these species, E. crossotus, P.
maculatofasciatus and S. annulatus were common
during the sampling period.
The fish species found in our study have been
reported for the Baha Magdalena-Almejas lagoon
complex (Torres-Orozco & Castro-Aguirre, 1992; De
La Cruz-Agero et al., 1994; Galvn-Magaa et al.,
2000). The importance of our results is the high
number of fish species found, and mostly were
juveniles (62), which confirm that Rancho Bueno is
used as a nursery and feeding area by fish species with
commercial importance.
The coastal lagoon of Rancho Bueno had a high
number of fish species comparing with other locations
in Baja California Sur. Rodrguez et al., 1998 and
Gutirrez-Snchez et al. (2007) also found a high
number of fish species; however De La Cruz (2004)
found only 25 fish species in four estuarine areas from
Baha de la Paz. The abundance and relative biomass
analysis showed that the main fish species (E.
crossotus, P. maculatofasciatus and S. annulatus)
represented over 70% of the total relative abundance
and almost 37% of the relative biomass. This indicates
that, in spite of being the most numerous species, their
small size affects their biomass. The southern
locations from the Rancho Bueno lagoon had the
highest relative abundance, almost 40%.
The highest species richness values occurred
during the warm months, and the lowest values during
the cold months. Gutirrez-Snchez et al. (2007)
reported in Bahia Magdalena, Mexico, the highest
values of species richness between February and July,
as a consequence of the mix of fish species with
different zoogeographic affinities. In Baha
Concepcin (Gulf of California), Rodrguez-Romero
et al. (1998) found the highest species richness in
September and the lowest in February. The species
richness in the southern Bahia Concepcion was also
influenced by the muddy substrate, because locations
with several habitat types increase the species richness
(Krebs, 1978; Blaber, 1985; Rodrguez-Romero et al.,
1994), because there are prey from different habitats
which are consumed by fishes. We found the highest
diversity during the warm months, with the highest
value (3.6 bits ind-1) in October and the lowest in
April (0.4), which agrees with the diversity changes
associated to sampling location, fishing method, fish
dynamics, biology of each fish species, feeding
relationships, and environmental conditions
(Margalef, 1974).
The Rancho Bueno coastal lagoon could be
considered as a mature fish community, considering
the high diversity found with little disturbance (Odum,
1972). The locations in the southern area are
apparently uniform, because they are in the most
protected area; however, these shallow areas are
associated with high changes in water temperature and
salinity, and with the highest diversity and evenness.
Seasonal changes in diversity are associated with
changes in water temperature, which also affect the
presence of fish, diversity and abundance (Rodrguez-
Romero et al., 1998, 2005). De La Cruz (2004)
studied fish assemblages in four mangroves areas
close to Baha de La Paz (Gulf of California), he
found the highest values of abundance and diversity
during the warm months and the lowest during cold
months; whereas Acevedo (1997) in Laguna Ojo de
Liebre (western coast of Baja California) registered
that locations in the north coastal lagoon had the
highest water temperatures and the highest fish
diversity. Also Horn & Allen (1985), found that fish
communities in bays and estuaries in southern
California, are influenced by oceanic waters and had
 Lat. Am. J. Aquat. Res. 256

Table 4. Biological Value Index of fish species found at Rancho Bueno, Mexico. Species with (*) have commercial
importance.
Tabla 4. ndice de Valor Biolgico de las especies de peces registradas en Rancho Bueno, Mxico. Las especies marcadas
con asterisco (*) tienen importancia comercial.

1993 1994
Species
Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep
Achirus mazatlanus 25 12 7 35 8 39 18 32 13 24 9 26
Arius platypogon* 5
Balistes polylepis* 27 21 22 17 10 8 6 11
Bothus constellatus 32 9 9 9 9 9 5
Calamus brachysomus* 29 13 22 21 24
Caranx caninus* 2 6
Centropomus medius* 9
Chaetodipterus zonatus* 7 7 9
Chaetodon humeralis 15
Cyclopsetta panamensis* 8 10 18 5 15
Cynoscion parvipinnis* 14 9
Dactylagnus mundus 7 8 9
Diapterus peruvianus* 9 14 8 6 14 29
Diodon holocanthus 8 8 7
Diodon hystrix 7 7 14
Diplectrum pacificum* 13 6
Epinephelus analogus* 15 5 7
Etropus crossotus 62 34 77 65 40 87 40 70 78 77 47 39
Eucinostomus dowii* 21 20 15 7 19 19 16 10 34
Eucinostomus gracilis* 65 19 66 16 20 8 45
Eugerres axillaris* 10
Fistularia commersonii 7
Gerres cinereus* 10
Gymnura marmorata* 7 10 9 20 8 9 1
Haemulon steindachneri* 7 15 3
Haemulopsis leuciscus* 12 7 15 9 15 3
Haemulopsis nitidus* 3
Hippocampus ingens 4 10 13 15
Hoplopagrus guntheri* 10 7 18
Hypsoblennius gentilis 8 8 9 17
Hypsopsetta guttulata* 7
Lutjanus aratus* 10 10 7
Lutjanus argentiventris* 8 15 16 14 9 17 29
Lutjanus colorado* 4
Lutjanus novemfasciatus* 5
Menticirrhus undulatus* 10
Microlepidotus inornatus* 4
Micropogonias ectenes* 9 6
Orthopristis cantharinus* 8 10
Orthopristis reddingi* 22 4 18 7 9 30
Paralabrax maculatofasciatus* 72 14 81 70 16 16 14 16 52 19 47 22
Paralabrax nebulifer* 9
Paralichthys californicus* 45 9 9 19 16 5 15 23 15 7 35
Paralichthys woolmani* 38 9 26 8
257 Fish assemblage in a coastal lagoon from Mexico

1993 1994
Species
Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep
Pleuronichthys ritteri 8 9
Pomadasys bayanus* 4 20
Pomadasys macracanthus 2 6 7
Pomadasys panamensis* 6 4
Prionotus ruscarius 11 9 8 22 6 5 5
Pseudupeneus grandisquamis 12 19 5 12 7 5
Scarus perrico* 7
Scorpaena russula 8 6 1
Sphoeroides angusticeps 4 1
Sphoeroides annulatus* 24 32 40 24 10 36 17 34 40 26 27 53
Syacium ovale 42 7 9
Symphurus atramentatus 4 28 4 6 31 21 27 14
Symphurus fasciolaris 18
Synodus lucioceps 2 63 38 25 55 9 26 24 9 12
Urobatis halleri 6 10 8 4 19 17 22 10 9 8
Urobatis maculatus 8
Urotrygon asterias 7 12 9
Xenistius californiensis 2

Figure 4. Spatial Principal Component Analyses associated with water temperature, salinity, depth, substrate (grain type)
total abundance, biomass, fish dominant species and sampling locations (1 to 10).
Figura 4. Anlisis espacial de componentes principales asociado a la temperatura del agua, salinidad, profundidad,
substrato, abundancia total, biomasa, especies de peces dominantes y localidades de muestreo (1 a 10).
 Lat. Am. J. Aquat. Res. 258

Figure 5. Monthly Principal Component Analyses associated with water temperature, salinity, biomass, number of fish
species (SPP), diversity, total abundance. JF: January-February, MA: March-April, MJ: May-June, JA: July-August, SO:
September-October, NO: November-December.
Figura 5. Anlisis mensual de componentes principales asociado a temperatura del agua, salinidad, biomasa, numero de
especies de peces, diversidad, abundancia total. JF: enero-febrero. MA: marzo-abril, MJ: mayo-junio, JA: julio-agosto,
SO: septiembre-octubre, NO: noviembre-diciembre.

seasonal changes in abundance and diversity. The
biological value index showed that E. crossotus, E.
gracilis, S. annulatus, P. maculatofasciatus and E.
dowii were the most important fish species in the
Rancho Bueno coastal lagoon. Their dominance might
be attributed to their high occurrence during all
sampling.
In the upper Gulf of California, Prez-Mellado &
Findley (1985) found that E. crossotus and
Citharichthys spp. were the most abundant species in
the shrimp trawl by-catch, followed by Diplectrum
pacificum and Scorpaena sonorae; whereas
Rodrguez-Romero et al. (1998) in Baha Concepcin
(central Gulf of California) found that P.
maculatofasciatus, E. crossotus, Urobatis halleri and
Sphoeroides lispus were the most important fish
species.
Our PCA and cluster analysis indicated that two
groups characterized the fish assemblage in the
Rancho Bueno coastal lagoon. In the northern area
with deeper water, the highest biomass was
represented by few fish species with high importance;
larger fish were more frequent and these species had
temperate zone affinity or were widely distributed,
such as P. californicus, Orthopristis cantharinus, E.
crossotus, Sciacium ovale and Urobatis halleri.
In the southern area, we found high abundance and
diversity, with more fish of small size (mostly
juveniles). Juveniles were common in protected areas
associated to mangroves. The most common species
were: E. dowii, B. polylepis, H. guntheri, Sphoeroides
annulatus, E. gracilis, Lutjanus argentiventris,
Syacium ovale, Diapterus peruvianus and O. reddingi,
which are from temperate-tropical habitats or are
widely distributed (Robertson & Allen, 2002). Baja
California Sur is a biogeographically transition zone
(Castro-Aguirre & Torres-Orozco, 1993), where
tropical, sub-tropical, and temperate fish coexist.
Changes in spatial and seasonal fish composition are
associated to fluctuating environmental conditions in
this transition zone. Galvn-Magaa et al. (2000)
confirmed that northwestern Mexico is one of the
most diverse areas in terms of tropical, temperate and
tropical-temperate transition marine species.
The west coast of Baja California Sur is a tropical-
temperate transition zone, where seasonal gradients
259 Fish assemblage in a coastal lagoon from Mexico
are influenced by the cold California Current and the
Eastern Pacific Equatorial Current (Bizzarro, 2008).
The water temperature changes, substrate type, and
feeding habitats were the most influential
environmental elements affecting the fish assemblages
in this area. The monthly PCA also indicated two
distinct periods, dominated by water temperature:
winter-spring and summer-autumn (Fig. 6). The water
temperature, habitat type and primary productivity are
important for ecosystem productivity (Mendoza-
Salgado & Lechuga-Devze, 1995).
In conclusion, the Rancho Bueno coastal lagoon
supports nursery and feeding areas for juvenile fish
with high commercial importance, such as snappers,
groupers, mojarras and flatfishes. Also is a
reproduction area for many commercial fish species
from temperate and tropical affinities. We found
seasonal changes in the fish assemblages of this
coastal lagoon based on changes in water temperature,
substrate type and depth. The highest species richness
and diversity were found during the warmer months,
and the highest number of organisms was found in the
southern area, where high water temperature and
muddy bottoms included Sargassum spp. and
mangrove roots; whereas the northern area had few
fish species, the bottom was sandy and had low water
temperature.
ACKNOWLEDGEMENTS
We thank Mario Cota-Castro and Juan Jos Ramrez
for helping with sampling. Financial support was
provided by the Centro de Investigaciones Biolgicas
del Noroeste project Estructura y funcin de
comunidades de peces en el Estero de Rancho Bueno,
B.C.S. Mexico. FGM and FJGS thank the Instituto
Politcnico Nacional (COFAA and EDI fellowships).
We thank Laura Sampson for editing the English
version of this manuscript.
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Lat. Am. J. Aquat. Res., 39(2): 261-270, 2011 Relative growth of symbiotic crab Austinixa aidae 261
DOI: 10.3856/vol39-issue2-fulltext-7

Research Article

Relative growth and sexual dimorphism of Austinixa aidae (Brachyura:

Pinnotheridae): a symbiont of the ghost shrimp Callichirus major from the
southwestern Atlantic

Douglas Fernando Peir1, Paulo Ricardo Pezzuto2 & Fernando Luis Mantelatto1
1
Laboratory of Bioecology and Crustacean Systematics, Department of Biology, FFCLRP
University of So Paulo, Postgraduate Program in Comparative Biology
Avenida Bandeirantes 3900, CEP 14040-901, Ribeiro Preto, SP, Brazil
2
Universidade do Vale do Itaja, Centro de Cincias Tecnolgicas da Terra e do Mar
Rua Uruguai, 458, CEP 88302-202, Itaja, SC, Brazil

ABSTRACT. Species of the family Pinnotheridae constitute an ideal group for morphometric studies due to
their complex morphological adaptations. These adaptations respond to the selective pressure of a symbiotic
life style. This study describes the relative growth and morphometric features of the symbiotic pea crab
Austinixa aidae (associated with the ghost shrimp Callichirus major), from the sandy beaches in the southwest
Atlantic, Brazil. Significant differences were detected in the biometric proportions, particularly the chelar
propodus length and carapace width, of each sex. These dimensions were also related to the size at which the
individuals reached morphological sexual maturity (5.1 mm of carapace width for both sexes). Males and
females were 2.4 times wider than long, which corresponds to the principal adaptation developed by Austinixa
species to live in cryptic environments. Moreover, juveniles were proportionally more rounded. The changes
in the biometric proportions of carapace length and width of A. aidae were more pronounced in males and
females, adaptations that facilitate roaming within the galleries of their hosts.
Keywords: pinnotherid crabs, traditional morphometry, size-at-maturity, sexual dimorphism, southwestern Atlantic.

Crecimiento relativo y dimorfismo sexual en Austinixa aidae (Barchyura:

Pinnotheridae): un simbionte del camarn fantasma Callichirus major
del Atlntico sudoccidental

RESUMEN. Las especies de la familia Pinnotheridae constituyen un grupo ideal para la realizacin de
estudios morfomtricos, debido a sus complejas adaptaciones morfolgicas. Estas adaptaciones son respuesta a
la presin de seleccin debida a su vida simbionte. En este estudio se describi el crecimiento relativo y las
caractersticas morfomtricas del cangrejo simbionte Austinixa aidae (asociado con el camarn fantasma
Callichirus major), de una playa de arena del Atlntico suroeste de Brasil. Se determinaron diferencias
significativas en las proporciones biomtricas de cada sexo, entre la longitud del propodio y ancho del
caparazn. Estas dimensiones estuvieron relacionadas tambin con la talla en que los individuos muestran
cambios morfolgicos en su madurez sexual (5.1 mm de ancho del caparazn en ambos sexos). Los machos y
hembras fueron 2,4 veces ms anchos que largos, lo que corresponde a la adaptacin principal que las especies
del gnero Austinixa, han desarrollado para vivir en ambientes crpticos. Adems, los juveniles fueron
proporcionalmente ms redondeados. Los cambios en las proporciones biomtricas de longitud y ancho del
caparazn de A. aidae, fueron ms pronunciados en machos y hembras, adaptaciones que facilitan el
desplazamiento al interior de las galeras construidas por sus hospederos.
Palabras clave: cangrejos pinnothridos, morfometra tradicional, talla de madurez, dimorfismo sexual,
Atlntico sudoccidental.

___________________
Corresponding author: Fernando Luis Mantelatto (flmantel@usp.br)
262 Lat. Am. J. Aquat. Res.
INTRODUCTION
Pea crabs of the family Pinnotheridae De Haan, 1833
constitute a promising group for morphometric studies
because of their complex morphological adaptations to
symbiotic life style. Over 300 species of this family
display symbiotic relationships (both facultative and
obligated) with a wide variety of bivalves, gastropods,
polychaetes, crustaceans, echinoderms, echiurids,
brachiopods, balanoglossids and ascidians (Schmitt et
al., 1973; Harrison & Hanley, 2005; Ng et al., 2008).
These symbioses are an intriguing system and,
consequently, almost all the morphological features of
these crabs are strongly adapted in order to achieve a
successful relationship. Their adaptation to this variety
of hosts likely accounts for their diversity, and this can
consequently drive towards a confused state of
systematics in some members of the group (Palacios-
Theil et al., 2009).
Among representatives of this family, the
polyphyletic pinnotherid crab genus Austinixa Heard
& Manning, 1997 (sensu Palacios-Theil et al., 2009) is
less diverse than other members of the Pinnotheridae,
and comprise currently eight described species (Ng et
al., 2008). The enlargement of carapace, the third pair
of pereopods, and a conspicuous lobe on the outer
margin of the basal segment on the exopod of the third
maxilliped are the main synapomorphies with the
Pinnixa complex (in which Austinixa was included)
(Heard & Manning, 1997; Campos, 2006). These
morphological modifications presumably facilitate
lateral movement within the microhabitats (narrow
tubes and burrows) occupied by these crabs (Zmarzly,
1992; McDermott, 2006).
As far as we know, only three studies have been
devoted exclusively to understand the relative growth
(allometry) in Austinixa: Alves & Pezzuto (1999),
Alves et al. (2005) and Valena-Silva et al. (2008), all
on Austinixa patagoniensis (Rathbum, 1918). For
Austinixa aidae (Righi, 1967), no studies have been
published.
Likewise the lifestyle, the allometry of pea crabs
varies considerably, and some body character-
ristics/features are poorly understood for species of
Austinixa. Taking into account the lack of descriptions
on the allometry, the aim of this study was to describe
the relative growth and body features of the symbiotic
crab A. aidae [associated with the thalassinid ghost
shrimp Callichirus major (Say, 1818)], from a sandy
beach in the southwest Atlantic. We also estimated the
size at maturity and the existence of sexual
dimorphism in this population.
MATERIALS AND METHODS
Sampling was carried out bimonthly during daytime at
low tide (in an area of approximately 400 m length
and 30 m width), from May 2005 to September 2006
in the intertidal zone of Perequ-au Beach, Ubatuba,
northern coast of State of So Paulo, Brazil
(232459.99S, 450317.13W), a semi-protected
and dissipative beach composed by fine sand. Crabs
were collected with commercial yabby pumps,
developed by Rodrigues (1966) and similar to the one
described by Manning (1975), from Callichirus major
galleries, separated from the sand by a 1 mm mesh
sieve, frozen, and analyzed in laboratory.
Crabs were sexed by revising the shape of the
pleopods. Males have a pair of long, thin pleopods on
the ventral surface of the first abdominal somite and a
pair of short pleopods on the second abdominal somite
(together they compose the gonopods); females have
four pairs of short pleopods from the second to the
fifth abdominal somites (Narchi, 1973). Specimens
with undifferentiated or not developed pleopods and
gonopore were considered/named juveniles (no
identified as males or females). The following
measurements were taken under a stereomicroscope
with the aid of a drawing tube (0.1 mm precision):
carapace width (CW), carapace length (CL), abdomen
width (AW) (between fourth and fifth abdominal
tagma), height (HQ) and length (LQ) of cheliped
propods (left and right), and the gonopod length (GN)
(from the shaft to tip). The wet weight (WW) was
measured, after the samples were drained by paper
towel, with an electronic analytical balance (0.0001 g
precision), to assess changes in weight related to
sexual maturity.
The carapace width was used as independent
variable, because it represents the crabs body size. To
assess the chelae dimorphism (heterochely), the
Mann-Whitney Rank Sum Test (due the non-
normality of the data) was applied to compare
differences in mean values of HQ and LQ, in both
chelipeds. The same test was applied to compare
differences on sizes of males and females.
Relative growth was quantitatively described by
fitting the allometric equation (Y = aXb) for each body
dimension against the independent variable (CW) by
least-squares regression analysis (Hartnoll, 1974,
1978). Inflection (transition) points corresponding to
changes in the allometry pattern during the growth
were first identified by eye on dispersion graphs. They
were then iteratively searched by a specific routine of
the software Regrans (Pezzuto, 1993); the routine
seeks the CW value where the data could be split into
two subsets resulting in the lowest combined residual
 Relative growth of symbiotic crab Austinixa aidae
sum of squares. An Overall Test for Coincidental
Regressions (Zar, 1996, p. 368) was conducted to
check the validity of the transition point. It
compares the difference between the global sum of
squares (calculated from a single model fitted to the
data), and the pooled residual sum of squares (i.e. of
the subsets located to the left and right sides of the
transition point) (Zar, 1996). If a significant difference
was found, the ANCOVA ( = 0.05) was used to test
the difference between intercepts and slopes of the
two regressions, corresponding then to the pre and
post-pubertal phases of growth (Zar, 1996). On the
analysis of the allometric growth, constant (b) gives
information about the increase of one biometric
dimension in relation to another; isometric growth was
considered when b was = 1, negative allometric
growth with b < 1, and positive allometry with b > 1
(Hartnoll, 1982). When involved different units, like
the CW and the WW, the value of isometry assume b
= 3 (Valenti, 1984; Biagi & Mantelatto, 2006).
The sexual dimorphism in Decapoda occurs by
differences in relative growth between males and
females, which in initial stages are not clear. There are
body structures that present strong and consistent
patterns of variations in allometry associated to
maturation, for example the cheliped of males and the
abdomen of females in Brachyura (Hartnoll, 1978,
1982). These structures are related to reproductive
activities of both sexes, and are associated to
dimorphism in mature stages. The body dimension
related to maturation and reproductive activity
increase in major rates than the carapace (positive
allometric growth) (Hartnoll, 1982).
Maximum and minimum sizes of males and
females were verified, as well as the minimum size of
ovigerous females and the length of their reproductive
period, which was identified by the percentage of
ovigerous females in relation to the total number of
females caught bimonthly (Alves et al., 2005).
The normality of data-set was evaluated before to
the use of parametric tests. The statistical analysis
were conducted by using Sigma-Stat 2.03 and
Regrans (Pezzuto, 1993), according to Zar (1996) (P <
0.05 significance). All material was preserved in
ethanol 80% and deposited in the Crustacean
Collection of the Departamento de Biologia,
Faculdade de Filosofia, Cincias e Letras de Ribeiro
Preto, Universidade de So Paulo, (CCDB/FF
CLRP/USP) under the catalogue # 2102.
RESULTS
Relative growth
In total, 246 males (42.2%), 263 females (45.1%) and
74 juveniles (12.7%) of A. aidae were analyzed for
263
relative growth. This analysis revealed differences in
growth rates of a few body structures in both males
and females (Table 1).
The carapace length of males, females, and
juveniles showed negative allometric growth (b < 1),
with no transition points (Fig. 1a, Table 1). The same
pattern was also found for the abdomen width of
males (Fig. 1b). On the other hand, the female
abdomen width exhibited two transition points at 5.1
and 7.2 mm CW. Below 5.1 mm and between 5.1 and
7.2 mm, growth was positive allometric, and from 7.2
mm growth was isometric. For juveniles, growth was
positive allometric, without transition points.
Because no statistical differences were found
between the HQ and HL of both left and right chelar
propodus (P = 0.931 and P = 0.942 for total of
individuals; males P = 0.897 and P = 0.772; females P
= 0.982 and P = 0.822; and juveniles P = 0.513 and P
= 0.577, respectively), only the measurements of the
left chelar propodus were used in the relative growth
analysis.
The maximum height of the chelar propodus of
males and females (Fig. 1c) showed positive
allometric growth, with no transition points. For
juveniles, growth showed negative allometry, with no
transition points.
The maximum length of the male chelar propodus
showed positive allometric growth, with a break in the
dispersion data and an inflection at 5.1 mm CW (Fig.
1d). For females, growth was positive allometric,
while for juveniles, growth was isometric, both with
no significant transition points.
The wet weight of males showed positive
allometric growth up to 5.7 mm CW, and after this
size, growth changed to negative allometric. In
females, growth was positive allometric up to the
transition point at 5.4 mm CW, changing to isometric
in larger sizes. For juveniles, growth was described by
a single, positive allometric equation (Fig. 1e).
The gonopods showed isometric growth up to 3.0
mm (CW), and after that the growth was negative
allometric (Fig. 1f).
Body features, maturity and sexual dimorphism
The CW of male crabs varied between 2.0 and 10.1
mm (mean 5.8 2.2 mm CW), and females between
2.5 and 10.5 mm (mean 6.1 2.0 mm CW). No
significant differences in CW between the sexes were
detected (P = 0.154).
The CW of males was, on average, 2.4 0.4
(standard deviation) times the CL; for females and
juveniles, the means were 2.4 0.3 and 1.9 0.3,
respectively. Smaller individuals had, therefore, a
264 Lat. Am. J. Aquat. Res.

Table 1. Austinixa aidae. Regressions for body dimensions: carapace length (CL), abdomen width (AW), height of left
cheliped propodus (HQ), length of left cheliped propodus (LQ), wet weight (WW), and gonopod length (GL) versus the
carapace width (CW), separately for males, females and juveniles. Sample number (n), equation for total data (Total)
when no transition points are present, correlation coefficient (r), allometric level (a), positive (+), negative (-), isometric
(=), allometric growth constant (b). All measurements are in mm. All correlations were significant (P < 0.05).
Tabla 1. Austinixa aidae. Anlisis de regresin entre diferentes dimensiones corporales: Longitud del caparazn (CL),
ancho del abdomen (AW), altura del propodio del quelpodo izquierdo (HQ), longitud del propodio del quelpodo
izquierdo (LQ), peso hmedo (WW), longitud del gonoporo (GL) versus el ancho del caparazn (CW), anlisis separado
para machos, hembras y juveniles. Nmero de individuos (n), ecuacin de regresin (Total) cuando no estn presentes
puntos de transicin, coeficiente (r), alometria (a), positivo (+), negativo (-), isometra (=), constante de crecimiento
alometrico (b). Todas las medidas son en mm. Todas la correlaciones fueron significativas (P < 0,05).

Dimension Sex n Segment Y = aXb r a b

0.711
Males 246 Total CL = 0.671CW 0.967 - 0.711
CL Females 263 Total CL = 0.628CW0.764 0.956 - 0.764
Juveniles 74 Total CL = 0.743CW0.627 0.861 - 0.627
Males 244 Total AW = 0.303CW0.884 0.985 - 0.884
Females 97 < 5.1 AW = 0.139CW1.692 0.889 + 1.692
AW 164 5.1 < CW < 7.2 AW = 0.143CW1.783 0.715 + 1.783
> 7.2 AW = 0.597CW1.097 0.731 = 1.097
Juveniles 70 Total AW = 0.228CW1.197 0.916 + 1.197
Males 238 Total HQ = 0.096CW1.379 0.974 + 1.379
HQ Females 252 Total HQ = 0.114CW1.193 0.965 + 1.193
Juveniles 69 Total HQ = 0.156CW0.854 0.847 - 0.854
Males 102 < 5.1 LQ = 0.243CW1.197 0.949 + 1.197
136 > 5.1 LQ = 0.195CW1.312 0.949 + 1.312
LQ
Females 255 Total LQ = 0.275CW1.084 0.989 + 1.084
Juveniles 69 Total LQ = 0.308CW0.978 0.922 = 0.978
Males 108 < 5.7 WW = 0.00002CW4.557 0.808 + 4.557
110 > 5.7 WW = 0.0003CW2.834 0.957 - 2.834
WW Females 135 < 5.4 WW = 0.0001CW3.646 0.796 + 3.646
90 > 5.4 WW = 0.0002CW3.133 0.961 = 3.133
Juveniles 70 Total WW = 0.000008CW5.000 0.601 + 5.000
GL Males 31 < 3.0 GL = 0.134CW1.629 0.637 = 1.629
209 > 3.0 GL = 0.362CW0.876 0.974 - 0.876

slightly more rounded body than males and females,
whose carapaces become progressively narrower with
size.
As identified by dispersion points and values
obtained by the regression function between LQ and
CW, males attain sexual maturity at 5.1 mm CW (Fig.
1d, Table 1). In females, sexual maturity also occurs
from 5.1 mm CW, as indicated by the AW/CW
relationship (Fig. 1b, Table 1). This value corresponds
also to the smallest ovigerous females observed during
the study period. The ovigerous females occurred on
almost all sampled months and seasonal increases in
the frequency of this sexual category were also
identified. These features led us to characterize the
reproductive period as seasonal continuous.
DISCUSSION
Relative growth
The carapace length of males and females did not
show significant changes in the allometric pattern
during the growth. Only a few differences, for both
sexes, were detected in the CL vs CW relationship.
This pattern can be observed in many species of
 Relative growth of symbiotic crab Austinixa aidae 265

Figure 1. Austinixa aidae. Relationships between width (CW) and: a) carapace length (CL), b) abdomen width (AW), c)
height of left cheliped propodus (HQ), d), length of left cheliped propodus (LQ), e) wet weight (WW), f) gonopod length
(GL). The arrows show the transition points (white arrows for females; black arrows for males).
Figura 1. Austinixa aidae. Representacin de diferentes relaciones biomtricas entre las variables dependientes a)
longitud del caparazn (CL), b) ancho del abdomen (AW), c) altura del propodio del quelpodo izquierdo (HQ), d)
longitud del propodio del quelpodo izquierdo (LQ), e) peso hmedo (WW), f) longitud del gonopodo (GL) versus ancho
del caparazn (CW) como variable independiente. Las flechas indican los puntos de transicin (flechas blancas para
hembras y negras para machos).
266 Lat. Am. J. Aquat. Res.
Brachyura (Hartnoll, 1982; Alves et al., 2005),
including A. patagoniensis (Alves & Pezzuto, 1999;
Alves et al., 2005; Valena-Silva et al., 2008). In
contrast, the abdomen allometry is one of the best
dimensions to evidence sexual dimorphism in
brachyuran crabs (Hartnoll, 1974). The enlargement of
the female abdomen is more evident in sexually
mature individuals (Hartnoll, 1982). In Pinnotheridae,
the discontinuity in the relative growth of abdomen is
related to the sexual maturity of females (Pohle &
Telford, 1982; Bell, 1988; Alves & Pezzuto, 1999;
Alves et al., 2005), probably related to pleopodial
incubation mechanism. In the present study, a
transition stage in female abdomen growth was
apparent at 5.1 mm CW, which is probably the size at
the puberty molt. This estimate of maturity size
coincided with the size of the smallest ovigerous
females captured (5.1 mm CW). In addition, another
transition point at 7.2 mm (CW) reflects the end of the
increase in abdomen growth. As observed in the
present study, the relative growth rate of the abdomen
has a tendency to decrease as soon as it attains the
functional size (Hartnoll, 1978). This occurs because
any disproportionate increase in abdomen width could
reduce the efficiency of egg incubation, and creates
difficulties for the crabs locomotion (Hartnoll, 1982),
especially for pinnotherids which live associated with
hosts and are sometimes limited in terms of
locomotion because of the small internal space
available. In addition, the pattern of sexual
dimorphism in body size herein observed for A. aidae
represents one of some other lines of reasoning that
argues in against the idea of social monogamy in this
species, which is polygynandrous (Peir et al.,
submitted). In this sense, this topic need more work
and to be experimentally explored in the future.
In males it is possible to identify an interval in the
dispersion points at 5.1 mm CW in the relationship
involving the maximum length of the cheliped
propodus, which is related to the acquisition of sexual
maturity. The meaning of full chelar development
occurring only with maturity is related to economy of
resources, reducing the waste of energy on increase of
these structures causes during the initial instars
(Hartnoll, 1982).
Females did not show noticeable changes of
allometry in the chelae, although the relationships
showed positive allometry. Some species of
Pinnotheridae have sexually dimorphic chelae, e.g.:
Austinixa behreae (Manning & Felder, 1989),
Austinixa chacei (Wass, 1955), A. patagoniensis
(Rathbun, 1918), (see Manning & Felder, 1989),
Pinnixa faba (Dana, 1851), Pinnixa littoralis Holmes,
1894, Pinnixa minuscula Zmarzly, 1992, Pinnixa
occidentalis Rathbun, 1893, among others (see
Zmarzly, 1992). The relationships involving the
chelae indicate a smaller investment in the growth of
this structure in females, probably due to absence of
fights for territory, burrow construction or courting
behaviour, allowing females to allocate energy to the
somatic growth.
The dimensions of the left and right chelar
propodus (HQ and LQ) of A. aidae represent reliably
the size of these structures when compared with each
other, considering that both sides do not differ in size,
shape, and probably function. The same was observed
in A. patagoniensis in two different localities (Alves &
Pezzuto, 1999; Alves et al., 2005). This similarity
between both sides differs from the frequently pattern
observed in Brachyura with many levels of
heterochely (Hartnoll, 1982). The shape and size of
chelipeds are important parameters for brachyuran
lifestyles, since these structures are used in
reproductive and agonistic interactions, as well as in
feeding (Negreiros-Fransozo & Fransozo, 2003). In
mature individuals of A. aidae, the chelipeds are
strong with the palm quadrangular in males, and
rectangular with convex edges in females (Melo,
1996).
The wet weight of males showed a break in the
continuity of dispersion points at 5.7 mm CW, which
may reflect the weight at sexual maturity, occurring
0.6 mm after the relationships involving the chelae. In
females, a discontinuity of this relationship occurred
at 5.4 mm CW, which is also related to the estimated
size at sexual maturity. Although these results
corroborate the estimated sizes at maturity, they
should be treated with caution because weight can be
strongly influenced not only by body size but also by
the nutritional state of individuals and the time of
year, which add variability to the data. The juveniles
did not show transition points in weight, probably
because of limitations in the accuracy of the
measurements and/or low variation in this dimension
during this life stage.
Carapace size of male and female A. aidae was
very similar. This pattern between both sexes appears
to be common among the members of this genus (A.
patagoniensis - Alves & Pezzuto, 1998; Alves et al.,
2005; Valena-Silva et al., 2008; A. gorei -
McDermott, 2006), which may be related to the small
size attained by the specimens. However, some
differences in this size pattern were detected; for
instance, females of A. aidae attained a slightly larger
size (10.5 mm CW) than males (10.1 mm CW), which
may indicate sexual differences in growth. Females
being larger than males is not a common pattern in
brachyurans, and differs from that found for
 Relative growth of symbiotic crab Austinixa aidae
Table 2. Austinixa aidae. Maximum size of males and females, minimum size of ovigerous females and the known
reproductive periods of species of the genus Austinixa. All measures refer to carapace width (mm).
Tabla 2. Austinixa aidae. Tamao mximo de machos y hembras y tamao mnimo de hembras ovgeras y los periodos
reproductivos de especies del gnero Austinixa. Todas las medidas estn referidas al ancho del caparazn (mm).
Locality Maximum size
Species
(Latitude) Males Females
Austinixa Balnerio
11.5 11.5
patagoniensis Cassino (3213S)
Austinixa Balnerio
13.6 13.1
patagoniensis Cambori (2659S)
Austinixa Ubatumirim Beach
9.5 9.4
patagoniensis (2320S)
Perequ-au Beach
Austinixa aidae 10.1 10.5
(2324S)
A. patagoniensis in Brazil (Valena-Silva et al., 2008)
(Table 2). The larger size attained by the females
allows us to hypothesize that 1) they have a faster
growth rate than males, and 2) this may be
advantageous because the larger size may be related to
high reproductive potential and incubation of more
eggs. The physical space available for egg attachment
is a limiting factor in decapods (Reid & Corey, 1991;
Hines, 1982), and for associated pinnotherid crabs
there are still many questions to be answered, e.g., the
reproductive features (fecundity, reproductive output),
and which aspects of the reproductive biology are
adaptable to locally occurring environmental factors.
Comparing the maximum size of A. aidae with
other Austinixa species, A. aidae is slightly smaller
than A. patagoniensis and larger than A. gorei, A.
cristata, A. behreae, and A. chacei (see Manning &
Felder, 1989; Alves & Pezzuto, 1998; McDermott,
2006), which probably is related to differences in local
dynamics and hosts where the species live, and
including availability of resources in the environment,
effects of predation, and influence of latitude as well.
These small size differences among the species and
sexes may be related to latitudinal variation. In terms
of carapace size, the members of A. patagoniensis
from the southernmost regions (32o and 26oS) are
larger than at Ubatuba (23S) (Alves & Pezzuto, 1999;
Alves et al., 2005). The pattern of mean size of the
specimens, with southern crabs reaching larger sizes,
agrees with that proposed by Abele (1982), who
postulated that the size of crustaceans decreases with
decreasing latitude. According to Mantelatto et al.
(2010), the explanations for this size difference may
be related to 1) less-stressful social and energy-
demanding activities in the southern population, and
2) the possibility that this profile is acting in
267
Minimum size of Reproductive
References
ovigerous females period
Seasonal
8.0 Alves & Pezzuto (1998)
(October to March)
7.9 Continuous Alves et al. (2005)
6.7 No data available Valena-Silva et al. (2008)
Present study; Peir &
5.1 Seasonal continuous
Mantelatto (2011)
combination with differences in food limitations and
temperature between the two areas. Obviously, the
lack of information available on the size of specimens
along the species geographical distribution does not
at present allow a comparative analysis. Reproduction
is outside the scope of this paper, but it is important to
highlight the possible influence of latitude on
reproductive period. Ubatuba is subtropical and a
biogeographical boundary, where the geographical
distributions of many tropical species end and those of
temperate and subantarctic species begin (Costa et al.,
2000). This situation explains the continuous presence
of egg-bearing females of A. aidae in Ubatuba, in
contrast to the seasonal reproduction in the
southernmost population of A. patagoniensis (Table
2). The differences in minimum size attained by
ovigerous females for the different regions (Table 2)
also corroborate our hypothesis. The underlying
reasons for these differences need to be investigated in
the future, in order to clarify these patterns.
Body features, maturity, and sexual dimorphism
The carapace width of differentiated males and
females of A. aidae was, on average, 2.4 times the
length, which corresponds to the principal adaptations
of Austinixa species to live in cryptic environments.
On the other hand the unsexed juveniles were
proportionally more rounded. This feature, is shared
among species of Pinnixa and Austinixa, and has been
suggested by various authors (Zmarzly, 1992; Heard
& Manning, 1997; McDermott, 2006) to represent an
adaptation to the symbiotic lifestyle of these crabs,
which inhabit callianassid galleries and polychaete
tubes. The wider and slimmer (anterior-posterior)
body facilitates the locomotion inside the burrows
constructed by its hosts. The complexity of host use
268 Lat. Am. J. Aquat. Res.
pattern can be influenced by several factors that have
not been evaluated by us as fitness payoffs to hosts
and their symbionts, spatial patterning or density of
the host population, and the ability of symbionts to
recognize suitable hosts and to initiate and maintain
the symbiotic relationship (see Grove & Woodin,
1996, for review).
In agreement with the recognized role of the
cheliped and abdomen in reproductive functions in
Brachyura (Hartnoll, 1982; Alves et al., 2005), and the
importance for determination of morphological
maturation, the probable size of maturity for A. aidae
is 5.1 mm CW for males and females. Like their
congener, males and females of A. aidae reach sexual
maturity at similar sizes. The size of maturity of A.
patagoniensis, based on allometry studies, were
established between 7.8 and 7.9 mm CW for males
(obtained by transition points for the growth of
chelae), and between 7.9 and 8.3 mm CW for females
(obtained by transition points for the growth of the
abdomen). In addition, the sizes of maturity estimated
for each sex were identical for populations at
Balnerio Cassino, State of Rio Grande do Sul
[associated with Sergio mirim (Rodrigues, 1971)] and
Balnerio Cambori, State of Santa Catarina
(associated with Callichirus major), located farther
south in Brazil (Alves & Pezzuto, 1999; Alves et al.,
2005).
Finally, the influence of the host on crab maturity
size and maximum size of the species is not totally
clear and is still under evaluation. To better
understand the causes and the role played by host
characteristics in the natural history of A. aidae,
different studies will be necessary, such as: comparing
this natural species relationship in different areas, as
well as observations of pinnotherids interacting with
the host in a controlled laboratory setting, in order to
check if crabs are attracted to host odors during the
larvae or megalopae settlement and subsequently if
they do or do not lose this ability during the adult
stage.
ACKNOWLEDGMENTS
This study formed part of a Masters degree thesis by
DFP, and was supported by a fellowship from
CAPES. FLM and DFP are grateful to CNPq for a
research and PhD fellowships, respectively. Part of
this study was supported by funding from the CNPq
(grants 471794/2006-6 and 473050/2007-2) to FLM.
Special thanks to all members of the Laboratory of
Bioecology and Crustacean Systematics of
FFCLRP/USP for their help during field and
laboratory work, especially to Ivana Miranda for
suggestions, and to anonymous reviewers for their
suggestions and contributions toward the improvement
of this paper. The support of the Postgraduate Program
in Comparative Biology of FFCLRP/USP, and of the
Centro de Biologia Marinha (CEBIMar/USP) during
the collections are also acknowledged. We also thank
Dra. Janet Reid (JWR Associates) for revision on
English and Luis M. Pardo and Patricio Hernez for
Spanish revision. All data collection was conducted
according current applicable state and federal laws of
Brazil.
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Zar, J.H. 1996. Biostatistical analysis. Prentice-Hall,
New Jersey, 662 pp.
Zmarzly, D.L. 1992. Taxonomic review of pea crabs in
the genus Pinnixa (Decapoda: Brachyura:
Pinnotheridae) occurring on the California Shelf, with
descriptions of two new species. J. Crust. Biol.,
12(4): 677-713.
 Cryopreservation of the microalgae Chaetoceros calcitrans
Lat. Am. J. Aquat. Res., 39(2): 271-279, 2011 271
DOI: 10.3856/vol39-issue2-fulltext-8

Research Article

Cryopreservation of the microalgae Chaetoceros calcitrans (Paulsen):

analysis of the effect of DMSO temperature and light regime during different
equilibrium periods

Joan Sebastin Salas-Leiva1 & Enrique Dupr1

1
Universidad Catlica del Norte, Facultad de Ciencias del Mar
P.O. Box 117, Coquimbo, Chile

ABSTRACT. We evaluated the effect of three variables (cryoprotectant temperature, light regime, and time of
exposure to the cryoprotectant) throughout the equilibrium period during cryopreservation on the viability of
the microalga Chaetoceros calcitrans (Paulsen). For this, the cryoprotectant dimethyl sulfoxide (DMSO) at
5% (v/v) was added at three different temperatures (4, 10, and 25C) before placing the microalgae in
cryobiological straws for freezing. Once inside the cryobiological straws, the microalgal-cryoprotectant
suspensions were subjected to the following light regimes for 15 or 45 min: complete light, complete darkness,
light/darkness, and darkness/light. Suspensions were then frozen under controlled conditions and stored in
liquid nitrogen. The viability index proposed by Caavate & Lubian (1995b) was used to measure microalgal
viability after cryopreservation. Results indicated that it is necessary to use a cryoprotectant to ensure the
viable cryopreservation of C. calcitrans. Statistical analyses showed that the temperature of the DMSO
influenced the viability of cryopreserved microalgae and that there was no synergistic effect between the other
variables studied. The viabilities obtained with DMSO at 25C, 10C, and 4C were 34.9%, 27.8%, and 20.6%,
respectively.
Keywords: cryopreservation, diatoms, DMSO, temperature, light, equilibrium period.

Criopreservacin de las microalgas Chaetoceros calcitrans (Paulsen): anlisis del

efecto de la temperatura de DMSO y rgimen de luz durante diferentes
perodos de equilibrio

RESUMEN. Se evalu el efecto de tres variables la temperatura del crioprotector, el rgimen de luz y el
tiempo de exposicin al crioprotector durante el perodo de equilibrio en el proceso de criopreservacin
sobre la viabilidad de la microalga Chaetoceros calcitrans (Paulsen). Para ello se utiliz, el crioprotector
dimetilsulfxido (DMSO) al 5% (v/v), el cual fue adicionado a tres temperaturas diferentes (4, 10 y 25C)
antes de que las microalgas fueran introducidas dentro de pajuelas criobiolgicas para su congelacin. Una vez
dentro de las pajuelas, las suspensiones de microalgas con crioprotector se sometieron durante 15 o 45 min a
luz completa, oscuridad completa, luz/oscuridad y oscuridad/luz. Luego se congelaron de manera controlada y
se almacenaron en nitrgeno lquido. La viabilidad de las microalgas posterior a la criopreservacin fue
medida a travs del ndice de viabilidad propuesto por Caavate & Lubian (1995b). Los resultados indicaron
que es necesario el uso de criprotector para la criopreservacin viable de C. calcitrans. El anlisis estadstico
demostr que la temperatura del DMSO influye sobre la viabilidad de la microalga criopreservada y que no
existe efecto sinrgico entre las dems variables de estudio. Las viabilidades alcanzadas usando DMSO a
25C, 10C y 4C fueron de 34,9%, 27,8% y 20,6% respectivamente.
Palabras clave: criopreservacin, diatomea, DMSO, temperatura, luz, periodo de equilibrio.
___________________
Corresponding author: Joan Sebastin Salas-Leiva (jsalasleiva@gmail.com)

INTRODUCTION cultures. For example, species such as Chaetoceros

calcitrans offers high content of fat acids (EPA),
Microalgae used in aquaculture offer main nutritional antioxidants e immune system stimulants substances
requirements to vertebrate and invertebrate aqua- (vitamin C and B2), and its small size (2.5 to 6 m of
272 Lat. Am. J. Aquat. Res.
diameter) makes it strongly appropriated to feed
mollusks, echinoderms, crustaceans and some
zooplankton like Artemia (Brown et al., 1997, 1999;
Becker, 2004; Krichnavarruk et al., 2005; Khoi et al.,
2006).
The intensive production of microalgae for feeding
purposes, often face problems caused by loss of stock
cultures or nutritive quality of these microorganisms
(Caavate & Lubian, 1995a; Day & Brand, 2005;
Mitbavkar & Chandrashekar, 2006; Gwo et al., 2005).
For that reason, aquaculture facilities always look
for strains of microalgae from subcultures or
cryopreserved collections with biochemical profiles
suitable for feeding commercial species (Caavate &
Lubian, 1995b; Cordero & Voltolina, 1997; Day &
Harding, 2007).
Cryopreservation allows the viable storage of cells
or tissues over long periods of time at extremely low
temperatures (-196C), keeping them in a state of
suspended animation in which biological activity
practically stops (Saks, 1978). The main advantages of
microalgal cryopreservation are the immediate
availability of strains for culture, low costs of
maintenance of strains, optimal use of space and
materials, and avoidance of genetic drift that could
occur through serial transfer when cultures are
maintained long-term (Kuwano et al., 2004). Despite
the importance of cryopreservation, its application to
microalgae should be studied to better understand the
degrees of susceptibility and sensitivity of these
organisms to cryopreservation, such as: type of strain
and the effect of cell size, shape, growth and rate
phase, freezing and thawing rate, storage temperature
and duration, among others, that affect post-freezing
viability (Mortain-Bertrand et al., 1996; Taylor &
Fletcher, 1999; Rhodes et al., 2006; Day & Harding,
2007).
Cryopreservation involves three stages:
equilibrium, freezing and thawing. To protect cells
throughout the process, cryoprotectant agents (CPAs)
are added before freezing (Fuller, 2004; Dumont et al.,
2006). During the equilibrium period, the microalgae-
cryoprotectant suspension is maintained for a
predefined time to allow exchange between
intracellular solutes and the cryoprotectant solution.
Three important variables are related to the use of
CPAs: concentration, temperature and time of
exposure, and there are different methods of handling
them reported in literature. For example, tests with
DMSO concentrations ranging from 1 to 32%,
equilibrium periods lasting from 10 to 240 min and
temperatures ranging between 4 and 23C (Panis et
al., 1990), have indicated that low CPA concentrations
(< 10%) and short equilibrium periods (< 30 min) at
low temperatures (0-10C) increase post-thawing
viability (Tzovenis et al., 2004; Day, 2007). Other
studies suggest that high viability can be obtained with
concentrations of approximately 20% CPA,
equilibrium periods between 30-45 min (or longer)
and temperatures of approximately 20C (Caavate &
Lubian, 1994, 1995b, 1997a, 1997b; Poncet & Vern,
2003; Mitbavkar & Chandrashekar, 2006; Gwo et al.,
2005). These contrasting results have not only been
reported in microalgae, but also in other
microorganisms (Hublek, 2003; Wu et al., 2008).
Another important aspect during the equilibrium
period is the chemical and osmotic stress induced by
the addition of CPAs. Under stressed conditions, the
light irradiation of cells can damage the
photosynthetic systems (photosystem II). This damage
can be lethal, depending on the amount of time cells
are exposed to stress, even if it is to low-light
irradiation (Yordanov & Velikova, 2000; Murata et
al., 2007).
Several microalgae species have been
cryopreserved with different methodologies obtaining
viabilities up to 100% (Caavate & Lubian, 1994,
1995a , 1995b). In the case of species of the genera
Chaetoceros, Chaetoceros gracilis (Caavate &
Lubian, 1995b, 1997a) and Chaetoceros sp. (Cordero
& Voltolina, 1997) have shown viabilities after
cryopreservation lower than 40%. For the species
Chaetoceros muelleri, cryopreservation has been
successfully reported using DMSO 10% and 15%,
however, there are not quantitative reports of viability
(Rhodes et al., 2006).
On the basis of the information mentioned above,
this study aims to analyze the effect of the DMSO
temperature, time of exposition to this cryoprotectant
and light regimen during the equilibrium period on the
post-cryopreservation viability of C. calcitrans.
MATERIALS AND METHODS
Culture of Chaetoceros calcitrans
A strain of C. calcitrans was obtained from the
laboratory of Universidad Catlica del Norte at
Coquimbo, Chile. Two flasks of 250 mL were used to
establish two 120 mL cultures using Guillard &
Ryther (1962) medium enriched with silicate (30
Na2SiO3.9H2O). Cultures non axenic but free of
protozoan and bacteria (genera Vibrio) were
maintained at 20C, under continuous irradiation at 65
mol photons m-2 s-1 provided with cold light lamps
(Philips TL-TRS 40W/54). One culture was labeled as
t and the other, as d. Both t and d cultures were
 Cryopreservation of the microalgae Chaetoceros calcitrans
harvested on the 5th day. The t culture was carried to
intermediate culture with a volume of 1400 mL under
the conditions of culture media, temperature, and
irradiation (same conditions above mentioned). The d
culture, was used to estimate a growth curve using
different initial densities. Seven cultures of 120 mL
were inoculated with approximately 95000 (d1),
360000 (d2), 865000 (d3), 970000 (d4), 1310000 (d5),
1585000 (d6) and 2565000 (d7) cells per mL-1.
Growth according to initial and final densities was
analyzed based on a function of potential correlation
with the equation Y= aXb (Caavate & Lubian,
1995b).
The t culture was used to perform cryopreservation
tests. To begin treatments, the intermediate t culture
was harvested on the 6th day and placed in 50 mL
tubes, which were then centrifuged at 2500 rpm for 10
min. The microalgal pellet obtained was resuspended
and distributed into three 50 mL tubes to carry out all
treatments (each tube was considered a replicate of the
entire experiment and also was used to make its own
control).
Cryopreservation procedures
To apply treatments, 0.30 mL microalgal concentrate
from intermediate t culture were placed in 1.5 mL
Eppendorf tubes. The stock solution of the
cryoprotectant dimethyl sulfoxide (DMSO) was
prepared at 10% (v/v) with autoclaved and micro
filtered seawater and it was added at a ratio of 1:1
(microalgae:cryoprotectant) to each sample at three
temperatures (4, 10, and 25C). Final cryoprotectant
concentration was 5% (v/v). At each temperature, the
microalgae-cryoprotectant suspensions were intro-
duced into 0.5 mL straws (IMV France) and sealed
with polyvinyl alcohol (Sigma). The equilibrium
period lasted 15 or 45 min while the straws were
exposed to four light regimes: complete light,
complete darkness, light/darkness and darkness/light.
Light and darkness in the latter two regimes were
distributed equally as follows: for the 15 min period,
straws with microalgae were exposed to 7.5 min light
and 7.5 min darkness and vice versa; for the 45 min
period, straws were exposed to 22.5 min light and 22.5
min darkness and viceversa (Table 1). Light
irradiation in each treatment was the same mentioned
in culture conditions.
To compare the effect of cryopreservation with and
without DMSO, additional tests were carried out at
temperatures of 4, 10, and 25C and with 15 min of
equilibrium period under complete light. All straws
were filled as described before but sterilized
microfiltered seawater was added instead of the
cryoprotectant.
273
All tests were carried out using a CryoLogic CL-
3300 freezing system and the CryoGenesis V5
software. The temperature of the straws was
diminished starting at treatment temperatures (4, 10,
and 25C) down to -4C, using a cooling rate of 3C
min-1. This temperature was held for 1 min and
continuing with the freezing at the same cooling rate
down to -60C (held for 10 min). Finally, the straws
were placed in liquid nitrogen (-196C) and stored
until evaluation.
Samples were thawed using a water bath at 25C
for 2 min and the content of the straws was distributed
in 1.5 mL Eppendorf tubes. Culture medium was
added step-by-step to a 0.1 mL aliquot of microalgae-
cryoprotectant solution of each treatment in tubes.
Each tube was used to carry out a 10 mL culture under
the same growth conditions described previously. Cell
density was measured every day from the inoculation
day until day 5 using a Neubauer counting chamber
under a phase-contrast photon microscope (Nikon
Optiphot).
Evaluation of growth and viabilities
Culture growth curves were estimated using
exponential correlation. Specific growth () of C.
calcitrans was calculated using the following
equation:
(day-1) = [Ln(Cf/Ci)]/(tf- ti) (1)
where Ci is the initial cell concentration; Cf, the final
cell concentration; and t, the time of culture in days.
Specific growth () was calculated after the adaptation
phase. Growth curves were illustrated for each
treatment according to Affan et al. (2007).
The viability index (V) proposed by Caavate &
Lubian (1995b) was used to estimate post-
cryopreservation viability:
V = [(C0/Ci)x(C5/(aC0b)] x 100 (2)
where C0 is the inoculation density (day 0); C5, final
density for day 5 of culture; Ci, maximum initial
density (dilution 1:100 prior to cryopreservation); a
and b, are regression coefficients obtained for 5 days
in relation to C0 in the d cultures.
The term aC 0 b is equivalent to the expression
aX b in a potential equation.
The experiment corresponded to a completely
randomized factorial design that generated 24
treatments (Table 1), each with three replicates. Three
non-cryopreserved controls and d cultures were
available throughout the process. Viability indexes (V)
were calculated for each replicate and were compared
using a factorial ANOVA, followed by Duncans
274 Lat. Am. J. Aquat. Res.
Table 1. Light regime, temperature, and time of exposure of microalgae to DMSO during the equilibrium period for the
different treatments (T).
Tabla 1. Rgimen de luz, temperatura y tiempo de exposicin de las microalgas durante el tiempo de equilibrio para los
diferentes tratamientos (T).
Light regime Complete light Complete darkness
Time of exposure DMSO temperature (C)
(min) 4 10 25 4 10
15 T1 T9 T17 T2 T10
45 T5 T13 T21 T6 T14
multiple range tests. All statistical analyses were
performed with a 95% confidence level ( = 0.05)
using Statsoft statistics software version 7 (Statsoft,
UK).
RESULTS
Non-cryopreserved cultures (controls)
Cell growth was similar in controls of all replicates
and there were no significant differences among them
(P > 0.05). Growth curves showed correlation
coefficients ranging between 0.86 and 0.89. Average
initial density and on the fifth day were 2.0 x 106 cells
mL-1 and 3.5 x 106 cells mL-1respectively. Controls
and d cultures showed similar growth tendencies (Y =
aebx). The specific growth rate was faster in cultures
obtained from inoculations with low cell density mL-1
(Table 2). The correlation aXb for d cultures indicated
an inverse relationship between initial and final
inoculation densities (Y = 1 x 106 X-0.072; R2 = 0.8325).
Cryopreservation of Chaetoceros calcitrans
Post-cryopreservation cultures
All cryopreservation tests without DMSO at 4, 10 and
25C, resulted in complete cell death on day 2 of
culture post-cryopreservation. In those treatments
using DMSO, different percentages of viability were
observed after thawing (day 5).
Initial culture densities of post-cryopreservation
treatments at time of inoculation (C0) ranged between
3.1 x 105-7.7 x 105 cells mL-1, and densities on day 5
of culture (C5) varied between approximately 2.5 x
106-3.7 x 106 cells mL-1. Growth curves of the 24
treatments exposed to cryopreservation exhibited an
adaptation phase within the first two days of culture.
High cell death and low densities were observed on
day 2 in all cultures. From day 3 on, evidence of an
exponential growth phase was determined from a high
cell growth rate (Fig.1).
Light/darkness Darkness/light
25 4 10 25 4 10 25
T18 T3 T11 T19 T4 T12 T20
T22 T7 T15 T23 T8 T16 T24
Specific growth ( day-1) was higher in cultures of
cryopreserved cells than in non-cryopreserved cells
(controls). Growth curves of treatments, as well as,
specific growth rates were similar to those reported for
d cultures. The highest specific growth rates in
cryopreserved treatments were reached with the
treatment with the lowest cell densities (treatments 17,
15, and 13) and conversely, low specific growth rates
were reached with treatments with higher cell
densities (treatments 22, 23, and 18) (Table 2). Of the
treatments with DMSO at 4 and 10C, 93.75%
presented average growth rates above 1 ( day-1),
whereas only 50% of the treatments with DMSO at
25C exceeded that same growth rate. Controls
presented a growth rate of 0.11 day-1.
Estimation and comparison of viability
The average initial concentration (Ci) before
cryopreservation was of 2.0 x 106 cells mL-1. The
viability of C. calcitrans in all cases was higher than
12.2% (treatment 15) and did not exceed 34.9%
(treatment 22) (Table 2, Fig. 2). A factorial ANOVA
was performed to identify those variables that most
influence the viability of cryopreserved C. calcitrans.
Data (proportion of viability) presented a normal
frequency distribution according to the Kolmogorov-
Smirnov test (P > 0.05), and variance homogeneity
was verified according to Levenes test (P > 0.05).
Hypotheses of the statistical model and their
interactions were compared by parametric statistical
analysis, which indicated that only the temperature of
DMSO had a significant effect (P < 0.05) on the
viability of cryopreserved C. calcitrans (Table 3).
Duncan multiple range analysis, performed after the
factorial ANOVA, revealed significant differences
between the temperatures of 4 and 25C and between
10 and 25C (P < 0.05), whereas there were no
significant differences between the temperatures of 4
and 10C. Although analyses indicated that the light
regimen had no statistically significant effect, average
 Cryopreservation of the microalgae Chaetoceros calcitrans 275

Table 2. Growth rates ( day-1) and viabilities indexes of Chaetoceros calcitrans. Controls, d cultures and treatments.
Tabla 2. Tasas de crecimiento ( dia-1) e ndices de viabilidad para Chaetoceros calcitrans. Controles, cultivos d y trata-
mientos.

Treatment day-1 Viability index (%) Treatment day-1 Viability index (%)
Control 0.11 0.04 9 1.16 0.22 21.5 2.72
d1 1.28* 10 1.25 0.49 21.1 12.78
d2 0.83* 11 1.05 0.32 22.9 3.53
d3 0.51* 12 1.30 018 21.5 11.10
d4 0.47* 13 1.41 0.19 14.1 0.89
d5 0.35* 14 1.01 0.35 27.8 17.55
d6 0.28* 15 1.58 0.04 12.2 3.08
d7 0.10* 16 1.10 0.45 19.5 12.54
1 1.10 0.13 19.1 6.90 17 1.67 0.30 16.7 11.57
2 1.28 0.41 15.5 7.64 18 0.75 0.23 31.7 7.71
3 1.20 0.25 18.5 9.89 19 1.03 0.19 29.0 10.60
4 1.15 0.38 20.6 1.94 20 0.88 0.06 23.5 4.73
5 0.88 0.15 19.3 13.75 21 1.09 0.17 14.8 6.53
6 1.16 0.23 15.6 8.44 22 0.70 0.03 34.9 7.82
7 1.03 0.18 16.6 9.25 23 0.77 0.08 32.7 7.84
8 1.09 0.28 16.0 4.96 24 1.04 0.38 21.4 14.43
*single measurements
Data highlighted in bold indicates the highest viabilities.

Figure 1. Growth curves of all treatments exposed to

cryopreservation (numbers to the right indicate
treatments; Ctrl: control).
Figura 1. Curvas de crecimiento de todos los trata-
mientos sometidos a criopreservacin, (Nmeros a la
derecha: indica el tratamiento y Ctrl: control).

viability tended to increase with complete darkness
and a 15 min of time of exposure.
DISCUSSION
Growth and cryopreservation
Cell growth of Chaetoceros calcitrans was similar in
both d and t cultures (prior to cryopreservation). No
adaptation phase was detected in either culture. If it
did occur, it was very mild, similar to that reported by
Phatarpekar et al. (2000) for the same species; this
could be attributed to faster cellular reproduction than
in other species. For example, adaptation phases
longer than 1 day have been reported for Chaetoceros
muelleri and C. gracilis, Tetraselmis tetrathele and T.
gracilis, Dunaliella salina and D. tertiolecta, and
Navicula incerta, among others (Caldern & Serpa,
2003; Leal et al., 2003; Affan et al., 2007; Moura-
Junior et al., 2007). The specific growth rates of d
cultures were higher with low densities of inoculated
cells as it was expected; since they are conditioned by
factors such as nutrient depletion, pH alteration, CO2
deficiency, and reduced light penetration, among
others (Fogg & Than-Tun, 1960).
276 Lat. Am. J. Aquat. Res.

It was only possible to generate viable cell cultures of

Figure 2. Effect of temperature of DMSO (5%) during
the equilibrium period on viability of Chaetoceros
calcitrans.
Figura 2. Efecto de la temperatura del DMSO (5%)
durante el perodo de equilibrio sobre la viabilidad de
Chaetoceros calcitrans.
C. calcitrans when DMSO was added. Low or no
viability has been reported for the species C. gracilis
(Caavate & Lubian, 1995b), Chaetoceros sp.
(Cordero & Voltolina, 1997), and Nannochloropsis
oculata (Gwo et al., 2005) in the absence of CPA.
Although viabilities up to 69% have been obtained
without using CPA for Tetraselmis chuii,
Nannochloropsis gaditana and Nannochloris atomus
(Caavate & Lubian, 1995b) and, certain
Chlorococcaceae and Cyanobacteria (Day et al.,
2000). Such differential responses to cryopreservation
(with/without cryoprotectant) depend directly on each
species physiological mechanisms to tolerate osmotic
stress induced by below-zero temperatures. In the case
of C. calcitrans, its reaction to cryopreservation
without DMSO could be explained by the excessive
dehydration at the intracellular level caused by the
formation of extracellular ice crystals that promote
cell death (Tanaka et al., 2001; Day & Harding, 2007).

Table 3. Factorial variance analysis (ANOVA) of viability post-cryopreservation of C. calcitrans. SS: sum of squares.
DF: degrees of freedom. SM: square of the mean, and F values and P value.
Tabla 3. Anlisis de Varianza Factorial (ANOVA) de la viabilidad posterior a la criopreservacin de C. calcitrans. SS:
Suma de cuadrados. DF: grados de libertad. SM: Cuadrado de la media, F y P (estadsticos).

Variable SS DF SM F value P value

Temperature (DMSO) 0.079 2 0.039 4.638 0.014
Light regime 0.044 3 0.014 1.735 0.172
Time of exposure 0.003 1 0.003 0.408 0.525
Temperature x light regime 0.094 6 0.015 1.841 0.110
Temperature x time of exposure 0.004 2 0.002 0.290 0.749
Light regime x time of exposure 0.013 3 0.004 0.521 0.669
Temperature x light regime x time of exposure 0.019 6 0.003 0.375 0.891
Error 0.411 48 0.008

Mechanical damage, cannot be discarded because
several organelles could have been destroyed. The
responses to cryopreservation obtained in this study,
as well as the results of Cordero and Voltolina (1997)
in Chaetoceros sp., suggest that the presence of CPAs
is necessary for post-freezing cell recovery in
Chaetoceros microalgae as in other microorganisms.
DMSO has shown high levels of toxicity in several
species (Caavate & Lubian, 1994; Fuller, 2004).
Although in the case of C. calcitras was indispensable
to obtain viable cells after criopereservation, which
indicates a natural tolerance to this kind of substances
in its cytoplasm. Natural tolerance for freezing and
hiperosmotic substances in other diatoms of this
genera, such as Chaetoceros castracanei and species
from Artic and Antartic, has been attributed to the
accumulation of free amino acids (mainly proline) and
DMSP (a DMSO precursor) (Ferrario et al., 2004;
Mock & Thomas, 2005; Houdan et al., 2005; Ralph et
al., 2005).
Effectiveness of cryopreservation
The maximum mean viability reached in this study
was 34.9%. In studies conducted by other authors
(Caavate & Lubian, 1995b, 1997a, 1997b), the
viabilities of different non-diatom microalgae treated
with CPA reached 100%, whereas viabilities for
diatoms such as C. gracilis were below 40%, this
suggests that, within the physiological mechanisms of
diatoms to respond to osmotic stress, the presence of a
rigid silicon wall seems to play an important role in
cryopreservation because it could confer fragility to
 Cryopreservation of the microalgae Chaetoceros calcitrans
the cryopreserved cell (rupture during freezing or
thawing). Mortality caused by that fragility could be
minimized, in the case of C. calcitrans, by the high
surface/volume ratio of this species, which, would
help reduce the formation of intracellular ice
(Mortain-Bertrand et al., 1996). However, this should
not be considered a rule for small-sized diatoms
because other factors, such as rate of freezing and
thawing, also affect microalgae viability, regardless of
the inherent conditions of the cells and growth
conditions (Ben-Amotz & Gilboa, 1980a, 1980b;
Caavate & Lubian, 1997a, 1997b; Day et al., 1998).
The analysis of the variation of V indicated that the
temperature of DMSO during the equilibrium phase is
the factor that most influences post-freezing viability
of C. calcitrans. The Duncan multiple range test
indicated that viability at 4 and 10C is lower than at
25C. Based on these results, the optimal temperature
of DMSO during the equilibrium phase of
cryopreservation of C. calcitrans is 25C. This
temperature is close to the range mentioned by Taylor
& Fletcher (1999), who recommended using
equilibrium temperatures between 18 and 23C, as
well as to that proposed by other authors (Caavate &
Lubian, 1995b,1997a, 1997b), who obtained high
viabilities (> 90%) with different microalgae species.
Studies conducted by Tanaka et al. (2001) also
indicated that temperatures close to 23C facilitate the
osmotic exchange of DMSO solution and the cell
during the equilibrium period, because increasing
temperatures increase molecular movement and
kinetic energy of the H2O-DMSO solution; this causes
DMSO diffusion to proceed faster at 25C with the
appropriate solute concentration than at 4 and 10C. In
this study, when DMSO was added at 4 and 10C,
average V were lower than 20%, contrary to what was
found by other authors (Panis et al., 1990; Mortain-
Bertrand et al., 1996; Hublek, 2003) who suggested
that temperatures between 0 and 10C during the
equilibrium period are appropriate for cryopre-
servation because they protect the cells from CPA
toxicity since at physiological temperatures, the
cryoprotectant is highly toxic. We suggest that it is
more important to ensure the entry of DMSO into the
cell than to try to minimize its toxicity because the
freezing/thawing process apparently has a more
traumatic effect than that induced by CPA toxicity.
In addition to the temperature and concentration of
DMSO, the length of the equilibrium period is also an
important aspect to be considered. In this study,
statistical analyses indicated that the length of two
equilibrium periods (15 and 45 min) with DMSO does
not have a significant effect on the viability of C.
calcitrans. This can be attributed to DMSO is a fast-
277
penetrating cryoprotectant and does not require a
prolonged equilibrium period to yield good results, as
compared with slow-penetrating CPAs, such as
glycerol, that need more than 60 min (Karlsson &
Toner, 1996; Day et al., 1998; Hublek, 2003; Fuller,
2004). The DMSO rate of penetration during the
equilibrium period depends on cell size and type,
differential permeability of cell membranes, and
membrane lipid content. Therefore the lengths of
effective equilibrium periods vary from species to
species (Salinas-Flores et al., 2008). Norton & Joiner
(1968) reported DMSO 7.5% and equilibrium periods
up to 149 min to cruopreserve sporocites of Eimeria
tenella due its low permeable membrane.
There are no reports on the effect of using light
regimens during the equilibrium period similar those
used in this study. The light regime results did not lead
to the detection of significant differences in viability;
however, it is interesting to note a pattern of low
viabilities seen in those treatments that included
complete light. This result could be attributed to
alteration or damage in the electron transport system.
This has been described for the green algae
Chlamydomonas reinhardtii where severe damage was
observed in the electron transport chain when the
algae was exposed to methanol in the presence of light
during the equilibrium period. Piasecki et al. (2009)
recommend that these microorganisms be cultured
under very low light or in complete darkness during
this phase.
Finally, post-cryopreservation cell survival or
mortality can be mainly attributed to the existence of
several levels of genetic variability (Medlini et al.,
2000), which would be responsible for the differential
response of C. calcitrans cells to osmotic stress and
post-freezing survival lower than 100% (Fahy, 1986).
ACKNOWLEDGEMENTS
This study was supported by Fondef Grant D05 I-
10246. Our sincere appreciation to Dr. Dayana Salas-
Leiva for her assistance in the statistical design of this
study, the critical reading of the manuscript, and her
helpful comments. We want to thank to Roberto
Garca for his help during the experimental phase of
this study.
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DOI: 10.3856/vol39-issue2-fulltext-9

Research Article

Assessment of catalase activity, lipid peroxidation, chlorophyll-a, and

growth rate in the freshwater green algae Pseudokirchneriella subcapitata
exposed to copper and zinc

Paulina Soto1, Hernn Gaete1,3 & Mara Eliana Hidalgo2

1
Departamento de Biologa y Ciencias Ambientales
2
Departamento de Qumica y Bioqumica
3
Centro de Investigacin y Gestin de Recursos Naturales (CIGREN), Facultad de Ciencias
Universidad de Valparaso, Valparaso, Chile

ABSTRACT. In this work, the effect of copper and zinc on green alga Pseudokirchneriella subcapitata was
evaluated through catalase activity, lipid peroxidation by TBARS essay, growth rate, and the chlorophyll-a
concentration. Catalase activity increased significantly (P < 0.05) in comparison to the control at 0.1 mg L-1
copper and 0.075 mg L-1 zinc, whereas the damage to the cell membrane expressed as nmols/106cell of
malondialdehyde increased significantly (P < 0.05) at 0.025 mg L-1 copper and 0.1 mg L-1 zinc. On the other
hand, a significant (P < 0.05) decrease in chlorophyll-a concentration was found at 0.075 mg L-1 of both
metals. The results showed that catalase activity, lipid peroxidation, and chlorophyll-a concentration were
more sensitive to metals than the growth rate.
Keywords: toxicity, bioassays, water quality, oxidative damage, Pseudokirchneriella subcapitata, Chile.

Evaluacin de la actividad de la catalasa, peroxidacin lipdica, clorofila-a y tasa de

crecimiento en la alga verde de agua dulce Pseudokirchneriella subcapitata
expuesta a cobre y zinc

RESUMEN. En este trabajo, se evalu el efecto del cobre y zinc en la alga verde Pseudokirchneriella
subcapitata a travs de la actividad catalasa, peroxidacin lipdica por el ensayo TBARS, tasa de crecimiento
y concentracin de clorofila-a. La actividad catalasa aument significativamente (P < 0,05) en comparacin al
control en 0,1 mg L-1 y 0,075 mg L-1 de cobre y zinc respectivamente, mientras que el dao en la membrana
celular expresado en nanomols/106 clulas de malondialdehdo aument significativamente en 0,025 mg L-1 y
0,1 mg L-1 de cobre y zinc respectivamente. Por otra parte, hubo una disminucin significativa (P < 0,05) en la
concentracin de clorofila-a en ambos metales a 0,075 mgL-1. Los resultados mostrados en actividad catalasa,
peroxidacin lipdica y concentracin de clorofila-a son parmetros ms sensibles que la tasa de crecimiento a
los metales.
Palabras clave: toxicidad, bioensayos, calidad de agua, dao oxidativo Pseudokirchneriella subcapitata,
Chile.
___________________
Corresponding author: Hernn Gaete (hernan.gaete@uv.cl)

INTRODUCTION an essential redox-active transition metal, which acts

Metals such as copper and zinc are released into the
aquatic ecosystems by anthropogenic activities such as
agricultural, industrial and mining (Yruela, 2005). In
this ecosystems the primary producers play an
important role in the structure and functioning of
aquatic ecosystems. Any negative effect on them will
affect upper trophic levels (Li et al., 2006). Copper is
as a structural element in regulatory proteins, and
participates in electron transport in photosynthesis,
mitochondrial respiration, oxidative stress responses,
cell wall metabolism and hormone signaling (Moreno,
2003; Srivastava et al., 2006). Zinc is essential for the
stability of cell membranes in the activation of over
300 enzymes in the metabolism of proteins and
nucleic acids (Cakmak & Marschner, 1988). However,
281 Catalase, lipidperoxidation, chlorophyll-a and growth in P. subcapitata exposed to copper and zinc
in high concentrations these metals can be toxic to
aquatic organisms (Srivastava et al., 2006).
The metals, as other environmental factors
(ultraviolet light, extreme temperatures, radiation,
environmental pollution, etc.) induce ROS (reactive
oxygen species) formation inside the cell (Marshall &
Newman, 2002). These ROS are formed under
physiological conditions in manageable proportions,
while maintaining a balance due to the defensive
cellular enzymes (Drge, 2003). The breakdown of
this balance is known as oxidative stress, which results
in alterations of the structure-function of organs,
systems, or specialized transport (Ames et al., 1993).
The damage caused by oxidative stress in fatty acid
rich structures, such as cell membranes, results in lose
rigidity, integrity and permeability. This process
known as lipidperoxidation, produces carbonylic
compounds such as malondialdehyde. Aerobic
organisms have developed antioxidant defence
mechanisms to prevent cell damage by ROS (Finkel &
Holbrook, 2000; Sohal et al., 2002). The enzyme
catalase has an active participation in the reactions that
reduce the intracellular levels of H2O2 formed from
the superoxide radical (De Zwart et al., 1999).
Although copper can act at many different levels in
the cell, one of the most important mechanisms of
copper action in green plants is believed to be the
inhibition of electron transfer in the chloroplasts, the
destruction of the chloroplast membrane, and
inhibition of the photosynthetic pigments formation
(Yan & Pan, 2002; Charles et al., 2006).
The microalga of freshwater Pseudokirchneriella
subcapitata has been used in toxicity bioassays due to
their sensitivity to chemicals agents. In these tests, the
exposed population rate growth is the response
variable determinated (NCh2706, 2002). At present, it
is known that the molecular alterations are the first
detectable, quantifiable responses, allowing the
evaluation of exposure to agents at sublethal level.
The biomarker concept is based in that the first level
of interaction of pollutants with organisms is the
molecular-cellular (Huschek & Hansen, 2005).
The studies on oxidative stress caused by metals in
microalgae are few, the most are in green plants
(Okamoto et al., 1996; Lee & Shin, 2003; Elisabetta &
Gioacchino, 2004; Mallick, 2004; Li et al., 2006).
The lipidperoxidation`s products determination
(TBARS), together with the evaluation of the catalase
activity are effective methods used to assess oxidative
stress (Scandalios, 1997; Nordberg & Arne, 2001). In
this research is proposed that the molecular response
is more sensitive than the response at the population
level in P. subcapitata exposed to copper and zinc.
The goal of this study is to evaluate the effect of
copper and zinc on P. subcapitata, through the activity
of catalase, lipidperoxidation by TBARS assay,
growth rate and concentration of chlorophyll-a.
MATERIALS AND METHODS
The green alga species Pseudokirchneriella
subcapitata, belonging to the order Chlorococcales,
class Chlorophyceae, was acquired in the Laboratory
of Phycology of University of Concepcin, Chile.
Bioassays
The bioassays were carried out according to the
Chilean standard NCh2706 (2002). Prior to the
bioassay a nutrient solution consisting of five stock
solutions, which contain: micronutrients, macro-
nutrients, Fe-EDTA, trace elements and NaHCO3 was
prepared. The algae was inoculated into 500 mL
Erlenmeyer flasks in an equal volume for all samples,
from culture stock during the exponential phase of
growth. Then, they were enriched with the nutrient
concentration to avoid false negatives, and volumes of
copper sulphate pentahydrate (CuSO4.5H2O) and zinc
sulphate heptahydrate (ZnSO4. 7H2O) were added
until a concentration of 0.025, 0.05, 0.075 and 0.1 mg
L-1 of Cu and Zn respectively. Finally, the flask was
adjusted to 300 mL with distilled water. Additionally,
a blank was prepared containing only the inoculum of
P. subcapitata, nutrients and water. Each treatment
and the blank, in triplicate, was exposed to continuous
cool white light with a low intensity of 90 10 mol
m-2 s-1, at 23C 2C and shaken by hand every day.
To have a biomass of microalgae that would make the
determinations, the exposure time was 15 days. The
cell density (n) was determined at the beginning and
the end of the bioassay counting directly in a
microscope using a Neubauer Bright Line
hemacytometer.
The growth rate (k) expressed as number of cell
duplications was determined from:
k = 3,322 x log Nn log N0
tn
Where tn is the time elapsed between the start and
end of the trial (in days), N0 is the nominal initial cell
density and Nn is the density at the end of the test.
Chlorophyll-a
To determine the chlorophyll-a concentration, 100 mL
of the sample was filtered and immersed in acetone
(90% V/V) for 20 h in darkness and cold. The
absorbance of the solvent was determined at 630, 645
 Lat. Am. J. Aquat. Res.
and 665 nm in a spectrophotometer (Cecil CE 2000
model 2041). The chlorophyll-a concentration was
calculated through the Richards & Thompson (1952):
mg chl-a m3 = (15, 6 E665 2 E645 0,8 E630) x 10
V
Where E665 is the absorbance at 665 nm, E645 the
absorbance at 645 nm, E630 at 630 nm and V the
volumen sample leaked.
Oxidative stress parameters
A volumen of 200 mL of each treatment was
centrifuged and frozen with liquid nitrogen before
grinding it with a mortar. Two mL of buffer 50 mM
sodium phosphate (pH 7.0) were added to obtain an
approximate volume of 3 mL, 1 mL of which was
used to measure thiobarbituric acid reactive species
(TBARS) and the remaining 2 mL to determine the
enzymatic activity of catalase (CAT).
Determination of thiobarbituric acid reactive
species (TBARS)
Lipidperoxidation was determined using the TBARS
assay: samples were treated with trichloroacetic acid
and then with thiobarbituric acid, the complex formed
absorbed at 540 nm, the results are expressed in
nanomoles of MDA/106 cells. MDA content was
calculated using the calibration curve of MDA bis
dimethylacethal.
Catalase activity (CAT)
The enzymatic activity of catalase was determined, by
spectrophotometry following the hydrogen peroxide
degradation rates for 1 min every 15 sec, at 240 nm
which is accelerated in the presence of enzyme
(Ratkevicius et al., 2003; Contreras et al., 2005;
Cargnelutti et al., 2006; Hidalgo et al., 2006). The
sample (2 mL) was concentrated by centrifugation at
3500 rpm for 15 min. A blank (2.9 mL sodium
phosphate buffer pH 7.0 and 100 mL of supernatant)
was used. The results are expressed as U/106 cells (Li
et al., 2006). The results were analyzed through the
analysis of variance Anova and correlation determined
with the program Systat 5.0. For each treatment three
replicates were considered.
RESULTS
The growth rate of P. subcapitata exposed to copper
decreased at 0.075 mg L-1, while in the presence of
zinc no statistically significant differences to the
control was found in the range of concentration tested
(Fig.1), however correlations with metal concen-
282
Figure 1. Growth rate of P. subcapitata exposed to
copper and zinc *: significant difference to the control (P
< 0.05)( n:4).
Figura 1. Tasa de crecimiento de P. subcapitata
expuesta a cobre y zinc *: diferencia significativa al
control (P < 0,05).
trations (Table 1) were observed. The concentration of
chlorophyll-a decreased significantly at copper
concentration 0.05 mg L-1 and zinc concentration
0.075 mg L-1. However an increase of chlorophyll-a at
0.025 mg L-1 of copper was observed (Fig. 2). Only
the correlation with zinc was significant (Table 1).
The catalase activity increased in comparison to
the control in 0.075 mg L-1 and 0.05 mg L-1 of copper
and zinc, respectively (Fig. 3). Zinc induced the
activation of the antioxidant enzyme catalase at lower
concentration than copper. The correlation between
metal concentration and catalase activity was
significant only for zinc (Table 1). There was
significant correlation between lipid damage
expressed as malondialdehyde content and catalase
activity (Table 1). The lipid damage in the cell
membrane was higher with copper than zinc. The
damage was observed in exposure to 0.025 mg L-1
copper, while for zinc it was observed at 0.1 mg L-1
(Fig. 4). In this case, the correlation between damage
to the cell membrane expressed as nmols/106cell of
malondialdehyde was significant to copper and zinc
(Table 1).
DISCUSSION
Copper was more toxic than zinc in relationship at the
rate growth, chlorophyll-a content and, lipope-
roxidation endpoints, wich is similar to what was
reported by Utgikar et al. (2004) in Vibrio fischeri.
However, copper toxicity was lower than what was
found by Kaneko et al. (2004); these autors reported
an IC50 at 0.11 mg L-1 of copper in Selenastrum
capricornutum, similar values were reported by
Bossuyt & Janseen (2004) in the same species, our
283 Catalase, lipidperoxidation, chlorophyll-a and growth in P. subcapitata exposed to copper and zinc

Table 1. Correlation between measured parameters.

Tabla 1. Correlacin entre los parmetros medidos.

Concentration CatCu CatZn ClofCu ClofZn MdaCu MdaZn

CatCu 0.71
CatZn 0.98* -
ClofCu 0.74 -0.53 -
ClofZn -0.93* - -0.96*
MdaCu 0.92* 0.93* - -0.69
MdaZn 0.81 - 0.78 - -0.88*
Cu -0.88* -0.92* - 0.74 - -0.98*
Zn -0.90* - -0.95* - 0.90* - -0.78
Concentration : metal concentrations; CatCu: catalase activity exposured to copper; CatZn: catalase
activity exposured to zinc; ClofCu: Chlorophyll-a exposured to copper; ClofZn: chlorophyll-a exposure
to zinc; MdaCu: MDA production exposured to copper ; MdaZn : MDA production exposured to
zinc; Cu: growth rate exposured to copper; Zn: growth rate exposured to zinc. *: indicate significant
correlation (P < 0.05).

Figure 2. Chlorophyll-a concentrations in P. subcapitata

exposed to copper and zinc. *: significant difference to
the control (P < 0.05).
Figura 2. Concentracin de clorofila-a en P. subca-
pitata expuesta a cobre y zinc. *: Indica signifi-
cativamente diferente al control (P < 0,05).
Figure 4. Effect of copper and zinc different
concentrations on MDA production in P. subcapitata. *
:Indicate significantly different to the control (P < 0.05).
Figura 4. Efectos del cobre y zinc a diferentes
concentraciones sobre la produccin de MDA en P.
subcapitata. *: Indica significativamente diferente al
control (P < 0,05).

study show that at copper concentration similar the

Figure 3. Catalase activity in P. subcapitata exposed to
copper.and zinc. *: significant difference to the control
(P < 0.05).
Figura 3. Actividad catalasa en P. subcapitata expuesta
a cobre y zinc. *: Indica significativamente diferente al
control (P < 0,05).
inhibition on the rate growth was less to twenty
percent. The differences may be due to the chemical
characteristics of test water, such as pH, hardness,
time exposure, concentration and type of chelating
agent in the nutrients used in the these studies. On the
other hand, the differences in the effects of the
respective metals could be attributed to the redox
potential of the metals. Copper has a greater redox
potential that zinc (Cu E = 0.16 and Zn E = -0.76)
which would lead to an increased oxidant effect at
lower concentrations.
 Lat. Am. J. Aquat. Res.
A manifestation of the hormesis effect was
expressed under the Cu exposure. The stimulation of
chlorophyll-a at the most low concentration of copper
was similar to that founded by Knauer et al. (1997)
and Janssen & Heijrick (2003). Whitton (1970)
reported that the algae growth may be stimulated by
low metal concentrations and inhibited at high metal
concentrations. The parameter chlorophyll-a concen-
tration was more sensitive than growth rate. The
lowest content of chlorophyll-a in the higher
concentrations of the metals can be due to the
peroxidation of chloroplast membranes. Metals can
destabilize the membrane by oxidation due to free
radicals formation. Copper alters membrane tilacoides
and causes changes in its composition (De Vos et al.,
1991), interference with the photosynthetic system and
the a decline in the rate of photosynthesis (Cook et al.,
1997; Yruela, 2005). Our results differ from those
reported by Bossuyt & Janssen (2004), who found a
significant increase in chlorophyll-a at higher
concentrations of metals in P. subcapitata. However,
these authors used a different medium to that used in
the present study and their cultures were acclimated
previously to 60 and 100 g L1, which would explain
the differences with our results.
The catalase activity was higher in the highest
concentrations tested. Similar results are reported by
Li et al. (2006) when Pavlova viridis was exposed to
copper and zinc. Contrarily, Srivastava et al. (2006)
found that the catalase enzyme is dependant on
concentration-time, their results show an increase in
catalase activity until the 7 day of exposure with 108%
induction. However, catalase activity declines in
plants exposed to up 5 and 25 M copper
independently of the exposure duration, indicating a
maximum decline of 42% on day 7 at 25 M,
probably due to enzyme degradation at higher free
radicals concentration. Tripathi et al. (2006) reported
less catalase activity at lower concentrations in
Scenedesmus sp. when exposed to copper and zinc,
than the present study. The results in our work suggest
that the antioxidant enzyme catalase plays an
important role at higher toxicant concentrations in P.
subcapitata. The antioxidant catalase in P. subcapitata
was protective at lower concentrations in P.
subcapitata exposed to zinc compared to copper
exposure.
Both metals provoked damage to lipid. MDA
content increased significantly from 0.025 mg L-1 and
1.0 mg L-1 in copper and zinc respectively, indicating
rise in lipid peroxidation in P. subcapitata. This is
similar to that found by Li et al. (2006) with the
microalga Pavlova viridis (Prymnesiophyceae), whose
results show that the MDA content is expressed
284
significantly from 0.5 mg L-1 of copper and 3, 25 mg
L-1 of zinc. The difference with our work can be
explained by the different sensibility between species.
Similarly, Srivastava et al. (2006) reported a gradual
increase in the content MDA and significant
differences to the control in Hydrilla verticillata at the
highest concentration of copper tested.
In conclusion, both metals induce the antioxidant
activity of catalase. Copper induces lipidperoxidation
at lower concentrations than zinc. Copper and zinc
cause adverse effects on the physiology of P.
subcapitata determined through the content of
chlorophyll-a. The growth rate was less sensitive to
the metals that catalase activity, lipidperoxidation and
chlorophyl-a content. The molecular parameters can
be more adecuate than growth rate to monitoring the
effect in microalgae aquatic ecosystems.
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Research Article

Biologa de la raya guitarra Rhinobatos leucorhynchus (Gnther, 1867)

(Rajiformes: Rhinobatidae) en el Pacfico colombiano

Luis Fernando Payn1, Andrs Felipe Navia1, Efran A. Rubio2 & Paola Andrea Meja-Falla1
1
Fundacin Colombiana para la Investigacin y Conservacin de Tiburones y Rayas, SQUALUS
Carrera 79 N 6-37, Cali, Colombia
2
Universidad del Valle, Departamento de Biologa, Seccin de Biologa Marina
A.A. 25360, Cali, Colombia

RESUMEN. La raya guitarra Rhinobatos leucorhynchus es comnmente capturada como fauna acompaante
en la pesca del camarn de aguas someras del Pacfico colombiano, tanto a nivel industrial como artesanal. A
partir de 286 ejemplares capturados incidentalmente entre 2001 y 2007, se estudiaron diferentes aspectos
biolgicos de esta especie. Las hembras fueron proporcionalmente ms grandes que los machos, aunque el
crecimiento fue similar en ambos sexos (alomtrico). Los embriones no presentaron diferencias sexuales
significativas ni en talla ni en peso. La proporcin sexual en adultos fue 2,4:1 (hembras-machos), mientras que
en embriones esta proporcin fue de 1:1. El 51,5% de machos present claspers desarrollados y calcificados y
el 56,5% de las hembras estaban grvidas, presentando fecundidades entre 1 y 6 embriones, con tallas entre 3
y 19,5 cm, sugiriendo una talla de nacimiento entre 19 y 19,5 cm LT. La talla mediana de madurez de las
hembras fue menor que la de machos (48,48 cm y 51,18 cm LT, respectivamente), y las hembras presentaron
cras a partir de 44 cm LT. Los hbitos alimentarios de esta especie mostraron 30 tems presa, con camarones
de la familia Penaeidae, y especialmente Trachypenaeus sp. como alimento principal. La raya guitarra
present diferencias significativas en la dieta de machos y hembras, y la amplitud de nicho indic que es
especialista en su dieta. Los resultados de este estudio aportan informacin til para plantear medidas de
manejo de R. leucorhynchus, especie que requiere atencin, dado sus caractersticas biolgicas y su
importancia comercial y de consumo.
Palabras clave: batoideos, reproduccin, crecimiento, dieta, ecologa alimentaria.

Biology of the guitar ray Rhinobatos leucorhynchus (Gnther, 1867)

(Rajiformes: Rhinobatidae) in the Colombian Pacific

ABSTRACT. The guitar ray Rhinobatos leucorhynchus is commonly caught as by-catch of industrial and
artisanal shrimp trawling in the shallow waters of the Colombian Pacific. The biological aspects of this species
were studied using 286 animals caught as by-catch between 2001 and 2007. The females were proportionally
larger than males, although growth was similar (allometric) for both sexes. The embryos showed no significant
differences by sex in either size or weight. The adult sex ratio was 2.4:1 (females-males), whereas in embryos
this ratio was 1:1. 51.5% of males, 51.5% had developed, calcified claspers, and 56.5% of females were
pregnant, carrying between 1 and 6 embryos of 3 to 19.5 cm, suggesting a size at birth of 19 to 19.5 cm TL.
The median size at maturity for females was lower than that of males (48.48 cm and 51.18 cm TL,
respectively), and the females had embryos starting at 44 cm TL. The feeding habits of this species showed 30
prey items, with shrimp from the Penaeidae family and especially Trachypenaeus sp. as main food. The diets
of male and female guitar rays differed significantly, and the niche breadth indicated that this species has a
specialist diet. The results of this study provide useful information for proposing management measures for R.
leucorhynchus, a species that requires attention given its biological characteristics and its importance in terms
of commerce and human consumption.
Keywords: batoids, reproduction, growth, diet, feeding ecology.

___________________
Corresponding author: Paola Andrea Meja-Falla (pmejia@squalus.org)
287 Biologa de Rhinobatos leucorhynchus en el Pacfico colombiano
INTRODUCCIN
Las rayas de la familia Rhinobatidae, conocidas
mundialmente como rayas guitarra y a nivel local
como guitarrillas, se agrupan en cuatro gneros, tres
subgneros y al menos 48 especies, y estn
distribuidas en todos los mares tropicales y templados,
desde aguas costeras y someras a profundidades hasta
de 370 m (Compagno, 2005). En el Pacfico Oriental
Tropical (POT) se encuentran los gneros Zapteryx y
Rhinobatos con dos y cinco especies, respectivamente,
siendo todas endmicas de esta regin (Robertson &
Allen, 2008). Para el Pacfico colombiano se ha
confirmado la presencia de Z. xyster, R.
leucorhynchus, R. planiceps, R. prahli, quedando por
confirmar la presencia de Z. exasperata y R.
glaucostigmus (Meja-Falla et al., 2007).
La familia Rhinobatidae, y en especial el gnero
Rhinobatos, hace parte importante de la captura
incidental de numerosas pesqueras en el mundo
(Stobutzki et al., 2002; Klippel et al., 2005) lo que,
junto a otras amenazas como la degradacin de
hbitats y el comercio de sus aletas dorsales (Fowler et
al., 2005), ha llevado a que 37 de las 48 especies estn
incluidas en la Lista Roja de Especies Amenazadas de
la IUCN, siendo 10 de stas categorizadas como
vulnerables o amenazadas y una como crticamente
amenazada (Rhinobatos horkelli) (IUCN, 2010).
Numerosos estudios sobre la historia de vida de
condrictios ubican a estas especies como estrategas k,
exhibiendo bajas tasas de crecimiento, maduracin
sexual tarda, bajas tasas de fecundidad y largos ciclos
de vida (Holden, 1974). Para el gnero Rhinobatos se
conocen pocos estudios en Amrica. Villavicencio-
Garayzar (1993) y Mrquez-Faras (2007) describen
que R. productus en el golfo de California alcanza la
madurez despus de los 50 cm longitud total (LT)
(machos a los 53 cm y hembras a los 57 cm LT), tiene
un largo periodo de gestacin (11 a 12 meses) y una
fecundidad promedio de cinco cras que nacen a los
17,5 cm LT. En Brasil, Lessa et al. (1986) y Texeira
(1982) proponen que las especies de Rhinobatos
presentan relacin directa entre la talla y la fecundidad
y diferenciacin sexual por talla. En el Caribe
colombiano, Grijalba-Bendeck et al. (2008) describen
la biologa reproductiva de R. percellens sealndola
como una especie matrotrfica con viviparidad
aplacentaria y fecundidad entre 2 y 4 embriones por
ao; y Polo-Silva & Grijalba-Bendeck (2008) la
ubican como un depredador con dieta preferencial de
crustceos.
R. leucorhynchus (Gnther, 1886) presenta dorso
de coloracin gris oscuro, algunas veces con manchas
plidas, hocico muy plido, translcido, sin punta
oscura y superficie inferior blanca. Esta especie habita
aguas tropicales costeras y estuarios de fondos suaves
y arenosos y est distribuida desde el golfo de
California a las islas Galpagos en Ecuador
(Robertson & Allen, 2008). En el Pacfico colombiano
esta especie es capturada regularmente como fauna
acompaante en faenas de pesca de camarn a nivel
artesanal e industrial (Navia, 2002; Gmez & Meja-
Falla, 2008); y aunque no presenta un alto valor
comercial, su carne es vendida a nivel local y las
aletas dorsales de los ejemplares ms grandes son
comercializadas (Navia et al., 2008). Aunque no
existe una pesca dirigida hacia la especie, su presencia
en hbitats estuarinos cercanos a la costa y aguas
someras, la hacen vulnerable a la pesca de arrastre
practicada en estas zonas.
Navia et al. (2009) plantean que el conocimiento
sobre R. leucorhynchus en Colombia se limita a pocos
registros de su distribucin latitudinal y batimtrica
(Navia, 2002; Payn, 2006), un estudio sobre sus
relaciones trficas con otras especies simptricas de
elasmobranquios (Navia et al., 2007) y a un estudio
preliminar para la determinacin de edad (Soler,
2006). Con este trabajo, cuyo objetivo fue estudiar la
biologa de la raya guitarra R. leucorhynchus, en
trminos de su crecimiento, reproduccin y
alimentacin, se incrementa el conocimiento sobre sus
caractersticas de historia de vida y se aporta
informacin til para futuras medidas de manejo y
conservacin de la especie.
MATERIALES Y MTODOS
Entre los aos 2001 y 2007, se capturaron ejemplares
de R. leucorhynchus en monitoreos a bordo de embar-
caciones de pesca industrial de camarn, en la zona
central de pesca del Pacfico colombiano (505N,
7716W-231N, 7835W). Los ejemplares fueron
congelados y trasladados al laboratorio para su
anlisis. Se registr el peso total (W), longitud total
(LT) y sexo de cada ejemplar. El estmago y las
gnadas fueron removidos de la cavidad corporal,
identificando, en este ltimo caso y de manera
macroscpica, el estado de madurez siguiendo las
escalas de Martin & Cailliet (1988) y Snelson et al.
(1988). Las cras encontradas fueron medidas (LT),
pesadas y sexadas y los huevos fueron contados y
medidos (dimetro en cm).
Las relaciones entre W (g) y LT (cm) fueron
estimadas para machos y hembras (en embriones y en
individuos libres) siguiendo el modelo W = a x LTb,
donde a y b son constantes. El tipo de desarrollo fue
definido a partir de la pendiente de la relacin de los
logaritmos de LT y W mediante una prueba t-Student,
 Lat. Am. J. Aquat. Res. 288

probando si es isomtrico (b = 3) o alomtrico (b 3) RESULTADOS

(Pauly, 1983). La similitud de esta relacin entre
machos y hembras fue evaluada mediante la Crecimiento
comparacin de los coeficientes de determinacin de Las hembras se capturaron en tallas entre 20,0 y 76,0
cada sexo (Zar, 1999). cm LT (59,21 10,56) y los machos entre 22,5 y 64,3
La proporcin de sexos fue determinada para cm LT (49,12 9,86), encontrando dimorfismo sexual
adultos y embriones usando una prueba de Chi- en la longitud total (nH = 201, nM = 85, g.l. = 2,81, t =
cuadrado con los valores observados y esperados (0,5) 7,43; P < 0,001). Sin embargo, ambos sexos
de machos y hembras. La longitud de primera presentaron un crecimiento similar, siendo alomtrico
madurez de machos fue determinada por el cambio de en ambos casos (bHembras= 3,24, bMachos= 3,30,
pendiente en la relacin de la longitud del clasper en tc-Hembras= 2,976, tc-Machos= 2,207; P < 0,05) y ligera,
funcin de la LT. Se evalu la existencia de
ms no significativamente, menor en las hembras (P =
dependencia de la fecundidad con la talla de la madre,
0,729) (Fig. 1).
a partir de la relacin de la LT con el nmero de
huevos y el nmero de cras. La talla mediana de Las cras (n = 101) se encontraron en diversos
madurez se estim para ambos sexos con una funcin estadios de crecimiento intrauterino, con tallas entre
logstica de la forma PLi=1/(1+e-b(Li+L50)), donde PLi es 3,0 y 19,5 cm LT (12,53 5,10) y pesos entre 0,2 y
la proporcin de individuos maduros en el intervalo de 24,2 g (9,19 8,22). Las diferencias sexuales en tallas
tallas Li, b es la pendiente y L50 es la talla a la cual el y pesos de las cras no fueron significativas (Tabla 1)
50% de los individuos estn maduros; este modelo fue y su desarrollo a nivel intrauterino fue similar entre
fijado usando regresin no lineal de mnimos machos y hembras, presentando ambos sexos una
cuadrados (Haddon, 2001). relacin longitud total-peso casi idntica (P > 0,05)
Los contenidos estomacales fueron identificados al (Fig. 2).
nivel taxonmico ms bajo posible y cada grupo de
presas fue contado y pesado con 0,01 g de precisin. Proporcin de sexos
Para determinar si el tamao de la muestra fue
Se analiz un total de 286 individuos adultos (201
suficiente para describir con precisin la dieta se us
hembras y 85 machos), hallando una proporcin de
la medida de diversidad trfica acumulada o curva de
acumulacin de especies (Ferry & Cailliet, 1996); para sexos dominada por hembras de 2,4:1 (2c = 47,05; g.l.
reducir el sesgo del orden de las muestras, se = 1; P < 0,001). Por su parte, los embriones cuyo sexo
realizaron 50 aleatorizaciones y para verificar la pudo ser determinado (35 hembras y 46 machos)
confiabilidad de la curva obtenida, se utilizaron los presentaron una proporcin sexual de 1:1 (2c = 1,49;
estimadores de riqueza de especies Chao e ICE g.l. = 1; P < 0,001), mostrando similitud en el aporte
(Colwell, 2005). La contribucin de cada tem de de ambos sexos a la poblacin.
presa a la dieta fue estimada usando tres ndices
numricos discutidos y revisados por Hyslop (1980) y
Corts (1997). El valor obtenido del ndice de
Importancia Relativa (IIR) se estandariz a porcentaje
(%IIR) para facilitar la comparacin entre tipos de
presas de una misma especie y entre dietas de
diferentes especies (Corts, 1997). Para probar la
independencia entre las categoras de alimento y sexo
se realizaron tablas de contingencia (columnas x filas)
(Zar, 1999), con contenidos estomacales agrupados en
siete categoras grandes y expresados como ocurrencia
(Corts, 1997). Anlisis de cambios ontognicos no
fueron realizados, dado el escaso nmero de
estmagos de individuos juveniles. Para determinar la
especializacin en la dieta se us la amplitud de nicho,
siguiendo la medida estandarizada de Levins (Ba)
(Krebs, 1999) y aplicando el %IIR (transformado a
proporcin) de las diferentes presas identificadas; este Figura 1. Relacin entre la longitud total y el peso total
ndice vara en un rango de 0 a 1, donde valores de machos y hembras de R. leucorhynchus.
cercanos a 0 indican una dieta especializada y Figure 1. Relationship between the total length and total
cercanos a 1 expresan dieta generalista (Krebs, 1999). weight of males and females of R. leucorhynchus.
289 Biologa de Rhinobatos leucorhynchus en el Pacfico colombiano

Tabla 1. Valores de la media y desviacin estndar de la longitud total (cm) y peso (g) de las cras de R. leucorhynchus,
indicando los valores de la prueba t entre sexos.
Table 1. Mean and standard deviation values of the total length (cm) and weight (g) of embryos of R. leucorhynchus,
indicating the t-test values between sexes.

Hembras (n = 35) Machos (n = 46) Valor t g.l. P

Longitud total 12,76 4.92 14,40 4.33 -1,562 79 0,122
Peso total 9,70 8.89 11,76 7.72 -0,983 79 0,329

que estaban maduros. La relacin entre la longitud

Figura 2. Relacin entre la longitud total y el peso total
en embriones de R. leucorhynchus.
Figure 2. Relationship between the total length and total
weight of embryos of R. leucorhynchus.
total (LT) y la longitud del clasper mostr un
crecimiento rpido entre los 42 y 50 cm LT, con punto
de inflexin en 47 cm (Fig. 4); el macho ms pequeo
con indicios de madurez fue de 42 cm LT,
correspondientes a los 62,1% de la longitud asinttica
calculada para machos en este estudio (67,68 cm LT).
La mayora de las hembras capturadas (86,0%)
estaban maduras, de las cuales el 56,5% present cras
en sus teros (estado 4) y el 26,3% huevos en sus
ovarios pero no cras (estado 3). La talla mnima de
madurez se registr a 44 cm LT, correspondiente al
55,0% de la longitud asinttica calculada para
hembras en este estudio (80,0 cm LT).
La talla mediana de madurez de las hembras fue de
48,5 cm LT, mientras que la de machos fue mayor
(51,2 cm LT) (Fig. 5). Estas tallas corresponden al
60,6% y al 75,6% de las longitudes asintticas
calculadas en el estudio, respectivamente.

Fecundidad
Rhinobatos leucorhynchus mostr funcionalidad en
sus dos ovarios, con fecundidad ovrica entre 1 y 16
huevos (5,61 2,87) que variaron entre 0,4 y 3,4 cm
de dimetro (1,86 0,64; n = 183). La fecundidad
uterina vari de 1 a 6 (3,45 1,15) con mayor
frecuencia (moda) en 4 embriones. Los resultados
encontrados sugieren que la fecundidad (ovrica y
uterina) de la raya guitarra es dependiente de la talla
materna, donde las hembras ms grandes presentaron
mayor cantidad de huevos y embriones (Fig. 3). El
tamao de cras y huevos mostr una relacin directa
durante la etapa de gestacin, observndose que a
medida que los embriones crecen, los huevos tambin
lo hacen. Finalmente, embriones con tallas cercanas a
19 cm LT, presentaron un desarrollo casi completo y
un saco vitelino muy pequeo. Figura 3. Relacin entre la longitud total de la madre
con el nmero de cras y huevos, indicando dependencia
Estados de madurez para hembras y machos de la fecundidad con la talla materna.
Al evaluar el estado de madurez de los machos se Figure 3. Relationship between the total length of
encontr que el 51,5% present los claspers females and the number of their embryos and eggs,
completamente desarrollados y calcificados indicando indicating dependence of fecundity with maternal length.
 Lat. Am. J. Aquat. Res.
Figura 4. Relacin entre la longitud total y la longitud
del clasper de machos de R. leucorhynchus.
Figure 4. Relationship between the total length and
clasper length of R. leucorhynchus males.
Figura 5. Ojivas de madurez sexual en machos y
hembras de R. leucorhynchus.
Figure 5. Sexual maturity ogives for males and females
of R. leucorhynchus.
Dieta
Se analizaron los contenidos estomacales de 211
ejemplares (147 hembras y 64 machos) donde se
encontraron 30 tems presa y un coeficiente de
vacuidad de 18,0%. La curva de acumulacin de
presas y sus respectivos estimadores indicaron que la
muestra fue suficiente para la descripcin de la dieta
de la especie, cubriendo ms del 91,7 % del total de
presas esperadas para una muestra de este tamao
(Fig. 6). De todas las presas identificadas, los
camarones, especialmente Trachypenaeus sp. fueron
los de mayor importancia en la dieta de la especie
(%IIR = 52,0) (Tabla. 2). La dieta de R. leucorhynchus
es heterognea, con dos tems presa (Trachypenaeus
sp. y Penaeidae) dominantes en nmero, ocurrencia y
290
Figura 6. Curva de acumulacin de especies para la dieta
de Rhinobatos leucorhynchus y sus respectivos esti-
madores.
Figure 6. Species accumulation curve for the Rhinobatos
leucorhynchus diet and its respective estimates.
peso, seguidos por crustceos, camarones no
identificados y peces (Fig. 7). La amplitud de nicho
calculada para R. leucorhynchus fue de 0,06,
indicando que es especialista en su dieta, con las dos
presas principales mencionadas.
Se encontr diferencia significativa entre la dieta
(agrupada) de machos y hembras de R. leucorhynchus
(2 = 13,288; g.l. = 6; P = 0,038), existiendo diferencia
en el mayor nmero de presas identificadas en las
hembras (7) y en el mayor consumo de peces. Por su
parte, los machos consumen menos presas (5), pero en
mayor proporcin crustceos y estomatpodos.
DISCUSIN
Los ejemplares de raya guitarra colectados en el rea
de estudio presentaron mayores tallas que las
reportadas por McEachran & di Sciara (1995) (62,5
cm LT) y por Robertson & Allen (2008) (63 cm LT)
para el Pacfico Oriental Tropical, siendo esta
diferencia mayor en hembras (76,0 cm LT) que en
machos (64,3 cm LT). Aunque la relacin entre
longitud total y peso no mostr diferencias
significativas entre hembras y machos, estos ltimos
son ligeramente ms pequeos que las hembras y
presentan un menor peso corporal en tallas similares.
Diferencias similares aunque significativas, han sido
reportadas para R. horkelli (Texeira, 1982), R.
productus (Villavicencio-Garayzar, 1995) y R.
cemiculus (Seck et al., 2004). A nivel embrionario, las
curvas de la relacin longitud total-peso de machos y
hembras fueron casi idnticas, presentando ambos
sexos un crecimiento similar. De esta forma, ambos
291 Biologa de Rhinobatos leucorhynchus en el Pacfico colombiano

Tabla 2. Valores de porcentaje de ocurrencia (%O), porcentaje en nmero (%N), porcentaje en peso (%W), ndice de
importancia relativa (IIR) y porcentaje de ndice de importancia relativa (%IIR) de las presas consumidas por Rhinobatos
leucorhynchus.
Table 2. Values of frequency of occurrence (%O), percentage by number (% N), percentage by weight (%W), index of
relative importance (IIR) and percentage of the index of relative importance (%IIR) of prey consumed by Rhinobatos
leucorhynchus.

Presa %O %N %W IIR %IIR

Trachypenaeus sp. 28,44 33,43 21,30 1556,32 51,98
Penaeidae 18,96 18,81 24,93 829,20 27,69
Crustceos 9,95 12,45 5,72 180,75 6,04
Camarones 8,06 11,29 5,87 138,22 4,62
Peces 9,95 3,62 10,13 136,80 4,57
Porichthys margaritatus 3,79 1,59 9,72 42,90 1,43
Callinectes sp. 4,27 1,88 5,14 29,96 1,00
Portunidae 5,21 2,32 1,84 21,68 0,72
Sicyonia sp. 3,32 1,45 1,57 10,01 0,33
Cangrejos 3,32 1,74 0,89 8,71 0,29
Stomatopoda 1,42 0,43 5,60 8,57 0,29
Batrachoididae 3,32 1,16 0,64 5,96 0.20
Squillidae 2,84 1,30 0,28 4,50 0,15
Raninoides benedicti 2,37 0,87 0,91 4,22 0,14
Trachypenaeus byrdi 1,90 0,87 0,73 3,04 0,10
Squilla sp. 1,42 1,16 0,63 2,55 0,09
Callinectes toxotes 1,90 0,58 0,61 2,25 0,08
Portunus sp. 1,90 1,01 0,09 2,09 0,07
Trachypenaeus brevisuturae 0,95 0,29 1,09 1,31 0,04
Trachypenaeus fuscina 0.95 0,43 0,68 106 0,04
Anomura 1,42 0,43 0,09 0,74 0,02
Processa sp. 1,42 0,43 0,08 0,73 0,02
Sicyonia disdorsalis 0,95 0,29 0,30 0,56 0,02
Meiosquilla swetti 0,95 0,43 0,13 0,53 0,02
Brachyura 0,95 0,43 0,10 0,51 0,02
Squilla parva 0,47 0,43 0,51 0,45 0,01
Solenoceridae 0,47 0,29 0,15 0,21 0,01
Solenocera agassizzi 0,47 0,14 0,23 0,18 0,01
Donacidae 0,47 0,29 0,03 0,15 0,00
Leucosiidae 0,47 0,14 0,03 0,08 0,00
TOTAL 122,27 100,00 100,00 2994,22 100,00

sexos presentan crecimientos similares durante su
desarrollo (tanto intrauterino como externo), pero
presiones intrnsecas a las hembras (p.e. su viviparidad
aplacentaria) provocan ligeros cambios, siendo ms
marcada esta diferencia en la talla mxima alcanzada
por ambos sexos.
La proporcin de sexos mostr diferencias
significativas siendo 2,4:1 favorable para las hembras,
estableciendo una posible segregacin por sexos, tal
como se ha planteado para varias especies de rayas
(p.e. Braccini & Chiaramonte, 2002; Ebert et al.,
2008). Adicionalmente, la muestra colectada para este
estudio no present individuos juveniles y la mayora
de las hembras y machos estaban maduros; as, se
puede sugerir que la zona donde se realizan los
arrastres de camarn industrial, presenta una alta
actividad reproductiva, con segregacin por tallas y
sexos. Sin embargo, considerando la proporcin
sexual encontrada en embriones (1:1), se propone que
el aporte a la poblacin de hembras y machos es
similar, pero luego del parto y durante el desarrollo de
los individuos, se inicia un proceso de segregacin
 Lat. Am. J. Aquat. Res.
Figura 7. Representacin grfica del ndice de
importancia relativa (IIR) de las presas consumidas por
R. leucorhynchus, indicando aquellas de mayor
importancia.
Figure 7. Graphic representation of the relative
importance index (IIR) of prey consumed by R.
leucorhynchus, indicating those of greatest importance.
espacial en tallas y sexos. Se han encontrado
resultados similares en proporcin de embriones en R.
productus, R. hynnicephalus y R. rhinobatos
(Villavicencio-Garayzar, 1993, 1995; Webin &
Shuyuan, 1993; Cek et al., 2009).
La fecundidad uterina de R. leucorhynchus (entre 1
y 6 embriones) es menor a la de otras especies de la
misma familia, como R. productus (2-10) (Downton-
Hoffmann, 2001; Mrquez-Faras, 2007) y Zapteryx
brevirostris (Abilhoa et al., 2007), pero ms alta que
la de R. cemiculus (2-4) (Valadou et al., 2006). As
mismo, la dependencia de la fecundidad con la talla
materna encontrada en la especie, ya ha sido registrada
en otras especies de Rhinobatos como R. horkelli, R.
annulatus, R. productus y R. hynnicephalus (Lessa et
al., 1986; Villavicencio-Garayzar, 1993; Webin &
Shuyuan, 1993; Mrquez-Faras, 2007; Kume et al.,
2009).
Los embriones con tallas cercanas a los 19 cm LT,
presentaron un desarrollo casi completo y un saco
vitelino muy pequeo; as, y considerando que la
menor talla conocida para un organismo de vida libre
es de 19 cm LT (Gmez & Meja-Falla, 2008) y el
embrin intrauterino ms grande encontrado en este
estudio fue de 19,5 cm LT, se considera la talla de
292
nacimiento entre estos valores (19,0 y 19,5 cm LT).
Esta talla es similar a la reportada por Villavicencio-
Garayzar (1993) y Downton-Hoffmann (2001) para R.
productus en el Pacfico Mexicano, pero es menor a lo
registrado por Abdel-Aziz et al. (1993), Capap et al.
(1997, 1999) e Ismen et al. (2007) para R. rhinobatos
en el Mediterrneo y el Atlntico este tropical.
La falta de datos a lo largo del ao no permiti
definir el ciclo reproductivo de la especie. Sin
embargo, la frecuencia de tallas de los embriones
permite considerar que cerca del mes de agosto, las
hembras pueden empezar a parir sus cras, tal como ha
sido reportado para R. hynnicephalus en aguas
japonesas (Kume et al., 2009).
La relacin directa entre el tamao de los huevos y
de los embriones, puede indicar que, simultneamente
al desarrollo embrionario se presenta el desarrollo
ovrico. Esto sugiere que, una vez los embriones son
expulsados, las hembras pueden recomenzar el ciclo
reproductivo. Esta posible estrategia reproductiva se
ajusta a la descrita para otras especies del mismo
gnero como R. horkelli, R. annulatus, R. productus y
R. cemiculus en las que para un mismo periodo de
tiempo, de manera simultnea al desarrollo
embrionario crecen los ovocitos de la siguiente
progenie, los cuales son fecundados en los das
siguientes a la expulsin de los neonatos
(Villavicencio-Garayzar, 1995; Valadou et al., 2006;
Kume et al., 2009). Esto explica adems la presencia
de embriones en etapas iniciales (3 cm LT) y finales
(19 cm LT) del desarrollo embrionario en un mismo
mes (p.e. agosto).
Ms del 90% de las hembras estaban maduras, por
lo que se infiere que el periodo entre junio y
septiembre es poca reproductiva para la raya guitarra.
Aunque no se encontraron machos con semen, ms del
60% estaban maduros, basado en la longitud, el grado
de calcificacin y rotacin de los claspers tal como
plantean Joung & Chen (1995). En cortes histolgicos
realizados a machos maduros de la especie (Payn,
2006), se observ que las clulas reproductivas
presentaban diferentes estados de madurez, mostrando
porcentajes similares entre clulas maduras
(espermatozoides) y clulas inmaduras (esperma-
togonias y espermtidas). De acuerdo con la poca
reproductiva en la cual fueron tomadas las muestras,
se pueden sugerir dos posibilidades, que los machos
ya se hubieran apareado y por lo tanto habran
descargado todo el semen, o por otra parte, que
estuvieran en una etapa previa al apareamiento en la
cual sus conductos se estuvieran cargando.
La talla mediana de madurez sexual de hembras
fue de 48,5 cm LT y de machos de 51,2 cm LT,
293 Biologa de Rhinobatos leucorhynchus en el Pacfico colombiano
mientras que la talla promedio de captura fue de 59,2
y 49,1 cm LT, respectivamente, por lo tanto, se infiere
que la mayora de los individuos capturados ya han
tenido la oportunidad de reproducirse anteriormente.
La talla mnima de madurez es similar para ambos
sexos (42 y 44 cm LT, para machos y hembras,
respectivamente). Sin embargo, dado que las hembras
alcanzan mayores tallas, el porcentaje en que alcanzan
esa talla si difiere entre machos y hembras (62,1% y
55,0%, respectivamente), y al igual que lo reportado
por Kume et al. (2009), las hembras alcanzan la talla
de madurez en tallas ms grandes que los machos.
La curva de acumulacin de presas construida para
R. leucorhynchus indic que el tamao de muestra fue
adecuado para hacer una descripcin de su dieta en el
rea de estudio. Esta especie es especialista en su dieta
consumiendo mayoritariamente camarones, en
especial de la familia Penaeidae y del gnero
Trachypenaeus. Estos resultados concuerdan con lo
reportado para otras especies del gnero en frica, el
Mediterrneo, California y Brasil (Caverivier &
Rabarison-Andriamirado, 1997; Goitein et al., 1998;
Shibuya et al., 2005; Basusta et al., 2007; Ismen et al.,
2007). Aparentemente R. leucorhynchus, al igual que
las otras especies de su gnero, no est adaptada para
perseguir activamente peces de media agua (Talent,
1982). Por el contrario, extrae su alimento de los
fondos areno-fangosos donde habita, llevando a que su
alimentacin est basada principalmente en
organismos de vida bentnica como los encontrados
en este estudio. Lo anterior ha llevado a que algunas
especies como R. annulatus sean consideradas las
principales depredadoras de ambientes bentnicos en
localidades particulares (Harris et al., 1988).
Los tems presa encontrados para R. leucorhynchus
concuerdan con lo descrito por Robertson & Allen
(2008), quienes plantean que los peces guitarra se
alimentan de invertebrados bentnicos y de peces
pequeos. Basusta et al. (2007) reportan que R.
rhinobatos ingiere peces como el segundo alimento en
importancia mientras que esta presa fue de menor
importancia para R. leucorhynchus, lo que puede
explicarse por el gran tamao de la primera (LTmax =
147 cm) con relacin a la especie en estudio (LTmax =
76,0 cm).
En el presente estudio se encontraron diferencias
significativas en el consumo de presas de machos y
hembras, siendo los peces consumidos en mayor
proporcin por hembras y los crustceos y
estomatpodos por machos, lo que muestra un uso
diferencial en la dieta. Diferencias trficas intra-
especficas ya han sido documentadas en varias
especies de batoideos (Kyne & Bennett, 2002; Morato
et al., 2003; Scenna et al., 2006) y se atribuyen
especialmente a cambios en las estructuras dentales
entre los sexos.
La ausencia de ejemplares juveniles en la muestra
sugiere una separacin espacial entre los diferentes
estados ontognicos, por lo cual los neonatos y
juveniles no ocurren en los mismos sitios de captura
de los adultos, y s lo hacen probablemente en zonas
ms cercanas a la costa. Los estados tempranos
tienden a concentrarse en sectores poco profundos de
gran productividad y abundante alimento, como por
ejemplo, aguas someras, planicies submareales
costeras y estuarios (Bass, 1978; Castro, 1987).
AGRADECIMIENTOS
Los autores agradecen a los pescadores artesanales e
industriales de Buenaventura que aportaron las
muestras para efectuar este trabajo; a Don Agustn
Martnez, por facilitar los embarques en el barco
camaronero Arraijn; a Henry Lpez por facilitar el
trabajo de muestras en el Puerto; a la Universidad del
Valle y la Fundacin SQUALUS por el apoyo
logstico; a IdeaWild por la donacin de equipos para
trabajo de campo y de laboratorio, a los miembros de
la Fundacin SQUALUS Jos Sergio Hleap y
Alexnder Tobn por el apoyo a bordo, y a Juliana
Lpez por el apoyo en el anlisis de muestras en
campo y en laboratorio.
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Lat. Am. J. Aquat. Res., 39(2): 297-305, 2011 Age and growth of brazilian flathead 297
DOI: 10.3856/vol39-issue2-fulltext-11

Research Article

Age determination, validation, and growth of Brazilian flathead

(Percophis brasiliensis) from the southwest Atlantic coastal waters (34-41S)

Alfredo C. Barretto1, Margarita B. Sez2, Mara R. Rico2 & Andrs J. Jaureguizar2,3

1
Departamento de Biodiversidad y Biologa Experimental, Facultad de Ciencias Exactas y Naturales
Universidad de Buenos Aires (UBA), Ciudad Universitaria Pabelln 2, 1428, Buenos Aires, Argentina
2
Instituto Nacional de Investigacin y Desarrollo Pesquero (INIDEP)
P.O. Box 175, 7600 Mar del Plata, Argentina
3
Comisin de Investigaciones Cientficas de la Provincia de Buenos Aires
Calle 526 entre 10 y 11, 1900 La Plata, Argentina

ABSTRACT. The age and growth parameters of Brazilian flathead, Percophis brasiliensis, from the
southwest Atlantic coastal waters (34-41S) were determined for samples collected in spring (n = 853; years
1998 and 2000) and winter (n = 596; year 2004), whereas age was validated through the edge analysis of
otoliths collected in 2007 (n = 1367 otoliths). The indices of precision APE, V, and D were used to test the
reproducibility, between agers, of the ages determined from 845 otoliths. Maximum determined ages were 19
years for males and 15 years for females. One opaque and one translucent band are laid down per year, in the
sagittal otolith. According to the APE (0.668%), V (1.121%), and D (0.647%) indices, the age determination
was consistent. Von Bertalanffys growth parameters [males: spring (L = 58.1 cm, k = 0.26 year-1, t0 = -2.02
years), winter (L = 58.7 cm, k = 0.21 year-1, t0 = -2.90 years); females: spring (L = 65.2 cm, k = 0.29 year-1,
t0 = -1.15 years), winter (L = 63.5 cm, k = 0.26 year-1, t0 = -2.01 years)] were significantly different between
sexes and seasons. From the first year of life, females grow faster and reach greater lengths than males of the
same age due, probably, to an asynchronism in the sexual maturity.
Keywords: Brazilian flathead, Percophis brasiliensis, age determination, otolith, validation, growth, south-
west Atlantic.

Determinacin de edad, validacin y crecimiento del pez palo

(Percophis brasiliensis) de aguas costeras del Atlntico sudoccidental (34-41S)

RESUMEN. Se determin la edad y los parmetros de crecimiento del pez palo, Percophis brasiliensis, de
aguas costeras del Atlntico sudoccidental (34-41S) en muestras obtenidas durante primavera (n = 853; aos
1998 y 2000) e invierno (n = 596; ao 2004), mientras que la edad fue validada mediante anlisis del tipo de
borde de otolitos colectados durante 2007 (n = 1367 otoliths). Los ndices de precisin APE, V, y D fueron
usados para probar la reproducibilidad, entre lectores, de las edades determinadas a partir de 845 otolitos. Las
edades mximas determinadas fueron 19 aos para machos y 15 aos para hembras. Una banda opaca y una
translcida se depositan anualmente en el otolito sagitta. Los ndices APE (0,668%), V (1,121%) y D
(0,647%) indican que la determinacin de la edad fue consistente. Los parmetros de crecimiento de Von
Bertalanffy [machos: primavera (L = 58,1 cm, k = 0,26 ao-1, t0 = -2,02 aos); invierno (L = 58,7 cm, k =
0,21 ao-1, t0 = -2,90 aos). hembras: primavera (L = 65,2 cm, k = 0,29 ao-1, t0 = -1,15 aos); invierno
(L = 63,5 cm, k = 0,26 ao-1, t0 = -2,01 aos)] fueron significativamente diferentes entre sexos y estaciones. A
partir del primer ao de vida, las hembras crecen ms rpido y alcanzan mayores longitudes que los machos de
la misma edad debido, probablemente, a un asincronismo en la madurez sexual.
Palabras clave: pez palo, Percophis brasiliensis, determinacin de edad, otolito, validacin, crecimiento,
Atlntico sudoccidental.

___________________
Corresponding author: Andres J. Jaureguizar (ajj@inidep.edu.ar)
298 Lat. Am. J. Aquat. Res.
INTRODUCTION
The Brazilian flathead Percophis brasiliensis (Quoy &
Gaimard) is a demersal fish species (Olivier et al.,
1968) that inhabits southwest Atlantic coastal waters.
Its distribution extends from 23S (Rio de Janeiro,
Brazil) to 47S (north of Santa Cruz Province,
Argentina) (Gosztonyi, 1981; Cousseau & Perrotta,
2004). In the southern area of its distribution (34-
41S), it is one of the most important species caught
by the coastal commercial fishery (Lasta et al., 1999;
Carozza et al., 2001; Fernndez-Aroz et al., 2004).
Despite the importance of this species and the
increasing captures that have been detected during the
last years (Rico & Perrotta, 2009), few studies have
been focused to obtain relevant biological information
for its fisheries management. There are information
about feeding (San Romn, 1972; Bergonzi, 1997),
growth (Tomo, 1969; San Romn, 1974; Perrotta &
Fernndez-Gimnez, 1996), distribution (Fernndez-
Gimnez, 1995; Rico & Perrotta, 2006) and
reproduction (Macchi & Acha, 1998; Militelli, 1999;
Militelli & Macchi, 2001; Rodrgues et al., 2007). For
successful fisheries management is very important to
evaluate the fish population state. Studies on age
determination and growth parameters estimation,
amongst others, are fundamental to knowledge of
population dynamics (Sparre & Venema, 1995; Cotter
et al., 2004; Dulvy et al., 2004; Begg et al., 2005).
The age and growth parameters of Brazilian
flathead have been determined through the counting of
the otolith rings (Tomo, 1969; San Romn, 1974;
Perrotta & Fernndez-Gimnez, 1996). However,
none of these authors reported the growth parameters
of each sex nor validated the determined ages. In
marine teleost fishes it is assumed that growth
increments are laid down annually on hard parts, such
as scales or otoliths, and the age is determined by
counting the rings that are present in these hard
structures (Jones, 1992; Campana & Thorrold, 2001).
Errors in the assignment of age may contribute to
overexploitation of a stock or species, often through
underestimating true age and producing optimistic
estimates of growth and mortality rates. Consequently,
validation of age readings is a requirement for manage
stocks, particularly for those being assessed by means
of age-structured models (Campana, 2001; Begg et al.,
2005).
Therefore, the aims of this study were determine
the age of males and females of Brazilian flathead,
validate it, obtain the growth parameters of each sex
(in spring and winter) and compare it statistically
(between sexes, in each season; and between season,
for each sex). The seasonal migration of Brazilian
flathead, associated to its reproduction activity in the
salinity front located within the southwest Atlantic
coastal water (34-41S) (Macchi & Acha, 1998;
Militelli & Macchi, 2001), could allow differences in
the estimated growth parameters. Detect, therefore,
these differences is important at the time of using age-
length keys for transforming length data in age data.
This study represents the first attempt to validate
Brazilian flatheads age determination and to estimate
the growth parameter of each sex by season.
MATERIALS AND METHODS
Age determination
Samples were collected from southwest Atlantic costal
waters (34-41S) by bottom trawling in waters from 7
to 50 m depth (Fig. 1), during INIDEP cruises carried
out in spring (1998, 2000) and winter (2004). Age was
determined to 1449 specimens, 853 in spring (439
males, 414 females) and 596 in winter (251 males, 345
females). Of each specimen total length (TL) and sex
(by macroscopic examination of the gonads) were
recorded, while sagittal otoliths were removed from
the fish and stored dry in paper envelopes for age
determination. Randomly, one sagittal otolith from the
pair was embedded in opaque epoxy resin and
sectioned transversely through the core with a micro-
cutter (Maruto MC-201) obtaining thus thin transverse
sections of 0.5 mm in thickness. The opaque bands of
these sections were counted by two independent
readers under incident and transmitted light using a
stereomicroscope at 40X magnification. Age was
determined to the nearest lower without knowledge of
the length and sex of the specimen. If the two
independent readings differed, then the otolith was
considered unreadable. We used the average percent
error (APE), the coefficient of variation (V) and the
index of precision (D) (Beamish & Fournier, 1981;
Chang 1982) to test the reproducibility between agers
of the ageing process, from 845 otoliths (620 spring,
225 winter).
Age validation
The validation of the annual formation of opaque
bands was established by examining the monthly
proportions of opaque or translucent edges (Dannevig,
1933) throughout a year. Monthly samples (1367
otoliths) from commercial fisheries in the same area,
from January to December 2007, were use to validate
the age.
Growth
The Von Bertalanffy growth model (1938) was fitted,
in each season, to observed length-at-age data of
 Age and growth of brazilian flathead
Figure 1. Study area showing their bathymetry (m) and the location of the sampling stations during spring () and winter
().
Figura 1. rea de estudio indicando la batimetra y localizacin de las estaciones de muestreo durante primavera () e
invierno ().
males and females by nonlinear regression TL = L (1
e k(t t0); where TL is the total length (cm) at
age t (years), L the mean maximum total length
(cm), k a growth rate parameter (year-1) and t0 the
theoretical age (years) at zero length. The likelihood
ratio test (LRT) was used to estimate the growth
parameters (L, k, t0) and to compare the growth
curves (Aubone & Whler, 2000). The approximate
growth parameter values required by LRT were
obtained following Gulland & Holts methodology
(1959) for L [male (spring = 57.6 cm, winter 63.5
cm), female (spring = 63.3 cm, winter 62.1 cm)] and
von Bertalanffys methodology (1934) for k [males
(spring = 0.28 year-1, winter = 0.21 year-1), female
(spring = 0.43 year-1; winter = 0.29 year-1)] and t0
[males (spring = -1.93 years; winter = -1.54 years),
female (spring = -0.04 years, winter = 1.79 years)]
(Sparre & Venema, 1995). These approximate values
were also used to evaluate the goodness of fit of
different growth models through the Quasi-Newton
Method (QNM) of the Statistica 6 Program. QNM
was also used to estimate the goodness of fit of the
selected growth model to the observed length-at-age
data. All statistical inferences were based considering
an alpha error level of 5% ( = 0.05).
299
RESULTS
Age determination
Of the 1467 otoliths that were examined, 1449 were
considered readable (98.8% of coincidence between
readers). The average percent error (APE = 0.668%),
the coefficient of variation (V = 1.121%) and the
index of precision (D = 0.647) indicate that the
determination of age was consistent. All the spring
otoliths sections showed opaque bands at the edge,
whereas the 99.2% of the winter otoliths showed a
translucent one. The first band next to the core was not
as well defined as the others and in the 95.4% of the
otoliths it was opaque. In some cases this band was
very much thicker (or very much thinner) than the
second opaque band, in other cases was composed of
1 to 3 opaque bands separated by much thinner
translucent bands, or was less visible than the other
opaque bands, or was present on one side of the
sulcus. This band was only considered if it was
present inside the sulcus.
The age and length ranges of each considered
group of Brazilian flathead specimens were: males
[spring (0-14 years), (24-61 cm); winter (0-19 years),
(26-63 cm)], females [spring (0-14 years), (20-67 cm);
winter (0-15 years), (23-73 cm)]. Both sexes showed,
300 Lat. Am. J. Aquat. Res.
in each season, unimodal age frequency distributions:
males showed a modal value of 2 years in both
seasons, whereas spring modal value of females (2
years) was smaller than the one of winter (4 years)
(Fig. 2).
Age validation
The monthly proportions of the sagittal otoliths edge
types showed that the opaque-band formation begins
in September and it remains present at the otolith edge
until February; from this month on, the translucent
band begins to lay down and it is present at the
otoliths edge until September, when the opaque-band
formation begins (Fig. 3). This beginning of the
opaque band formation is earlier in males than in
females. These results show that, annually, one
opaque and one translucent band are deposited at the
edge of the sagittal otoliths and, therefore, one opaque
plus one translucent band represents 1 year of the
fishs life.
Growth
The von Bertalanffy growth model showed a good fit
to the observed length-at-age data (Table 1): females
are larger than males of the same age from the first
year of life (Figs. 4a y 4b). At this age, both sexes
attain 50% of its maximum total length. Comparison
of growth parameters for both seasons showed
significant differences between sexes (LRT, P < 0.01).
Figure 2. Age frequency distributions of males (a) and
females (b) during spring () and winter ().
Figura 2. Distribuciones de frecuencia de edades de
machos (a) y hembras (b) durante primavera () e
invierno ().
Figure 3. Monthly frequency of the opaque and
translucent edges in the sagitta otolith of Percophis
brasiliensis males () and females () during 2007 and
the monthly sample size by sex. Transverse section of a
sagitta, at core level, of a 5 years old specimen collected
in winter.
Figura 3. Frecuencia mensual de bordes opacos y
translucidos en otolitos sagitta de Percophis brasiliensis
por sexo: machos () y hembras () durante el ao 2007 y
tamaos mustrales mensuales por sexo. Seccin
transversal de un sagitta, a nivel del ncleo, de un
espcimen de 5 aos de edad colectado en invierno.
Females grow faster and attain larger sizes than the
males [L (P < 0.01), k (P < 0.1), t0 (P < 0.01), in
spring; and L (P < 0.01), k (P < 0.05), t0 (P < 0.1), in
winter] (Figs. 4a-4b; Table 1). The difference between
ks of both sexes was marginally significant in spring
(P = 0.06).
Furthermore, significant differences in the
estimated growth parameters of each sex were
detected between seasons (LRT, P < 0.05 for males
and P < 0.01 for females) (Figs. 4c-4d). The males
showed marginally significant differences in k (P =
0.077) and t0 (P = 0.056), but did not differ in L (P >
0.5); whereas the females showed significant
differences in L (P < 0.01) and t0 (P < 0.01), but did
not differ in k (P > 0.05).
DISCUSSION
The high coincidence percentage among the two
independent readers as well as the values of the
precision indices indicate that the sagitta otolith of
Brazilian flathead is easy to read, as happens with
most of sagitta otoliths of template waters marine
fishes (Panella, 1974; Ricker, 1979; Sparre &
Venema, 1995). In spite of this, there were doubts
about considering or not the first opaque band next to
the core because it was not as well defined as the
others. Peres & Haimovici (2004), studying chernias
Polyprion americanus (Bloch & Schneider) otoliths,
 Age and growth of brazilian flathead 301

Table 1. Von Bertalanffys growth parameters (L, k, t0) of Percophis brasiliensis, determination coefficient (r2)
estimated through LRT and QNM respectively, and sample size (n).
Tabla 1. Parmetros de crecimiento de von Bertalanffy (L, k, t0) de Percophis brasiliensis, coeficiente de determinacin
(r2) estimado mediante de LRT y QNM respectivamente, y tamao muestral (n).

Males Females
Parameter
Spring Winter Spring Winter
L (cm) 58.1 58.7 65.2 63.5
k (year-1) 0.26 0.21 0.29 0.26
t0 (years) -2.02 -2.90 -1.15 -2.01
n 439 251 414 345
r2 0.82 0.66 0.84 0.67

Figure 4. Growth curves of both sexes ( males and females) of Percophis brasiliensis in a same season, a) spring and
b) winter, and of each sex c) males and d) females by season ( spring and winter). Observed mean total length-at-age
and fitted von Bertalanffy growth model (dash line, predicted total length values for ages out of observed range). Sample
sizes (n) of each comparison were: a) ( 439 and 414), b) ( 251 and 345), c) ( 439 and 251) and d) ( 414 and
345).
Figura 4. Curvas de crecimiento de ambos sexos ( machos y hembras) de Percophis brasiliensis en una misma
estacin, a) primavera y b) invierno), de cada sexo c) machos y d) hembras por estacin ( primavera y invierno).
Longitud total media por edad observada y modelo de crecimiento de von Bertalanffy ajustado (lnea discontinua, valores
de longitud totales predichos para edades fuera del rango observado). Tamaos muestrales (n) para cada comparacin: a)
( 439 y 414), b) ( 251 y 345), c) ( 439 y 251) y d) ( 414 y 345).

considered it as a false band, and named it central
area. However, the age determinations made to the
nearest inferior age are not modified by considering or
not this band. Future studies must be done to verify if
this first opaque band is true or not. The maximum
ages observed in this study (19 years for males and 15
for females) were higher than maximum ages
registered for the species [6 years, Tomo (1969); 7
years, San Romn (1974); 12 years, Perrotta &
Fernndez-Gimnez (1996)].
It was verified that only one opaque and one
translucent band are laid down annually in the sagittal
otoliths of Brazilian flathead, which appear between
September-February and during the rest of the year,
respectively. This result is consistent with previous
studies for other coastal species at the region e.g.
302 Lat. Am. J. Aquat. Res.
Micropogonias furnieri (Desmarest) (Cotrina, 1998),
Cynoscion guatucupa (Cuvier) (Castelli-Vieira &
Haimovici, 1993; Lpez-Cazorla, 2000) and Pogonias
cromis (Linnaeus) (Urteaga & Perrotta, 2001). The
opaque-band (fast growth) formation period coincides,
partially, with Brazilian flatheads reproductive
period. Males reproductive period (August-April) is
wider than the females (October-April) (Rodrgues,
2009). This difference could be responsible of the
earlier onset of males opaque-band formation.
The Von Bertalanffy growth model acceptably
described (r2 0.7) Brazilian flatheads growth, as
generally occurs when this model is fitted to length-at-
age data of adult specimens (Jones, 1992; Sparre &
Venema, 1995). The estimated L (`s: 58.1 and 58.7
cm; s: 65.2 and 63.5 cm) values were lower than the
values estimated previously by Tomo (1969) [L =
86.94 cm (pooled sexes); L = 84.70 cm (females)], by
San Romn (1974) [L = 86.2 cm (pooled sexes)], and
by Perrotta & Fernndez Gimnez (1996) [L = 68.39
cm (pooled sexes; northern study area); L = 70.78 cm
(pooled sexes; southern study area)] (Tables 1 and 2).
On the other hand, the estimated k values (`s: 0.26
and 0.21 year-1; s: 0.29 and 0.26 year-1) were higher
than those estimated by San Romn (1974) [k = 0.170
year-1 (pooled sexes)] and by Perrotta & Fernndez-
Gimnez (1996) [k = 0.186 year-1 (pooled sexes;
northern study area); k = 0.145 year-1 (pooled sexes;
southern study area)]; were also higher than those
estimated by Tomo (1969) [k = 0.210 year-1 (pooled
sexes); k = 0.220 year-1 (females)], with the exception
of the males k value of winter (k = 0.210 year-1)
which was similar to those values estimated by the
latter author (Tables 1 and 2).
The lower L values estimated in this study could
be a consequence of the greater number of > 9 years
Table 2. Percophis brasiliensiss growth parameters (L, k, and t0) obtained, from von Bertalanffys model, by previous
studies in the southwest Atlantic coastal water (34-41S).
Tabla 2. Parmetros de crecimiento de Percophis brasiliensis obtenidos (L, k, and t0), a partir del modelo de von
Bertalanffy, por estudios previos en aguas costeras del Atlntico sudoccidental (34-41S).
Sample
Reference
Area Season
Perrotta & Fernndez-Gimenz (1996) Northern Winter
SACS
Perrotta & Fernndez-Gimnez (1996) Southern Winter
SACS
San Romn (1974) Inside All year
SACS round
Tomo (1969) Inside Not
SACS available
Tomo (1969) Inside Not
SACS available
old specimens (age from which maximum total length
seems to be reached) and of the greater longevity of
them. In the case of k, differences could be
consequence of the greater number of < 3 years old
specimens and of its younger ages. The age and
growth determinations done indicate that Brazilian
flathead is a relatively long-lived, low-growing
species; as most of the demersal species of the South
Atlantic coastal water (34-41S) (Lasta et al., 2000),
like M. furnieri (Agemax = 39 years; kmax 0.20
year-1; Carozza et al., 2004), C. guatucupa (Agemax =
23 years; kmax 0.40 year-1; Ruarte et al., 2004),
Pagrus pagrus (Linnaeus) (Agemax = 16 years; kmax
0.15 year-1; Cotrina & Carozza, 2000) and P. cromis
(Agemax = 41 years; kmax 0.18 year-1; Urteaga &
Perrotta, 2001).
Brazilian flathead showed differential growth from
the first year of life (Figs. 4a-4b); in coincidence with
San Romn (1974) females are larger than males of
the same age. Considering the age determinations
done in this study and the length-at-maturity reported
by Militelli (1999), males first sexual maturity occurs
when they are 1 years old (TL50% = 29.24 cm), while
in females this happens when they are 2 years old
(TL50% = 38.71 cm). This asynchronism in the sexual
maturity could explain the differential growth
developed for each sex because, from this event, the
growth rate decreases markedly (Brett, 1979). The
earlier onset of males sexual maturity could be
responsible for both the earlier decrease of their
growth rate and, consequently, the lower total length
reached because, after this event, they ought to
channel surplus energy not only into growth, like
females do up to 2 years old, but also into reproduc-
tion. This sexual dimorphism in growth, with females
larger than males of the same age, is common in some
L k t0
Sex
Type (cm) (year-1) (years)
Research 68.39 0.186 -1.956
Research 70.78 0.145 -2.858
Commercial 86.20 0.170 0.270
Commercial 86.94 0.210 0.160
Commercial 84.70 0.220 0.035
 Age and growth of brazilian flathead
coastal species that inhabit the South Atlantic coastal
water (34-41S), like M. furnieri (Carozza et al.,
2004) and C. guatucupa (Ruarte et al., 2004).
Finally, differences in the growth parameters of
each sex were detected between seasons. The seasonal
differences in females growth parameters (L and t0)
would be associated to their age-structure seasonal
changes whereas the seasonal similarity in males age-
structure would explain the non-significant seasonal
differences of their parameters (L, k, t0) [Figs. 2 and
4c-4d]. These seasonal changes in the female structure
could be related to spring reproductive immigration of
older female to the spawning area. Within the South
Atlantic coastal water (34-41S) the reproductive
activity is associated to outer salinity front of the Rio
de la Plata and El Rincon (Macchi & Acha, 1998;
Militelli & Macchi, 2001; Rodrgues et al., 2007).
Consequently, these results indicate that an adequate
age-length key is necessary for the estimation of
Brazilian flathead age from length data; that is, a key
that corresponds in sex and season with the sample of
lengths that will be transformed. Dissimilar growth
parameters between seasons have been detected in
species which have seasonal migratory-age-dependent
habits (Sparre & Venema, 1995). So, these results
could be indicating that Brazilian flathead of the South
Atlantic coastal water (34-41S) is a species which
have this kind of migratory habits, although studies
with a greater temporal cover are necessary to confirm
this hypothesis.
ACKNOWLEDGEMENTS
This study was partially published as part of a
Licenciatura thesis by the Biodiversity and
Experimental Biology Department, Universidad de
Buenos Aires (UBA),Argentina, and was carried out at
Instituto Nacional de Investigacin y Desarrollo
Pesquero (INIDEP-Mar del Plata), Argentina.
Contribution INIDEP N 1663. We thank INIDEP
Coastal Project for providing biological material and
information, and Alicia Matthews for improving the
language.
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DOI: 10.3856/vol39-issue2-fulltext-12

Research Article

Seasonal variation and influence of turbidity and salinity on the zooplankton of a

saline lake in central Argentina

Santiago Andrs Echaniz1 & Alicia Mara Vignatti1

1
Facultad de Ciencias Exactas y Naturales, Universidad Nacional de La Pampa
Avenida Uruguay 151, 6300 Santa Rosa, Provincia de La Pampa, Repblica Argentina

ABSTRACT. The limnology of saline water bodies at other latitudes is fairly well known, but in Argentina
such studies have only recently begun. The applicability of many conclusions regarding the functioning of
these environments around the world is limited due to the scant ecological knowledge of some endemic
species recorded in the assemblages of Argentine lakes. The aims of this work were to determine the effects of
salinity and inorganic turbidity on the taxonomic composition, abundance, and zooplankton biomass in a
shallow, hypereutrophic, mesosaline lake in the north of La Pampa province characterized by seasonality,
variations in level and salinity, and the lack of macrophytes and fishes, and to compare it with other shallow
lakes of the province. We found important differences with other saline lakes: the species richness was lower;
the mean abundance of zooplankton was between four and six times higher; and rotifers, which were not
affected by salinity or the concentration of inorganic suspended solids, were numerically predominant.
Crustaceans, on the other hand, were negatively affected by these environmental factors. Biomass was two-
fold higher than that recorded in the same period in two shallow lakes of Pampa, with similar nutrient
concentrations but lower salinities.
Keywords: saline lakes, inorganic turbidity, zooplankton biomass, Boeckella poopoensis, Argentina.

Variacin estacional e influencia de la turbidez y la salinidad sobre el zooplancton

de un lago salino de la regin central de Argentina

RESUMEN. La limnologa de los cuerpos de agua salinos de otras latitudes es bastante conocida, pero en
Argentina se ha comenzado a estudiar recientemente. Muchas conclusiones sobre el funcionamiento de estos
ambientes a nivel mundial son de aplicacin restringida debido a que las asociaciones registradas en los lagos
argentinos tienen algunas especies endmicas, cuyo conocimiento ecolgico es escaso. Los objetivos de este
trabajo fueron determinar los efectos de la salinidad y la turbidez inorgnica sobre la composicin taxonmica,
abundancia y biomasa zooplanctnica en un lago somero mesosalino hipereutrfico del norte de La Pampa,
caracterizado por su temporalidad, variaciones del nivel y salinidad, carencia de macrfitas y peces, y
compararlo con otros lagos someros de la provincia. Se encontraron importantes diferencias con otros lagos
salinos, la riqueza especfica fue menor, la abundancia media del zooplancton fue entre 4 a 6 veces superior y
el predominio numrico fue de los rotferos, que no fueron afectados por la salinidad o la concentracin de
slidos suspendidos inorgnicos, a diferencia de los crustceos, que fueron afectados negativamente por estos
factores ambientales. La biomasa fue dos veces ms elevada que la registrada en el mismo perodo en dos
lagos someros pampeanos con parecida concentracin de nutrientes pero con salinidades menores.
Palabras clave: lagos salinos, turbidez inorgnica, biomasa zooplanctnica, Boeckella poopoensis, Argentina.

___________________
Corresponding author: Santiago Echaniz (sechaniz@cpenet.com.ar)

INTRODUCTION 1986). They are widely distributed in the world and

are abundant in arheic and endorheic basins of arid
Saline water bodies can be defined as those with and semiarid regions (Williams, 2002). They are
salinities equal to or higher than 3 g L-1 (Hammer, highly influenced by the human activities carried out
307 Zooplankton of a turbid saline lake of Argentina
in their basins, which cause changes in their
characteristics, with the consequent loss of
biodiversity (Velasco et al., 2006).
The limnology of water bodies in other latitudes is
relatively well-known, whereas, in Argentina, there
are only a few reports on the saline lakes of Buenos
Aires (Olivier, 1955; Ringuelet, 1968, 1972) and
Santa Fe provinces (Jos de Paggi & Paggi, 1998), the
northwest (Locascio de Mitrovich et al., 2005;
Villagra de Gamundi et al., 2008) and Crdoba
province (Bucher, 2006). Therefore, the information
on their taxonomic composition, abundance and
zooplankton biomass and its variation is still scarce.
We have thus recently started studies on the
ecology and zooplankton of saline lakes of La Pampa
province, in the semiarid center of Argentina (Echaniz
et al., 2005, 2006; Vignatti et al., 2007). However, in
those works, we determined mainly the population
density but not the biomass in relation with
environmental parameters.
Many of the conclusions on the functioning of
saline lakes are applicable for the shallow lakes of La
Pampa, but little is known on the ecology of the
assemblages recorded in the central region of
Argentina, where some species, especially
crustaceans, are endemic to the neotropical region
(Adamowicz et al., 2004; Echaniz et al., 2005, 2006;
Vignatti et al., 2007).
The aims of this work were to analyze the
variations in the main limnological parameters and the
zooplankton of an inorganic turbid shallow lake with
high salinity, located in the north of La Pampa
province, along its annual cycle, and to test the
following hypotheses: i) that the high concentration of
dissolved solids affects the taxonomic composition
and abundance of the zooplankton community, ii) that
inorganic turbidity has detrimental effects on the
development of zooplankton (Quirs et al., 2002;
Torremorell et al., 2007), and iii) that at nutrient
concentrations equal to those of other Pampean water
bodies with lower salinity, this lake has a higher
biomass of zooplankton, in agreement with that
reported by Evans et al. (1996) for lakes of Canada.
MATERIALS AND METHODS
Study area
The Prato shallow lake is located in the north of La
Pampa province (6415W, 3526S) (Fig. 1), in a
plain region with soft hills and covered with a sand
layer of variable thickness (Calmels & Casado, 2005),
in the ecotone between the phytogeographical
provinces of the Pampean Plains and the Thorny
Forest (Cabrera, 1976). Has a surface of 62.8 ha and a
maximum depth of 2.6 m.
The mean annual precipitations of the region are
around 700 mm (Casagrande et al., 2006), with a
maximum in summer, but the potential evapotrans-
piration is about 800 mm year-1 (Roberto et al., 1994).
The lake is fed by rainfalls and, to a lesser extent, by
phreatic waters. It is an arheic water body, which loses
water by evaporation or infiltration and suffers large
level fluctuations. The land of its basin is used for
agriculture and extensive cattle breeding. It has a
regular shape, its bottom sediments consists mainly of
sands, and there is absence of macrophytes and ichtyc
fauna.
Field and laboratory work
Samples were collected monthly from December 2005
until December 2006, except in August, in the three
stations located along the longest axis of the lake.
Water temperature, dissolved oxygen concentration
(oximeter Lutron OD 5510), water transparency
(Secchi disc), and pH (digital pH meter Cornning PS
15) were determined in each station. Water samples
were taken and kept refrigerated until their analysis in
the laboratory.
Two quantitative zooplankton samples were
collected in each site with a 10-l Schindler-Patalas
trap, with a 0.04 mm mesh size, and one qualitative
sample with a net 22 cm in diameter and a similar
mesh size. All the samples were anesthetized with
CO2 and kept refrigerated until fixation, with the aim
to avoid contractions that may deform the individuals
collected.
Salinity was determined by means of the
gravimetric method with drying at 104C.
Chlorophyll-a concentration was measured by
extraction with aqueous acetone and spectropho-
tometry (spectrophotometer Metrolab 1700) (Arar,
1997; APHA, 1999), total nitrogen by means of the
Kjeldahl method, and total phosphorus by digestion
with potassium peroxodisulfate in acid medium and
UV-visible spectrophotometry (APHA, 1999).
The content of suspended solids was determined
with fiberglass filters (Microclar FFG047WPH), dried
at 103-105C until constant weight and calcined at
550C (EPA, 1993). Macro-and microzooplankton
(Kalff, 2002) were counted under a stereoscopic and a
conventional optical microscope, in Bogorov and
Sedgwick-Rafter chambers respectively.
Conventional measurements of the individuals of
each species sampled were taken with a Carl Zeiss
ocular micrometer, and length-dry weight formulae
were used to determine zooplankton biomass (Dumont
 Lat. Am. J. Aquat. Res.
Figure 1. Location of the Prato shallow lake in the north of La Pampa province, Argentina. a, b and c: sampling sites.
Figura 1. Localizacin de la laguna de Prato en el norte de la provincia de La Pampa, Argentina. a, b y c: sitios de
muestreo.
et al., 1975; Rosen, 1981; McCauley, 1984; Culver et
al., 1985; Kobayashi, 1997).
Non parametric ANOVA Kruskal Wallis test,
Spearmans correlations and principal component
analysis (PCA) (Zar, 1996; Mangeaud, 2004; Prez,
2004) were carried out by means of the PAST
software version 1.94b (Hammer et al., 2001).
RESULTS
Physical and chemical parameters
Spatial variations of this parameters were not
significant, so we used mean values. The mean
concentration of total dissolved solids in the water was
25.3 g L-1, but increased as the level of water
decreased (Fig. 2 and Table 1), and was characterized
by the predominance of Cl- and Na+, which were
higher than 49% and 92% of the anions and cations
respectively. The pH was high (9.02 0.16) and
relatively stable (Table 1).
The water temperature varied seasonally, with a
maximum of 26.8C in December 2005 and a
minimum of 8.1C in July 2006 (Fig. 3). The
concentration of dissolved oxygen was also variable,
oscillating between 9.8 mg L-1 in December 2005 and
1.3 mg L-1 in April 2006 (Fig. 3). The concentration of
nutrients was high and variable (Table 1).
Chlorophyll-a concentration correlated with water
temperature (R = 0.73; P = 0.0065) and presented a
maximum in February 2006, but was relatively low
and stable during the rest of the period studied (Fig.
4).
308
Figure 2. Monthly variation of maximum depth and
concentration of total dissolved solids (TDS) in Prato
shallow lake.
Figura 2. Variacin mensual de la profundidad mxima
y de la concentracin de slidos disueltos totales (TDS)
en la laguna de Prato.
The concentration of organic suspended solids was
higher during the first four months and was
significantly correlated with chlorophyll-a concen-
tration (R = 0.65; P = 0.022), whereas that of
inorganic suspended solids was more abundant during
the last six months (Fig. 4). We found a significant
correlation between the concentration of inorganic
suspended solids and that of total phosphorus (R =
0.75; P = 0.005).
Water transparency was reduced (0.17 m 0.06)
and variable along the year (Fig. 5, Table 1), and was
significantly correlated with the concentration of
inorganic suspended solids (R = -0.89; P = 0.0001),
but not significantly correlated with that of organic
suspended solids (R = 0.02; P = 0.940) or chlorophyll-
a concentration (R = 0.40; P = 0.194) (Fig. 8).
309 Zooplankton of a turbid saline lake of Argentina

Table 1. Main physical and chemical parameters registered in Prato shallow lake during the studied period. TP: total
phosforus, TN: total nitrogen.
Tabla 1. Principales parmetros fsico qumicos registrados en la laguna de Prato durante el perodo estudiado. TP:
fsforo total, TN: nitrgeno total.

Mean Min. Max.

Transparency (m) 0.17 0.08 0.31
Salinity (g L-1) 25.34 19.47 36.84
pH 9.02 8.9 9.32
TP (mg L-1) 18.1 11.25 25
TN (mg L-1) 28.62 20.63 35.63
TN:TP 1.58 1.3 2.5
Chlorophill-a (mg m-3) 30.79 9.35 94.79
Dissolved oxigen (mg L-1) 6.3 1.3 9.8
Inorganic suspended solids (mg L-1) 38.03 10 63.2
Organic suspended solids (mg L-1) 37.52 16 78.7

Figure 4. Monthly variation of the concentration of

Figure 3. Monthly variation of water temperature and
dissolved oxygen concentration in Prato shallow lake.
Figura 3. Variacin mensual de la temperatura del agua
y de la concentracin de oxgeno disuelto en la laguna de
Prato.
inorganic and organic suspended solids and chlorophyll-
a in Prato shallow lake.
Figura 4. Variacin mensual de la concentracin de
slidos suspendidos inorgnicos y orgnicos y de
clorofila-a en la laguna de Prato.

Zooplankton The density of the community presented two peaks

We recorded a total of six species (Table 2). Among
crustaceans, Moina eugeniae and the calanoid
Boeckella poopoensis were constantly present,
whereas M. macrocopa and the harpacticoid
Cletocamptus deitersi were recorded along four and
nine months respectively. Among rotifers, Brachionus
plicatilis was present along 10 months, whereas B.
dimidiatus along only 2 months (Table 2). Variations
of micro- and macrozooplankton abundance between
sampling sites were not significant.
The spatial variations of the zooplankton
abundance and biomass were not significant, so we
used mean values.
during the warmer months (Fig. 6), produced mainly
by rotifers (B. dimidiatus in January 2006 and B.
plicatilis in December 2006). Although their
abundance was very variable and there were months
during which they were not recorded, they presented
the highest annual mean abundance (Fig. 7, Table 2).
The PCA, whose first two components allowed
explaining more than 60% of the variance, showed
positive correlations between their abundance, the
concentrations of organic suspended solids,
chlorophyll-a and water temperature, but negative
correlations between their abundance and salinity and
inorganic suspended solids concentrations (Fig. 8).
 Lat. Am. J. Aquat. Res.
Figure 5. Monthly variation of water transparency in
Prato shallow lake.
Figura 5. Variacin mensual de la transparencia del agua
en la laguna de Prato.
Among crustaceans, the most abundant species was
B. poopoensis followed by M. eugeniae (Table 2). B.
poopoensis presented its maximum abundances at the
beginning of the summer, whereas M. eugeniae and
M. macrocopa did so during fall. The PCA showed
positive correlations between crustacean abundance,
chlorophyll-a concentration and water transparency,
but negative ones between crustacean abundance,
salinity and inorganic suspended solids (Fig. 8).
The mean biomass of the zooplankton community
(6614.1 g L-1 4336.9) presented a peak during fall
and a minimum in spring (Fig. 9). In all cases, the
highest contribution was that of crustaceans (Fig. 10),
among which B. poopoensis represented more than
their biomass and salinity and organic suspended solid
concentrations. The contribution of rotifers was
important only in December 2006, when it represented
29.5% of the total (Fig. 10) and the PCA also showed
a positive correlation with abundance and water
temperature (Fig. 8).
DISCUSSION
The Prato lake is located in the western boundary of
the Pampean plain (Cabrera, 1976), and although it
shares characteristics with typical Pampean lakes of
the province of Buenos Aires (Ringuelet, 1968 and
1972; Torremorell et al., 2007), such as the reduced
depth and the polymixis, it differs from them because
of its seasonality and great variations in water level
and salinity.
These fluctuations are typical of most shallow
lakes of La Pampa province, which are mainly fed by
precipitations and lose water by evaporation (Echaniz
310
Figure 6. Monthly variation in the total zooplanktonic
abundance in Prato shallow lake. The values are the
mean of the three sampling stations.
Figura 6. Variacin mensual de la abundancia total
zooplanctnica en la laguna de Prato. Los valores
corresponden al promedio de las tres estaciones de
muestreo.
Figure 7. Monthly variation in the percent composition
of the zooplanktonic abundance during the studied
period. The values are the mean of the three sampling
stations.
Figura 7. Variacin mensual de la composicin
porcentual de la abundancia zooplanctnica durante el
perodo estudiado. Los valores corresponden al promedio
de las tres estaciones de muestreo.
et al., 2005, 2006; Vignatti et al., 2007). This
phenomenon is particularly important because these
lakes are located in a region where the evapo-
transpiration overpasses precipitations (Roberto et al.,
1994). This characteristic was reflected in this lake by
the decrease of almost 0.6 m in the water level and an
increase in the concentration of dissolved solids,
which, at the end of the study, was almost twice of the
initial value, although it was within the mesosaline
range (Hammer, 1986).
The absence of variations in the spatial distribution
of physical and chemical parameters and zooplank-
tonic abundance and biomass of this lake was
311 Zooplankton of a turbid saline lake of Argentina

Figure 8. Results of the Principal Component Analysis (PCA). Rot.: rotifers, Clad.: cladocerans, Cop.: copepods, Ab.:
abundance, Biom.: biomass, TN and TP: total nitrogen and phosphorus concentrations, Inorg. susp. sol.: inorganic
supended solids, Org. susp. sol.: organic suspended solids, Transp.: water transparency, Temp.: water temperature, Chl a:
chlorophyll concentration.
Figura 8. Resultados del Anlisis de Componentes Principales (ACP). Rot.: rotferos, Clad.: cladceros, Cop.:
coppodos, Ab.: abundancia, Biom.: biomasa, TN y TP: concentraciones de nitrgeno y fsforo totales, Inorg. susp. sol.:
slidos suspendidos inorgnicos, Org. susp. sol.: slidos suspendidos orgnicos, Transp.: transparencia del agua, Temp.:
temperatura del agua. Chl a: concentracin de clorofila.

Table 2. List of species recorded, mean, minimum and maximum abundance and biomass and relative frequency of their
appearance in the samples.
Tabla 2. Lista de las especies registradas, abundancia y biomasa medias, mnimas y mximas y frecuencia relativa de
aparicin en las muestras.

Frequency Abundance (ind L-1) Biomass (g L-1)

(%) Mean Min. Max. Mean Min. Max.
Cladocerans
Moina eugeniae Olivier, 195 100 219.1 14 1235.3 1611.4 153 8190.2
Moina macrocopa (Straus, 1820) 33.3 28 0 312.7 185.54 0 2101.1
Copepods
Boeckella poopoensis Marsh, 1906 100 369.7 72.7 737.3 4236.3 512.2 9436
Cletocamptus deitersi (Richard, 1897) 66.7 4.2 0 13.5 4.28 0 17.2
Rotifers
Brachionus plicatilis Mller, 1786 83.3 1330.4 0 11546.7 412 0 3002.1
Brachionus dimidiatus Bryce, 1931 16.7 872.5 0 10467 34.9 0 418.7

probably related to their shallow depth, the shape of
their basin (flat and free from obstacles) and to wind
action, all of which determine their polymictic
condition and the permanent mixture of water.
Another feature shared by most lakes of La Pampa
is the predominance of Cl- and Na+, with propor-
tionally low bivalent cations concentrations (Ca++ and
Mg++) (Echaniz et al., 2006).
The lake studied presented some characteristics
that differentiate it from other environments of La
Pampa with similar salinity, in particular, among the
physical factors, its reduced transparency, which was
 Lat. Am. J. Aquat. Res.
Figure 9. Monthly variation in total zooplankton
biomass during the studied period. The values are the
mean of the three sampling stations.
Figura 9. Variacin mensual de la biomasa total del
zooplancton durante el perodo estudiado. Los valores
corresponden al promedio de las tres estaciones de
muestreo.
almost 10 times lower than that recorded in previous
studies (Echaniz et al., 2006; Vignatti et al., 2007).
This high turbidity was due to the differential
predominance of the two fractions of suspended solids
along the year. Those of organic origin were higher
during the summer, when the concentration of
chlorophyll-a was also high, whereas those of
inorganic origin were higher during winter and spring,
when more intense winds are present (Cano, 1980).
Due to the scarce depth of the lake, these winds cause
the removal and resuspension of bottom sediments
(Scheffer, 1998; Borell Lvstedt & Bengtsson, 2008).
In addition, unlike that found in similar lakes of the
province, this situation was favored by the total
absence of macrophytes, which make resuspension
more difficult.
The high concentrations of nutrients, which
allowed us to characterize the lake as hypereutrophic
(OECD, 1982), were similar to those of other
environments of La Pampa (Echaniz et al., 2008;
Echaniz & Vignatti, unpublished data), but, in
particular, total phosphorus was several times higher
than those reported by Quirs et al. (2002) and
Sosnovsky & Quirs (2006) for shallow lakes of
Buenos Aires province. This could be due, on one
hand, to the high impact caused by the dragging of the
feces of animals that feed on its basin, especially
during storms (Carpenter et al., 1998; Bennett et al.,
1999; Bremigan et al., 2008), since cattle can excrete
between 9 and 16 kg of phosphorus.ind.year-1 (Russell
et al., 2008). On the other hand, the resuspension of
sediments by the wind is particularly important in
312
Figure 10. Monthly variation in the percent composition
of zooplankton biomass. The values are the mean of the
three sampling stations.
Figura 10. Variacin mensual de la composicin
porcentual de la biomasa del zooplancton. Los valores
corresponden al promedio de las tres estaciones de
muestreo.
shallow lakes (Markensten & Pierson, 2003; De
Vicente et al., 2006; Borell-Lvstedt & Bengtsson,
2008), since removal favors the resolubilization of the
nutrients of the internal load (Havens et al., 2007),
which, in turn, favors the internal eutrophication of the
lake (Smolders et al., 2006). This was probably the
case in the lake studied in this work, since the highest
concentrations of phosphorus were found during the
second half of the year, during which stronger winds
are present (Cano, 1980) and the concentrations of
inorganic suspended solids were highest. In addition,
the reduced capacity of phosphorus and nitrogen
absorption of the sediments due to the relatively large
size of the predominant particles (Kapanen, 2008) and
to the fact that water is lost only by evaporation
because the lake is an arheic environment leads to
accumulation processes.
Zooplankton diversity was reduced, a common
situation in environments with high salinity (Hammer,
1986; Herbst, 2001; Ivanova & Kazantseva, 2006), but
another feature that differentiates this lake from others
of La Pampa is the lower species richness found, since
the species richness in other lakes with similar
concentrations of dissolved solids but much higher
transparency is close to 15 (Echaniz et al., 2006,
Vignatti et al., 2007).
As regards the zooplankton found, the species
recorded were typical of these ecosystems and were
characterized by the presence of autochthonous
halophilic crustaceans, such as Moina eugeniae, a
species restricted to saline waters of the central region
of Argentina (Paggi, 1998; Echaniz et al., 2006), and
313 Zooplankton of a turbid saline lake of Argentina
Boeckella poopoensis, a species that has a very wide
geographical distribution, from the north of Patagonia
to the south of Per (Menu-Marque et al., 2000; De
los Ros, 2005; Locascio de Mitrovich et al., 2005).
The two rotifer species found have a wide distribution
and are tolerant to salinity (Fontaneto et al., 2006).
Other important differences found with other saline
lakes of La Pampa were the high total mean
abundance, which was between four and six times
higher (Echaniz et al., 2006; Vignatti et al., 2007), and
the numeric predominance of rotifers, which were
almost four and ten times more abundant than
copepods and cladocerans respectively, in spite of
which their biomass was only about 7% of the total.
Among rotifers, B. plicatilis showed a more
constant presence, since it was recorded during most
of the year and its maximum density was several times
higher than the maximum recorded in other lakes of
the province (Echaniz et al., 2006).
The abundance and biomass of rotifers were
affected by water temperature and chlorophyll-a
concentration, but not by salinity or the concentration
of inorganic suspended solids. In contrast, the
abundance and biomass of both cladocerans and
copepods were negatively affected by the
concentration of inorganic suspended solids and
salinity, but positively affected by water temperature,
since both parameters were higher during summer and
fall.
The zooplankton biomass of Prato shallow lake
was two-fold higher than that recorded in the same
period in Don Toms and Bajo de Giuliani, two
shallow lakes of La Pampa, which showed a similar
concentration of nutrients, but salinities of 0.8 and
9.82 g L-1 and concentrations of chlorophyll-a of
154.6 and 173.7 mg m-3 respectively (Echaniz et al.,
2008; Echaniz et al., 2009).
Besides, the macrozooplankton biomass of Prato
lake was six times higher than the maximum
determined by Quirs et al. (2002) in a group of 23
organic turbid shallow lakes of Buenos Aires, which
presented salinities between 0.3 and 27 g L-1 and
concentrations of chlorophyll-a of up to 405 mg m-3.
This supports the hypothesis that although saline lakes
have low concentrations of chlorophyll-a, lower algal
biomass, and thus low primary productivity, they are
able to support high zooplankton biomasses (Evans et
al., 1996).
ACKNOWLEDGEMENTS
We thank the Facultad de Ciencias Exactas y
Naturales, Universidad Nacional de La Pampa for the
financial support of the project and Mr. Hugo Prato
and his family, owners of the rural establishment in
which the lake is located.
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DOI: 10.3856/vol39-issue2-fulltext-13

Research Article

Estimacin de mortalidad natural e incertidumbre para congrio dorado

(Genypterus blacodes Schneider, 1801) en la zona sur-austral de Chile

Rodrigo Wiff1, J.C. Quiroz1, Vilma Ojeda1 & Mauricio A. Barrientos2

1
Divisin de Investigacin Pesquera, Instituto de Fomento Pesquero
Blanco 839, Valparaso, Chile
2
Instituto de Matemticas, Pontificia Universidad Catlica de Valparaso
Blanco Viel 596, Cerro Barn, Valparaso, Chile

RESUMEN. El congrio dorado (Genypterus blacodes) es un pez demersal de gran importancia econmica en
la pesquera multiespecfica y multiflota que opera en la zona sur-austral de Chile (4128-5700S). Desde
principio de los aos noventas se consider para efectos de la evaluacin poblacional la existencia de un nico
stock. Sin embargo, varios antecedentes relacionados con la historia de vida y demografa han conducido a
que, desde el ao 2005, la evaluacin de esta especie se realice bajo dos stocks administrativos, uno en la zona
norte (4128-4700S) y otro en la zona sur (4700-5700S). La separacin de stocks produce una demanda
por actualizacin de parmetros de historia de vida, entre stos la mortalidad natural (M). En este trabajo se
estim M para el congrio dorado mediante mtodos empricos aplicados por zona y sexo. La incertidumbre en
M fue incorporada a travs de remuestreo de Monte Carlo considerando dos fuentes de error, una proveniente
de los parmetros de historia de vida que alimentan los modelos empricos y otra, proveniente de los
coeficientes que los definen. El promedio de M mediante los diferentes mtodos mostr, para una determinada
zona, importantes diferencias entre sexos, como tambin para sexos conjuntos entre zonas de pesca. Los
individuos de la zona norte presentaron mayor M que aquellos provenientes de la zona sur y los coeficientes de
variacin por mtodo son altamente dependientes del tipo de error incorporado. El mtodo de Pauly (1980)
parece ser el ms adecuado para el congrio dorado entregando valores de M para sexos conjuntos de 0,27 ao-1
(IC: 0,13-0,47) en la zona norte y 0,23 ao-1 (IC: 0,11-0,40) en la zona sur.
Palabras clave: Genypterus blacodes, mortalidad natural, pesquera demersal, historias de vida, demografa,
sur de Chile.

Estimation of natural mortality and uncertainty in pink cusk-eel

(Genypterus blacodes Schneider, 1801) in southern Chile
ABSTRACT. Pink cusk-eel (Genypterus blacodes) is a demersal fish of high economic importance for the
multi-species and multi-fleet fishery operating off far-southern Chile (4128-5700S). Since the early 1990s,
the existence of a single stock was assumed for purposes of stock assessments. However, several attributes
related with life history and demography led to the designation, as of 2005, of two administrative stocks of this
species, a northern-austral stock stock (4128-4700S) and a southern-austral stock (4700-5700S). The
division of these stocks has produced a demand for updating life history parameters, including natural
mortality (M). In the present work, we used empirical methods to estimate M for pink cusk-eel by zone and
sex. The uncertainty in M was incorporated through Monte Carlo resampling considering two sources of error:
one from the life history parameters that feed the empirical models and the other from the coefficients that
define them. The average M obtained by the different methods showed important differences between sexes
for a given zone and between combined sexes between the different fishing zones. The M for individuals from
the northern-austral zone was higher than that for those from the southern-austral zone. The coefficients of
variation by method were highly dependent on the type of error incorporated. Paulys (1980) method seems to
be the most appropriate for pink cusk-eel, providing M values for the combined sexes of 0.27 year-1 (IC: 0.13-
0.47) for the northern-austral zone and 0.23 year-1 (IC: 0.11-0.40) for the southern-austral zone.
Keywords: Genypterus blacodes, natural mortality, demersal fishery, life history, demography, southern
Chile.
___________________
Corresponding author: Rodrigo Wiff (rwiff@ifop.cl)
317 Mortalidad natural en congrio dorado, zona sur-austral de Chile
INTRODUCCIN
Las especies que constituyen el gnero Genypterus
son peces bento-demersales que habitan el talud y
plataforma continental en el hemisferio sur. Aunque
seis especies pertenecientes a este gnero podran ser
de inters econmico (Ward & Reilly, 2001), el
congrio dorado (Genypterus blacodes) es la especie
ms importante en trminos de intencionalidad de
pesca y niveles de captura, conformando importantes
pesqueras en Australia (Ward et al., 2001), Nueva
Zelandia (Horn, 1993), Argentina (Cordo, 2001) y
Chile (Wiff & Quiroz, 2010).
Acorde a los registros histricos de capturas
disponibles, la pesquera de congrio dorado en Chile
se ha desarrollado entre Talcahuano (3644S) y el sur
del Cabo de Hornos (5700S); sin embargo, la
principal zona de explotacin est circunscrita a la
zona sur-austral (4128-5700S) (Fig. 1).
Actualmente, el congrio dorado es capturado por una
pesquera multiflota constituida por una componente
industrial de embarcaciones arrastreras y palangreras,
y una segunda componente artesanal de embar-
caciones espineleras. Esta pesquera comenz a ser
monitoreada a principio de los aos setenta,
registrndose bajas capturas que evidenciaban una
reducida intencio-nalidad de pesca hacia esta especie.
Durante la dcada de los ochenta la flota comenz a
dirigir esfuerzo sobre el recurso y ya a principio de los
aos noventa, debido a los altos niveles de captura
registrados, las autoridades competentes decidieron
declarar al congrio dorado en estado de plena
explotacin (Decreto Supremo N 656).
Este estado de explotacin corresponde a una
disposicin de la Ley General de Pesca y Acuicultura
de Chile, que bsicamente faculta a la administracin
pesquera al establecimiento de cuotas de captura. En
este contexto, desde 1992 esta pesquera se ha
manejado por medio de cuotas de captura lo que ha
llevado a estimar niveles de biomasas. Las
estimaciones de biomasas son obtenidas regularmente
desde modelos de evaluacin de stock, los que han
contemplado el anlisis de poblacin virtual y los
modelos estadsticos de captura a la edad. Hasta el ao
2004, la modelacin inclua un nico stock de congrio
dorado distribuido en la zona sur-austral (Montecinos
& Canales, 2004). Sin embargo, Wiff et al. (2005)
mostraron diferencias demogrficas como tallas
medias y proporcin sexual como tambin en la
funcin de crecimiento al interior de la zona sur-
austral, proponiendo una diferenciacin en las zonas
de manejo de la pesquera demersal sur-austral (PDA).
Bajo estos argumentos, desde el ao 2005 se viene
realizando una modelacin poblacional separada para
la zona norte (4128S-4700S) y zona sur (4700-
5700S) de la zona sur-austral (Fig. 1), suponiendo la
existencia de dos unidades de stocks. Esta separacin
de stocks requiere el anlisis de los parmetros de
historias de vidas diferenciados por zonas. En este
sentido, si bien Wiff et al. (2007) contribuyeron
proporcionando estimaciones de parmetros de creci-
miento de von Bertalanffy por sexo, tanto para la zona
norte como la zona sur, an existe carencia sobre los
valores de mortalidad natural (M) para cada zona con
sus valores de incertidumbre asociados.
Las estimaciones disponibles de M para congrio
dorado han sido realizadas en forma determinista y
empleando mtodos bioanalgicos para la extensin
total de la zona sur-austral (Aguayo et al., 1986; Ojeda
et al., 1986). En este sentido, estimaciones detalladas
de M por zonas son altamente deseables para la
determinacin de biomasas poblacionales. El principal
objetivo de este trabajo es proveer estimaciones de
mortalidad de congrio dorado por sexo y zona, por
medio de un conjunto de modelos empricos e
incorporado la incertidumbre intrnseca de diferentes
parmetros de historia de vida.
El enfoque de modelacin para la determinacin
del status del recurso y estrategias de explotacin
actualmente implementado en congrio dorado depende
fuertemente de los valores de M (Wiff & Quiroz,
2010). En efecto, M es un parmetro clave en la
determinacin de la dinmica poblacional y esta tiene
influencia directa sobre los estimados de produccin,
ya sea en trminos de crecimiento somtico o la razn
entre la poblacin desovante y la abundancia de
reclutas. A pesar de su importancia, M ha sido el
parmetro de historia de vida estimado con menor
rigurosidad, esto en contraste con otros parmetros de
historia de vida como fecundidad, madurez y
crecimiento (Hewitt & Hoenig, 2005). Idealmente, las
tasas de mortalidad natural debiesen ser estimadas a
travs de mtodos tales como marcaje-recaptura o
anlisis telemtrico (Pollock et al., 2004). Sin
embargo, estos mtodos son difciles de implementar
para la poblacin de congrio dorado en Chile, tanto
por el costo asociado, como los aspectos logsticos
relativos a la prospeccin de un rea geogrficamente
accidentada como la zona sur-austral. Por otro lado, el
anlisis de la curva de captura es un mtodo comn
para estimar mortalidad, sin embargo, este mtodo
requiere supuestos acerca de la condicin virginal del
stock que es difcil de cumplir bajo los actuales
niveles de explotacin de congrio dorado (Wiff &
Quiroz, 2010).
Una alternativa para estimar M proviene de los
mtodos empricos, los cuales bsicamente tratan de
predecir procesos poblacionales complejos en base a
 Lat. Am. J. Aquat. Res. 318

Figura 1. Mapa de la zona de estudio indicando las reas de pesca y las principales ciudades.
Figure 1. Map of the study zone indicating fishing areas and the main cities.

otros parmetros de historia de vida o atributos acuerdo a la disponibilidad y calidad de los

demogrficos que son ms fciles de obtener.
Particularmente en el caso de M, las relaciones
empricas tratan de dar cuenta de la relacin existente
entre sta y otros parmetros de historia de vida. Estas
relaciones han encontrado sustento terico, tanto
desde el punto de vista evolutivo (Charnov, 1993)
como ecolgico (Jensen, 1996). En este trabajo se
emplean relaciones empricas para proporcionar un
rango plausible de M para congrio dorado
incorporando la incertidumbre.
MATERIALES Y MTODOS
Las estimaciones de M se obtuvieron a travs de cinco
mtodos empricos que fueron seleccionados de
parmetros de historia de vida. Los mtodos
seleccionados fueron (1) Alverson & Carney (1975);
(2) Pauly (1980); (3) Frisk et al., (2001); (4) Hoenig
(1983) y (5) Jensen (1996). Los tres primeros mtodos
consideran los parmetros de crecimiento de la
funcin de von Bertalanffy en longitud,
l(a) = l (1 e-k (a-a0)), donde l es la longitud a edad a,
l es la longitud asinttica, k es el coeficiente de
crecimiento y a0 es la edad terica cuando l=0. El
mtodo de Hoenig usa la longevidad amax, mientras
que el mtodo de Jensen incorpora la edad de madurez
a50%, como un indicador de la sobrevivencia (Tabla 1).
Los parmetros de crecimiento y sus errores
estndar, separados por zonas de la PDA y sexo
fueron obtenidos de Wiff et al. (2007), mientras que
 319

Tabla 1. Descripcin de los mtodos aplicados y su coeficiente de variacin (CV). M: mortalidad natural; l y k: parmetros de crecimiento de la ecuacin de von
Bertalanffy, a50%: edad del 50% de madurez, amax longevidad, T: temperatura del ambiente.
Table 1. Applied method description and their coeffcients of variation (CV). M: natural mortality, l y k: growth parameters of the von Bertalanffy equation, a50%: age at
50% of maturity, amax: longevity, T: habitat temperature.

Mtodo Formulacin Coeficientes (CV) Referencia de CV

Alverson & Carney (1975) M = 3k(1 - ) / = 0,62(0,22) Cubillos (2003)

= 0,0066
= 0,2790(0,24)
Pauly (1980) log10=(M) = - - log10(l) + log10 (k) + log10 (T) Pauly (1980)
(T) = 0,6543(0,11)
= 0,4634(0,18)
= 1,1(0,22)
Frisk et al. (2001) M = exp( k + ) Quiroz et al. (2010)
= 0,8(0,62)
Jensen (1996) M = / a50% = 1,65(0,20) *
= 1,44(0,20)
Hoenig (1983) log (M) = - log amax *
= 0,982(0,20)
Mortalidad natural en congrio dorado, zona sur-austral de Chile

(*) CV = 0.2 fue considerado

 Lat. Am. J. Aquat. Res.
sus respectivas matrices de correlacin fueron
obtenidas de Wiff et al. (2006). Luego, amax es
estimada como la edad a la cual el 95% de l es
alcanzado. La longitud al 50% de madurez (l50%) fue
obtenida de Aguayo et al. (2001), quienes reportan
(l50% = 82,2 cm (IC95%=80,5-84,2) para hembras y
(l50% = 70,2 cm (IC95%=66,7-73,8) para machos,
indistintamente de las zonas de pesca. Con estos
parmetros, a50% fue calculada con los parmetros de
crecimiento especficos para cada sexo y zona.
La incertidumbre fue incorporada siguiendo el
mtodo propuesto por Quiroz et al. (2010). De
acuerdo a estos autores, las estimaciones de M fueron
evaluadas incluyendo dos fuentes independientes de
incertidumbre:
(1) Los errores provenientes desde los parmetros
de historia de vida que son usados como valores de
entrada en los modelos empricos (de aqu en adelante
error de rasgo);
(2) el error intrnseco provenientes desde los
coeficientes que definen las ecuaciones empricas (de
aqu en adelante error de coeficiente). La
incertidumbre fue incorporada a travs del mtodo
Monte Carlo, remuestreando 5000 veces los
parmetros de crecimiento, longitud de madurez,
temperatura promedio del ambiente y los coeficientes
de regresin de los mtodos descritos.
La incertidumbre de los parmetros de crecimiento
fue incorporada a travs del remuestreo desde una
distribucin normal multivariada que utiliza la matriz
de covarianza descrita por los estimadores asintticos
de varianza y correlacin. Definiendo los parmetros
de crecimiento como un vector u de longitud n, se
tiene que u = {l , k , a0 } , luego es posible obtener m
vectores aleatorios u m* = X = [ x1 ,.., xm ]T desde la
funcin de distribucin de densidad:
1 1
f ( x1 ,.., xm ) = exp (X u )T 1 (X u ) , (1)
(2 ) n /2 2
1/2
donde es la matriz de varianza-covarianza (n x n) de
u, la cual rene las siguientes caractersticas: E(X) = u
tal que, E (X u )(X u )T = donde E es el operador
esperanza.
Por otro lado, el parmetro a50% fue remuestreado
desde una distribucin uniforme truncada acorde al
intervalo del 95% de confianza de la longitud a la
madurez. Un procedimiento similar fue implementado
para introducir la incertidumbre en la temperatura del
ambiente utilizada por el mtodo de Pauly (1980),
remuestreando desde una distribucin uniforme
truncada entre 8 y 11C. Estos valores de temperatura
320
corresponden a la mnima y mxima reportada para la
zona sur-austral (Bustos et al., 2007).
La incorporacin del error de coeficiente en el
mtodo de Pauly (1980) y el de Alverson & Carney
(1975), fue realizada a travs de remuestreo de los
coeficientes de regresin desde una distribucin
normal y con coeficientes de variacin (CV) acorde a
la Tabla 1. Debido a la falta de informacin
relacionada con los estimadores de varianza del
mtodo de Jensen (1996) y el de Hoenig (1983), al
igual que como lo consideraron Quiroz et al. (2010),
se asumi que los coeficientes de regresin fueron
normalmente distribuidos con un CV del 20%.
RESULTADOS
En trminos generales, las estimaciones promedio de
mortalidad natural (M) entregadas por los mtodos
para ambas zonas y sexos fueron menores con el
mtodo de Pauly (1980), ya sea incorporando
nicamente el error de rasgo o adicionando el error de
coeficiente (Tabla 2). Por el contrario, los mayores
niveles de M promedio se obtuvieron por el mtodo de
Frisk et al. (2001) y por el mtodo de Jensen (1996).
Cuando se analiza M a travs de los mtodos,
incorporando error de rasgo ms error de coeficiente,
la media para machos de la zona norte se encuentra
entre 0,33 y 0,55 ao-1; mientras que para los machos
en la zona sur, la media tiene un rango entre 0,30 y
0,49 ao-1. En el caso de las hembras de la zona norte,
la media de M a travs de los mtodos se encuentra
entre 0,26 y 0,43 ao-1. En el caso de las hembras de la
zona sur, el rango promedio de M a travs de los
mtodos result ligeramente inferior que el obtenido
para la zona norte, variando entre 0,24 y 0,38 ao-1.
Las estimaciones de M promedio para ambos sexos
incorporando ambas fuentes de error cubri entre 0,26
y 0,44 ao-1 para individuos de la zona norte y
medianamente menor, entre 0,23 y 0,34 ao-1, para
individuos de la zona sur-austral. En trminos de
gnero, los machos presentan una M mayor que en
hembras para una misma zona, adems, es recurrente
para ambos sexos que en la zona sur se obtengan
menores valores de M (Figs. 2 y 3).
La incorporacin del error de coeficiente produce
un incremento en el CV de M hasta en ms de 100
veces, esto en comparacin con las estimaciones de M
que nicamente incorporan error de rasgo. Sin
embargo, la sensibilidad de la incorporacin del error
de coeficiente vari a travs de los mtodos usados.
Por ejemplo, para el mtodo de Jensen (1996) y el de
Pauly (1980), la incorporacin del error de coeficiente
hace variar a los estimados de M entre 2 y 10 veces,
321 Mortalidad natural en congrio dorado, zona sur-austral de Chile

Tabla 2. Estimaciones de mortalidad natural en congrio dorado incorporando error de rasgo y error de coeficientes.
Table 2. Natural mortality estimates for pink cusk-eel incorporating trait-error and coefficient-error.

Zona Norte, Pesquera Demersal Sur-Austral

Sexo Error de Rasgo Error de rasgo + error de coeficiente
CV(%) Mediana Media CV(%) Mediana Media
Jensen (1996) Machos 7,04 0,37 0,37 20,90 0,37 0,37
Hembras 2,94 0,28 0,28 19,76 0,28 0,28
Ambos 3,34 0,26 0,26 20,10 0,26 0,26
Pauly (1980) Machos 4,27 0,31 0,31 38,03 0,31 0,33
Hembras 4,23 0,25 0,24 40,55 0,24 0,26
Ambas 4,25 0,25 0,25 40,54 0,25 0,27
Frisk et al. (2001) Machos 0,76 0,47 0,47 63,00 0,47 0,55
Hembras 0,89 0,35 0,35 65,78 0,35 0,43
Ambos 0,66 0,35 0,35 68,62 0,36 0,44
Alverson & Carney (1975) Machos 0,69 0,44 0,44 67,46 0,44 0,51
Hembras 0,81 0,34 0,34 66,39 0,34 0,39
Ambos 0,60 0,34 0,34 63,66 0,34 0,39
Hoenig (1983) Machos 0,65 0,38 0,38 62,28 0,39 0,45
Hembras 0,77 0,28 0,28 67,63 0,28 0,34
Ambos 0,57 0,29 0,29 68,34 0,30 0,35
Zona Sur, Pesquera Demersal Sur-Austral
Jensen (1996) Machos 8,20 0,42 0,42 21,57 0,42 0,42
Hembras 3,07 0,30 0,30 20,27 0,30 0,30
Ambos 3,28 0,29 0,29 20,20 0,29 0,29
Pauly (1980) Machos 4,33 0,28 0,28 39,33 0,27 0,30
Hembras 4,27 0,22 0,22 41,40 0,22 0,24
Ambas 4,27 0,21 0,21 41,68 0,21 0,23
Frisk et al. (2001) Machos 0,85 0,40 0,40 67,29 0,40 0,47
Hembras 0,60 0,31 0,31 69,54 0,31 0,38
Ambos 0,60 0,27 0,27 71,61 0,27 0,34
Alverson & Carney (1975) Machos 0,77 0,39 0,39 63,17 0,39 0,44
Hembras 0,54 0,30 0,30 62,43 0,30 0,35
Ambos 0,54 0,27 0,27 66,51 0,28 0,31
Hoenig (1983) Machos 0,75 0,35 0,35 65,24 0,35 0,42
Hembras 0,52 0,26 0,26 66,61 0,26 0,32
Ambos 0,53 0,24 0,24 72,35 0,24 0,29

mientras que para los restantes mtodos la DISCUSIN

incorporacin del error de coeficiente logra
incrementar los niveles de M entre 79 y 137 veces.
Esto indica que, frente la incorporacin de ambas
fuentes de incertidumbre, los intervalos de confianza
de M para los mtodos de Frisk et al. (2001); Alverson
& Carney (1975) y Hoenig (1983) son mayores que
aquellos estimados con el mtodo de Jensen (1996) o
el de Pauly (1980) (Figs. 2 y 3).
Cuando se analizan ambas fuentes de
incertidumbre, para todos los mtodos, zonas y sexos,
la media fue siempre mayor que la mediana. Esto
indica que al incorporar error de coeficiente produce
una asimetra negativa (kurtosis) en la distribucin de
M, posiblemente debido a la naturaleza log-normal de
los coeficientes que definen los mtodos empricos.
Cada uno de los mtodos implementados entregan
diferente estimaciones de media, mediana y CV. Estas
diferencias son causadas en parte por los parmetros
de historia de vida requeridos para la implementacin
de cada mtodo en especfico. Cuando solamente se
introduce el error de rasgo, los mtodos que dependen
de parmetros anexos a los de crecimiento (Pauly,
1980; Jensen, 1996), presentan mayor dispersin que
aquellos que dependen completamente del crecimiento
(Hoenig, 1983; Alverson & Carney, 1975; Frisk et al.
2001). Esto se puede deber a que los parmetros de
crecimiento de la funcin de von Bertalanffy
reportados por Wiff et al. (2007) presentan un
coeficiente de variacin muy bajo, que a su vez, es
 Lat. Am. J. Aquat. Res. 322

Figura 2. Estimaciones de mortalidad natural por sexo en congrio dorado para la zona norte de la pesquera demersal sur-
austral, incorporando error de rasgo y error de coeficiente.
Figure 2. Natural mortality estimates by sexes for pink cusk-eel in the northern-austral zone incorporating trait-error and
coefficient-error.

Figura 3. Estimaciones de mortalidad natural por sexo en congrio dorado para la zona sur de la pesquera demersal sur-
austral, incorporando error de rasgo y error de coeficiente.
Figure 3. Natural mortality estimates by sexes for pink cusk-eel in the southern-austral zone incorporating trait-error and
coefficient-error.
323 Mortalidad natural en congrio dorado, zona sur-austral de Chile
transferido a las estimaciones de M. Por otra parte, la
incorporacin del error de coeficiente incrementa de
forma importante el CV e introduce asimetra en la
distribucin de M, a travs de las zonas y entre sexos.
Este incremento de CV es una consecuencia directa de
la incorporacin de una fuente adicional de
incertidumbre, mientras que la asimetra de la
distribucin posiblemente obedece a la estructura
multiplicativa en escala logartmica que es asumida en
los errores de los diferentes coeficientes que describen
los mtodos aplicados.
Debido a que es imposible conocer el valor
verdadero de M, carece de sentido comparar los
mtodos en trminos de precisin, no obstante, es
acertado comparar estos mtodos en trminos de la
sensibilidad de M a los errores en los parmetros de
historia de vida y en los coeficientes que describen los
mtodos empricos. Adems, nuestros resultados
indican que los mtodos utilizados para estimar M no
deberan ser comparados utilizando nicamente error
de rasgo, sin antes evaluar las consecuencias en las
estimaciones de M debido a la incorporacin del error
en los coeficientes. En efecto, usar nicamente el error
de coeficiente puede ser difcil de interpretar cuando
se compara el mejor mtodo en trminos de CV,
debido a que stos son altamente sensibles al nmero
de coeficientes y a la forma funcional de sus errores.
De esta forma, la variabilidad en las estimaciones de
M est fuertemente asociada a la naturaleza
paramtrica de los mtodos aplicados. Por ejemplo,
los mtodos de Jensen (1996) y Alverson & Carney
(1975) dependen de un parmetro de historia de vida y
un coeficiente de regresin. En trminos de historia de
vida, el mtodo de Jensen depende de a50%, mientras
que el mtodo de Alverson & Carney (1975) utiliza el
parmetro de crecimiento k. Cuando ambos errores
son incorporados, el mtodo de Jensen (1996) presenta
el menor CV. Debido a que los parmetros de
crecimiento y la edad de madurez presentan valores
bajos de CV (Aguayo et al., 2001; Wiff et al., 2007),
los elevados niveles de CV para el mtodo de
Alverson & Carney (1975) en comparacin con el
mtodo de Jensen (1996), se deben al error de
coeficiente para cada uno de estos mtodos. Por otra
parte, el mtodo de Hoenig (1983) y el mtodo de
Frisk et al. (2001) tambin dependen de un parmetro
de historia de vida, pero stos requieren dos
coeficientes de regresin. Cuando ambas fuentes de
error son consideradas, estos mtodos muestran
intervalos de confianza ms altos que los obtenidos
por los restantes mtodos empricos. Esta es una
consecuencia derivada de la magnitud del error en los
coeficientes regresivos de estos mtodos, que en
definitiva se propagan a la variabilidad de M.
El mtodo de Pauly (1980) depende de dos
parmetros de historia de vida, cuatro coeficientes
regresivos y la temperatura del ambiente, sin embargo,
a pesar del mayor nmero de parmetros y
coeficientes regresivos, este mtodo no entrega el
mayor CV cuando ambas fuentes de error son
incluidas. En efecto, el mtodo de Pauly (1980)
muestra el segundo CV ms pequeo despus del
mtodo del Jensen (1996). Esta aparente contradiccin
entre el nmero de parmetros y coeficiente del
modelo de Pauly (1980) y la magnitud del CV de M,
fue explicado por Quiroz et al. (2010) y atribuido a la
alta correlacin existente entre los parmetros de
crecimiento. Bajo la metodologa propuesta en este
artculo para incorporar incertidumbre, cuando se
remuestrean parmetros altamente correlacionados, el
resultado es la obtencin de menor variacin como es
M en el caso del modelo de Pauly (1980). Otra
particularidad del mtodo de Pauly (1980) es la
incorporacin de la temperatura del hbitat, que en el
caso de la columna de agua y las profundidades donde
habita el congrio dorado, podran ser consideradas
invariable. Esto es particularmente importante ya que
se conoce que esto puede ser un factor clave en la
determinacin de M (Brown et al., 2004).
La propuesta del mtodo emprico ms adecuado,
depende de la calidad de los parmetros que alimentan
los mtodos empricos y la naturaleza matemtica de
estos. El mtodo de Jensen (1996) podra estar
sesgado para la determinacin de M, debido a que la
edad de madurez proviene de la madurez a la longitud
reportada por Aguayo et al. (2001) en individuos de
congrio dorado capturados en toda la extensin
geogrfica de la zona sur-austral, sin hacer ningn tipo
de distincin geogrfica en trminos de stock como
fue recomendado por Wiff et al. (2006). Por otro lado,
el mtodo de Hoenig (1983) utiliza la longevidad
mxima derivada de la talla asinttica, posiblemente
introduciendo un sesgo o un error adicional al
considerar una relacin funcional emprica entre la
longevidad y la longitud asinttica. As mismo, el
mtodo de Frisk et al. (2001) fue inicialmente
propuesto para elasmobranquios. Sin embargo, Quiroz
et al. (2010) sealan que especies de elasmobranquios
y peces telesteos comparten la misma dependencia de
M con los parmetros de crecimiento, lo que posibilita
el empleo de mtodos empricos desarrollados para
peces telesteos en poblaciones de elamosbranquios y
viceversa. De todas formas, la no especificidad del
mtodo de Frisk et al. (2001) exclusivamente para
telesteos podra causar que este mtodo muestre las
mayores estimaciones de M.
Por ltimo, bajo los argumentos descritos en el
prrafo anterior, se recomienda considerar las
 Lat. Am. J. Aquat. Res.
estimaciones del mtodo de Pauly (1980) como las
menos sesgadas para congrio dorado a travs de sexos
y zonas de pesca. En este contexto, las estimaciones
del mtodo de Pauly (1980) que incorporan ambos
errores (rasgos y coeficientes) sugieren emplear, ya
sea en modelos poblacionales o anlisis de
sobrevivencia, los siguientes valores de M: 0,33 ao-1
(IC: 0,17-0,57) para machos zona norte, 0,30 ao-1
(IC: 0,15-0,52) para machos zona sur, 0,26 ao-1 (IC:
0,13-0,47) hembras zona norte y 0,24 ao-1 (IC: 0,12-
0,43) hembras zona sur. Mientras que para sexos
conjuntos se sugiere utilizar 0,27 ao-1 (IC: 0,13-0,47)
para la zona norte y 0,23 ao-1 (IC: 0,11-0,40) para la
zona sur. Estas estimaciones son similares a las
reportadas para toda la zona sur-austral por medio de
mtodos empricos, como aquellas estimadas por
Aguayo et al., (1986) con valores de 0,35 ao-1 para
machos y 0,23 ao-1 para hembras, mientras que Ojeda
et al. (1986) calculan valores de 0,28 ao-1 y 0,25
ao-1 para machos y hembras respectivamente.
Investigaciones recientes orientadas a explorar la
estructura ecosistmica (Arancibia et al., 2003), como
tambin, el modelamiento multiespecie para la zona
sur-austral (Arancibia et al., 2010), han empleado el
valor de M = 0,26 ao-1 utilizado en las ms recientes
evaluaciones de stocks (Wiff & Quiroz, 2010), el que
ha sido adoptado de las estimaciones de Aguayo et al.
(1986) realizadas hace ms de una dcada. Por tanto,
es fehaciente que la actualizacin de los valores de M
en congrio dorado y su incertidumbre, ya sea por
gnero o rea de distribucin, viene a precisar los
resultados de investigaciones que emplean este
parmetro.
La tarea de comparar los mtodos empricos, ya
sea por la naturaleza de sus coeficientes o la
certidumbre en los parmetros de historia de vida, no
solamente obedece a la seleccin de un mtodo
consistente con los rasgos demogrficos y dinmica
poblacional de congrio dorado, sino tambin, por a las
consecuencias que conlleva una inadecuada
especificacin de M en los modelos de evaluacin de
stock. Ultang (1977) explor la sensibilidad de los
resultados del anlisis de poblacin virtual (APV) a un
conjunto de escenarios de variabilidad de M. Los
resultados fueron concluyentes en indicar que
imprecisiones de M en torno a un 50% deben
ocasionar sesgos del orden de 20% en las estimaciones
de la mortalidad por pesca. En este mismo sentido,
otras investigaciones han mostrado que la variabilidad
temporal de M incrementa de forma importante la
variabilidad de los reclutamientos estimados en el
contexto de un modelo edad-estructurado (Lapointe et
al., 1992; Aanes et al., 2007). En este sentido, evaluar
el nivel de sensibilidad de las estimaciones de
324
mortalidad natural es claramente esencial y la
incorporacin de las diferentes fuentes de
incertidumbre en la evaluacin de stock es, por tanto,
altamente deseable. Las estimaciones de M y sus
intervalos de confianza, en el caso de congrio dorado,
pueden ser incorporadas en los modelos de evaluacin
de stock y propagadas a las estrategias de manejo. Lo
ms comn es el anlisis de sensibilidad, donde una
evaluacin de stock es realizada repetidamente para
varios valores de M obtenidos desde los intervalos de
confianza (Quiroz et al., 2011). Una segunda va es
utilizar una aproximacin bayesiana configurando una
distribucin emprica de M en base a sus intervalos de
confianza y utilizarla como distribuciones a priori
(McAllister et al., 1994; Patterson, 1999). Finalmente,
la incertidumbre de M tambin puede ser incluida en
modelos estado-espacio, donde el error en M puede ser
incorporado como una de las componentes aleatorias
(error de proceso) que regulan la estocasticidad en la
dinmica poblacional (Millar & Meyer, 2000).
Este estudio evidencia que los estimados de M para
una determinada zona son diferentes entre sexos,
como tambin para sexos conjuntos entre zonas de
pesca. Para una zona dada, los machos presentan
mayores estimados de M que las hembras. Cuando se
compara entre zonas, los individuos de la zona norte
presentan mayor mortalidad que los provenientes de la
zona sur. Esto obedece a que los individuos de la zona
norte para un sexo dado, son ms pequeos a una edad
especfica (Wiff et al., 2007), haciendo que k sea
mayor. A su vez k es directamente proporcional a M
(Charnov, 1993), causando que en la zona norte se
obtengan mayores estimados de M que en la zona sur.
Las notorias diferencias de las magnitudes de
mortalidad natural por zona de pesca apoya la
diferenciacin de stock sugerida por Wiff et al. (2005)
y entregan elementos para profundizar en el concepto
de stock pesquero del congrio dorado en la zona sur-
austral. En este contexto, el primer antecedente sobre
la identificacin de unidades de stock en esta especie
fue realizado por Chong (1993) en base a un anlisis
morfomtrico de los otolitos. El resultado de este
anlisis mostr que an cuando las variables
morfomtricas presentan diferencias importantes entre
zona norte y sur, existe una importante sobreposicin
de los grupos etreos que impide considerarlos como
unidades discretas. Sin embargo, este estudio no fue
concluyente respecto a la determinacin de una o ms
unidades de stock, sugiriendo la necesidad de
incorporar otras tcnicas ms precisas de anlisis.
El comportamiento de especies pertenecientes al
gnero Genypterus sugiere una tendencia a conformar
mltiples poblaciones, las que pueden ser
consideradas administrativamente unidades de stock
325 Mortalidad natural en congrio dorado, zona sur-austral de Chile
independientes. Esta independencia en los stocks ha
sido confirmada en reas de pesca extranjeras
comparativamente menores que la zona sur-austral. En
este contexto, Wiff et al. (2005) reunieron
antecedentes biolgico-pesqueros, como crecimiento,
tallas medias, proporcin sexual, que avalan la
existencia de caractersticas demogrficas diferentes
para congrio dorado entre diferentes reas de la zona
sur-austral. Posteriormente, Wiff et al. (2007)
presentaron un anlisis detallado de los parmetros de
crecimiento, indicando que existen diferencias
estadsticas en el crecimiento entre la zona sur y norte.
En un trabajo ms reciente, Brito et al. (2008)
efectuaron un anlisis por medio de redes neuronales y
caracteres morfomtricos sugiriendo diferenciacin
geogrfica dentro de la zona sur-austral. Estos autores
adems, sealaron que los resultados son concordantes
con aquellos encontrados por Chong (1993).
Recientemente, Canales-Aguirre et al. (2010),
emplearon tcnicas de microsatelites para determinar
la variabilidad gentica y estructura poblacional del
congrio dorado en tres subzonas de la zona sur-austral
de Chile. Los resultados indicaron que no existe
diferenciacin gentica a nivel de poblacional para la
zona comprendida entre los 41 y 57S. Sin embargo,
el bajo contraste entre las muestras recopiladas en la
zona norte y sur, en concomitancia con el bajo poder
estadstico de las pruebas empleadas, dejan
importantes interrogantes sobre estos resultados y las
conclusiones sobre la existencia de ms de un stock de
congrio dorado para la zona sur-austral. El presente
trabajo complementa los vacos de conocimiento
respecto a la historia de vida de congrio dorado, y de
paso mejora la evaluacin de stock por zonas de
administracin en trminos de precisin y sesgo.
AGRADECIMIENTOS
Este trabajo fue financiado por el proyecto
Investigacin del estatus y evaluacin de estrategias
de explotacin en congrio dorado 2011, realizado por
el Instituto de Fomento Pesquero. Se desea agradecer
a dos revisores annimos cuyos comentarios
enriquecieron la versin final de este manuscrito.
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 Autofecundacin
Lat. Am. J. Aquat. Res., 39(2): 327-337, 2011 y malformacin larval en ostin Argopecten purpuratus 327
DOI: 10.3856/vol39-issue2-fulltext-14

Research Article

Asociacin entre la tasa de autofecundacin y la frecuencia de larvas

malformadas en poblaciones cultivadas del ostin del norte Argopecten
purpuratus (Lamarck, 1819)

Christopher Concha1, Emilio Figueroa1 & Federico M. Winkler1, 2

1
Departamento Biologa Marina, Facultad de Ciencias del Mar, Universidad Catlica del Norte
P.O. Box 117, Coquimbo, Chile
2
Centro de Estudios Avanzados en Zona ridas (CEAZA), Universidad Catlica del Norte
P.O. Box 117, Coquimbo, Chile

RESUMEN. El incremento de la frecuencia de malformaciones y la reduccin de la viabilidad y fecundidad

suelen ser las primeras manifestaciones de la depresin por consanguinidad en animales. El ostin del norte,
Argopecten purpuratus (Lamarck, 1819), es una especie hermafrodita funcional con autofecundacin parcial y
durante la reproduccin artificial puede presentar altos grados de autofecundacin. En este trabajo se analiz la
asociacin de la tasa de autofecundacin con la frecuencia de larvas malformadas y la supervivencia larval. Se
desovaron adultos maduros y se recogieron separadamente los gametos femeninos del 5 pulso de liberacin
en adelante y los masculinos. Los ovocitos fueron fecundados con espermatozoides de otro individuo,
formando familias de hermanos completos. La tasa de autofecundacin se verific por la proporcin de
ovocitos que entra en divisin en una muestra de ellos sin fecundar. La tasa de autofecundacin vari entre
familias de 0 a 100%, con distribucin de frecuencias normal. La proporcin de larvas malformadas se
distribuy al azar entre las familias analizadas, pero se correlacion negativamente, en forma moderada pero
significativa, con la tasa de autofecundacin y la temperatura media del cultivo. Los datos sugieren que la
autofecundacin en las familias de ostiones puede favorecer una mayor homeostasis del desarrollo larval.
Palabras clave: depresin por consanguinidad, pectnidos, hermafroditismo, homeostasis del desarrollo,
Argopecten purpuratus.

Association between self-fertilization rates and the frequency of malformed larvae in

farmed populations of the northern scallop Argopecten purpuratus (Lamarck, 1819)

ABSTRACT. Increased frequencies of malformations and the reduction of viability and fecundity are some of
the first manifestations of inbreeding depression in animals. The northern scallop, Argopecten purpuratus
(Lamarck, 1819), is a functional hermaphrodite species with partial self-fertilization. During artificial
reproduction, this species may present high degrees of self-fertilization. In this work, the association between
the selfing rate and the frequency of larval malformations and survival were analyzed. Mature adults were
spawned, and female and male gametes were collected separately from the fifth or later spawning pulses.
Oocytes were fertilized with sperm from another individual, forming families of complete siblings. Selfing
rates were verified by the proportion of cleaving oocytes in a non-fertilized sample. Self-fertilization ranged
from 0 to 100% among families, with a normal distribution. The proportion of malformed larvae was
distributed randomly among the families analyzed, but was negatively correlated moderately but
significantly with the selfing rate and the mean water temperature of the culture. These results suggest that
self-fertilization in scallop families can favor greater homeostasis of larval development.
Keywords: inbreeding depression, pectinids, hermaphroditism, developmental homeostasis, Argopecten
purpuratus.

___________________
Corresponding author: Federico Winkler (fwinkler@ucn.cl)
328 Lat. Am. J. Aquat. Res.
INTRODUCCIN
La consanguinidad o endogamia es un factor relevante
en el proceso de cambio de las frecuencias genotpicas
en una poblacin. En muchas especies con
reproduccin cruzada causa prdida en el valor de
parmetros vinculados con la adecuacin biolgica y
la produccin, conocida como depresin por
consanguinidad (Falconer & Mackay, 1996; Lynch &
Walsh, 1998). Este fenmeno ha sido ampliamente
informado para especies de plantas y animales
(Charlesworth & Charlesworth, 1979, 1987; Lande &
Schemske, 1985, 1987; De Rose & Roff, 1999;
Crnokrak & Roff, 1999; Lens et al., 2000; Wang et
al., 2002), incluido diversas especies de moluscos,
donde el incremento de la endogamia suele
manifestarse en una disminucin de las tasas de
crecimiento, mayor mortalidad o incremento de
frecuencia de malformaciones, entre otros (Beaumont,
1986; Evans et al., 2004; Deng et al., 2005; Ibarra et
al., 1995; Park et al., 2006; Martnez et al., 2007;
entre otros).
La consanguinidad se produce por el cruzamiento
entre individuos que estn ms emparentados entre s
que el promedio de la poblacin (Falconer & Mackay,
1996; Martnez & Figueras, 2007), y tiene su mxima
expresin en la autofecundacin. Esta es comn en
una gran variedad de plantas hermafroditas
(Charlesworth & Charlesworth, 1979), donde, sin
embargo, se han descrito evidencias de adaptaciones
que involucran sistemas que promueven la
exofecundacin (Charlesworth & Charlesworth,
1987). En animales, y particularmente en moluscos,
existen diversas especies hermafroditas, como ostras
(Murakoshi & Hirata, 1993; Evans et al., 2004),
caracoles de tierra (Ruppert & Barnes, 1996), entre
otros. Sin embargo, muchas de esas especies tambin
exhiben mecanismos que previenen la autote-
cundacin, como la alternancia de sexos (Ruppert &
Barnes, 1996; Calvo et al., 1998), mecanismos
eficientes de dispersin de gametos, sincronizacin de
desoves e incompatibilidad gamtica, entre otros
(Knowlton & Jackson, 1993).
En los moluscos pectnidos existe un gran nmero
de especies hermafroditas funcionales, cuyos
miembros poseen una gnada dividida en una porcin
masculina y otra femenina (Ruppert & Barnes, 1996;
Calvo et al., 1998). En varios de ellos se ha informado
la maduracin sincrnica de ambas porciones de la
gnada y desoves simultneos (Guzmn et al., 1998).
As, en el ostin del norte, Argopecten purpuratus
(Lamarck, 1819), se han registrado tasas de
autofecundacin que varan entre 0 y 100%, con
promedios en torno al 10 y 20%, durante desoves en
ambiente controlado (Winkler & Estvez, 2003; Toro
et al., 2009). En A. purpuratus y otros bivalvos, como
Pecten maximus, Placopecten magellanicus y
Crassostrea gigas, el proceso de desove se inicia
cuando los ovocitos pasan de la profase I a la metafase
I, seguido de la ruptura de la vescula germinal y su
liberacin al medio (Widoeati et al., 1995; Dsilets et
al., 1995; Kyosuka et al., 1997; Martnez et al., 2000).
Cuando el ovocito se encuentra en metafase I puede
ser fecundado por los espermatozoides y, en
pectnidos, al ser evacuados ambos tipos de gametos
por una va comn, es posible la autofecundacin en el
tracto genital (Mackie, 1984; Widoeati et al., 1995).
As, la autofecundacin durante el desove es
considerado un fenmeno comn en pectnidos
hermafroditas (Beaumont, 1986; Benninger & Le
Pennec, 1991; Ibarra et al., 1995). En cultivos
artificiales, donde los reproductores son confinados a
pequeos volmenes de agua, se presume que la
autofecundacin sera mayor que en la naturaleza,
pero no hay estimaciones de las tasa de
autofecundacin en el medio natural.
El efecto del incremento en la consanguinidad
derivado de la autofecundacin ha mostrado
resultados discrepantes entre estudios en pectnidos.
Algunos autores han informado evidencias de
depresin por consanguinidad, con supervivencias o
crecimientos menores en larvas producidas por
autofecundacin que los controles producidos por
fecundacin cruzada (Beaumont, 1986; Ibarra et al.,
1995; Martnez et al., 2007; Zheng et al., 2008; Toro
et al., 2009, 2010). Otros, en cambio, no han
encontrado evidencias de ello (Betancourt et al., 1994;
Winkler & Estvez, 2003).
El incremento de las malformaciones durante la
etapa de desarrollo es una de las primeras
manifestaciones de la depresin por consaguinidad
(Evans et al., 2004; Park et al., 2006). Esto se ha
observado en larvas de organismos marinos, como
abalones (Deng et al., 2005; Park et al., 2006), ostras
(Evans et al., 2004; Naciri-Graven et al., 2000) y
peces (Lu & Bernatchez, 1999; Wang et al., 2002),
entre otros. Tericamente, este fenmeno se asocia
con prdida de homeostasis de desarrollo, es decir, la
capacidad para compensar eficientemente los efectos
adversos del ambiente para desarrollar en forma
precisa el plan ontogentico contenido en el genoma
de los individuos, en un ambiente determinado
(Waddington, 1953, 1957; Dobzhansky & Wallace,
1953; Dobzhansky, 1955; Thoday, 1958; Nijhout &
Davidowitz, 2003). As, la mayor frecuencia de
malformaciones en una poblacin se vincula con
menores niveles de adecuacin biolgica (Evans et al.,
2004; Deng et al., 2005).
 Autofecundacin y malformacin larval en ostin Argopecten purpuratus
La presencia de larvas malformadas durante la
reproduccin artificial de Argopecten purpuratus ha
sido descrita por Avendao et al. (2001), quienes
consideran este factor como un problema en la
produccin de semillas de esta especie. Hasta el
presente no existe un anlisis de la variacin en la tasa
de malformaciones entre poblaciones de ostiones ni
una explicacin sobre sus posibles causas.
Considerando que las malformaciones son una
manifestacin frecuente de la depresin por
consanguinidad, y que durante la reproduccin
artificial de esta especie se producen grados variables
de autofecundacin, puede presumirse que ambos
fenmenos estn conectados. As, en este trabajo se
intenta verificar si la frecuencia de malformaciones en
las larvas es una consecuencia de la consanguinidad
derivada de la autofecundacin que se produce durante
la reproduccin artificial.
MATERIALES Y MTODOS
Se obtuvieron al azar reproductores maduros de una
poblacin de ostiones de cultivo provenientes de
captacin natural de baha Tongoy, los que fueron
trasladados al Laboratorio Central de Cultivos de la
Universidad Catlica del Norte, Sede Coquimbo. Con
ellos se establecieron 91 familias, por fecundacin
cruzada, y en cada una de ellas se estim la tasa de
autofecundacin, frecuencia de malformaciones y
mortalidad. Los experimentos se realizaron entre el 3
de julio del 2008 y 14 de enero del 2009.
Desove y obtencin de gametos
Adultos maduros fueron estimulados para inducir a
desove utilizando la metodologa descrita por Di Salvo
et al. (1984), recogiendo independientemente los
gametos masculinos y femeninos, cada uno de un
grupo diferente de ejemplares. Esta especie
normalmente libera sus gametos en pulsos, inicindose
el desove con la evacuacin de espermatozoides,
seguido, entre 10 y 20 min despus, por los ovocitos
(Martnez et al., 2007). El cambio de sexo fue
monitoreado por observacin del color del rin. Este
es observable por delante del msculo aductor al
separar las valvas del reproductor, y adquiere un color
blanco lechoso durante la expulsin de los
espermatozoides, cambiando a un color rojo
anaranjado al iniciar la liberacin de ovocitos
(Winkler & Estvez, 2003). Los espermatozoides se
recogieron en cubetas con agua filtrada a 1 y
esterilizada con luz UV, retirando los individuos del
recipiente antes de iniciarse el cambio en el tipo de
gametos liberados. Para la recoleccin de ovocitos se
dej que los individuos concluyesen de emitir gametos
329
masculinos, se los retir del recipiente en que estaban,
lavndolos cuidadosamente con agua filtrada y
esterilizada con UV, y se los coloc en un recipiente
con agua de mar fresca. Los primeros cinco pulsos de
emisin de ovocitos fueron descartados para prevenir
un exceso de autofecundacin. Para ello, luego de
emitir cada pulso de gametos, el reproductor fue
retirado del recipiente, lavado en la forma descrita
previamente y colocado en un nuevo recipiente con
agua fresca, segn el procedimiento descrito por
Winkler & Estvez (2003).
Previo a realizar la fecundacin cruzada, se separ
una muestra de 1 mL de agua desde el recipiente
conteniendo los ovocitos, la que se incub a
temperatura ambiente (aprox. 16C) por 4 h. Al cabo
de este tiempo se observ bajo microscopio, para
verificar la presencia de zigotos en divisin, productos
de autofecundacin (Winkler & Estvez, 2003) y se
obtuvieron tres fotos del desove de cada hembra con
una cmara fotogrfica digital Canon Power Shot A
620 adosada a un microscopio. Se examinaron 70
ovocitos/cigotos por hembra desovada, y la tasa de
autofecundacin se expres como el porcentaje de
cigotos en divisin sobre el total de ovocitos
analizados.
El incremento en el coeficiente de consanguinidad
(F) para cada familia durante el proceso de
reproduccin artificial se estim como:
F = (1 - C)/2
donde C es la proporcin de individuos producidos
por exofecundacin en la poblacin (Winkler &
Estvez, 2003). El incremento de consanguinidad
derivado del grado de parentesco entre los individuos
que se cruzan se consider despreciable para los
efectos de este experimento, dado que los
reproductores se obtuvieron al azar de una poblacin
silvestre (Tongoy) compuesta por ms de 60 millones
de individuos, de los cuales se estima que un 20%
seran adultos (S. Cortez, com. pers.), y los cruces se
hicieron al azar. As, la consanguinidad derivada de
este factor debera ser, en promedio, la misma que en
la poblacin base.
La fecundacin se realiz usando una proporcin
aproximada de 10 espermatozoides por ovocito. Cada
familia fue dispuesta en un estanque de 200 L
independiente, con agua de mar filtrada a 1 y
esterilizada con luz UV. El cultivo larval se realiz a
temperatura ambiente, con recambio completo de agua
cada dos das y aeracin constante a partir de las 48 h.
Se aliment a diario con 10 L de Isochrysis galbana
var. tahiti (2,5 x 104 cel mL-1) por estanque. La
densidad de larvas vari de ~12 larvas mL-1 al inicio
del cultivo, a ~1 larva mL-1 al final de ste. La
330 Lat. Am. J. Aquat. Res.
temperatura del agua de los estanques fue registrada
tres veces al da (maana, medioda y tarde) con un
termmetro (0,1C).
Durante el cambio de agua las larvas se retuvieron
en un tamiz de 45 m, y de l se colectaron muestras
de larvas siguiendo la metodologa descrita por Di
Salvo et al. (1984), las que fueron almacenadas en
tubos Eppendorf de 1,5 mL con formalina al 5% hasta
su anlisis. La supervivencia y la frecuencia de larvas
malformadas por familia se evalu al segundo da
post-fecundacin, a la mitad y al final del perodo de
cultivo. Para compensar eventuales variaciones en las
tasas de desarrollo causadas por diferencias en la
temperatura de cultivo (Ruiz et al., 2008), la segunda
medicin se hizo cuando las larvas alcanzaron las
251,7 Unidades Trmicas Acumuladas (UTA)
(Brenko & Calabrese, 1969; Uki & Kikuchi, 1984;
Prez, 2002; Gallegos, 2003; Gonzlez, 2003). La
mortalidad se estim por la diferencia en la cantidad
de larvas entre periodos sucesivos de medicin. Para
ello se cont bajo lupa el nmero de larvas vivas en
una alcuota de 1 mL de la muestra obtenida del tamiz,
y se extrapol al volumen total del estanque. El alto de
las larvas se midi a partir de imgenes digitales
obtenidas con un microscopio de transmisin dotado
con cmara fotogrfica, y usando el programa Image-
Pro Plus 4.0, calibrado para que las medidas fuesen
registradas en micrmetros.
La presencia de malformaciones se verific
mediante observacin bajo microscopio y registro
microfotogrfico de 50 larvas tomadas al azar por
familia, para cada etapa del cultivo definida
previamente. Como criterios para definir la
manifestacin de alteraciones en el desarrollo se
usaron las descripciones de la morfologa normal de
las larvas de A. purpuratus de Bellolio et al. (1994) y
de las deformaciones informadas por Avendao et al.
(2001).
Anlisis de los datos
La asociacin de la frecuencia de larvas malformadas
por familia con el porcentaje de autofecundacin o la
temperatura promedio del agua del cultivo, y la
relacin entre el porcentaje de autofecundacin y la
mortalidad larval en cultivo, se examinaron mediante
anlisis de regresin simple (Yi = + Xi). La
significancia de los coeficientes de regresin fue
verificada mediante una prueba t-Student (Sokal &
Rolf, 1981).
La distribucin de frecuencias de larvas
malformadas entre familia se compar con una
distribucin de Poisson, usando la prueba de Chi-
cuadrado para bondad de ajuste como prueba de
hiptesis. Los porcentajes de autofecundacin para las
familias se analizaron con una prueba de Kolmogorov-
Smirnov. La proporcin promedio de larvas
malformadas al inicio y a mediados del cultivo fueron
analizadas utilizando una prueba t-Student, para
verificar si exista diferencia entre ellos.
RESULTADOS
De las 91 familias formadas en siete eventos de
reproduccin (Tabla 1), slo 20 de ellas (22%)
alcanzaron el estadio de pediveliger, etapa en que se
inicia el proceso de fijacin, la cual se alcanz en 20 a
22 das de cultivo, dependiendo de la temperatura de
cultivo. Sesenta y dos familias (68%) sobrevivieron
hasta la etapa media del desarrollo larval. La
proporcin de larvas vivas promedio por familia
mostr una marcada cada a lo largo del cultivo, con
una reduccin de aproximadamente el 80% entre la
primera y segunda medicin, y slo el 5% de las
larvas de cada familia sobrevivi hasta el final del
cultivo (Fig. 1).
La tasa de autofecundacin vari de 0% a 100%
entre las familias, con un promedio general de 43%, y
distribucin normal (P > 0,05). El 19% de las familias
no present autofecundacin (F = 0) pero en un 17%
de ellas todas los cigotos producidos provienen de
autofecundacin (F = 50%) (Fig. 2). As, el
incremento de la consanguinidad promedio estimado
durante el proceso artificial de reproduccin fue de
21,5%. La longitud de las larvas al inicio del cultivo
vari entre 92 y 102 m, con un promedio de 98 3
m, alcanzando 207 9 m a la edad de fijacin (Fig.
3), con una tasa de crecimiento de 4,1 m da-1.
A las 48 h post-desove todas las larvas se
encontraron en estadio de veliger, con una concha de
forma semicircular con bordes regulares (Fig. 4a). A
mediados del cultivo esta forma se ha modificado
levemente para adoptar la tpica forma de larva D (Fig.
4c). En algunas larvas se observ una hendidura muy
marcada en el contorno de la concha, caracterstica
que se registr tanto a inicios (Fig. 4b) como a
mediados del cultivo (Fig. 4d). La proporcin de
larvas con esta malformacin vari entre las familias
de 0 a 12% al inicio, y de 0 a 10% mediados del
cultivo, con promedios de 4 y 3%, respectivamente (P
> 0,05). En la ltima medicin todas las larvas
observadas se encontraron en estadio de pedivelger,
con conchas de forma semicircular (Fig. 4e), y no se
observaron individuos con morfologas alteradas. La
distribucin de frecuencias de larvas malformadas
entre las familias fue al azar, tanto al inicio como a
mediados del cultivo (P > 0,05; Fig. 5).
 Autofecundacin y malformacin larval en ostin Argopecten purpuratus 331

Tabla 1. Temperatura promedio del agua ( DE) en estanques de cultivo de larvas de Argopecten purpuratus en tres
etapas del cultivo, para siete eventos de reproduccin.
Table 1. Mean water temperature in culturing tanks ( SD) with Argopecten purpuratus larvae at three moments of the
larval life span in seven culture batch.

Temperatura del cultivo (C)

Desove Fecha
Inicio Mediados Final Promedio
1 03/11/2008 17 ( 1,0) 17 ( 0,7) 17 ( 0,8)
2 14/11/2008 17 ( 0,6) 17 ( 0,6)
3 25/11/2008 17 ( 0,7) 18 ( 0,7) 18 ( 0,7)
4 09/12/2008 19 ( 1,0) 20 ( 0,6) 20 ( 0,6) 20 ( 0,7)
5 06/01/2009 19 ( 0,6) 19 ( 0,7) 19 ( 0,6) 19 ( 0,6)
6 07/01/2009 18 ( 0,6) 19 ( 0,8) 19 ( 0,7) 19 ( 0,7)
7 14/01/2009 19 ( 0,6) 19 ( 0,6) 19 ( 0,6)
Promedio 18 ( 0,7) 19 ( 0,1) 19 ( 0,6) 18,7 ( 0,5)

Figura 1. Supervivencia relativa promedio de larvas de Figura 3. Variacin en la longitud promedio de larvas de
A. purpuratus en tres momentos del periodo de cultivo. A. purpuratus a lo largo del perodo de cultivo.
Figure 1. Average relative survivorship of A. purpuratus Figure 3. Variation in the mean shell length of A.
larvae at three moments of the larval culturing period. purpuratus larvae along of the larval cultivation period.

edades (r = 0,426 y 0,359, respectivamente; P < 0,05).

Figura 2. Incremento de la consanguinidad (F),
estimado por la proporcin de cigotos autofecundados,
en 91 familias de A. purpuratus.
Figure 2. Increment of the inbreeding (F) estimated
trough the selfing rate, in 91 families of A. purpuratus.
Las familias con tasas ms altas de
autofecundacin tendieron a tener menor proporcin
de larvas malformadas que aquellas con menor
autofecundacin, tanto en las evaluaciones realizadas
a inicios como a mediados del cultivo (Fig. 6),
aprecindose una moderada pero significativa
correlacin negativa entre ambas variables en las dos
Por su parte, la temperatura media del agua del cultivo
no se asoci significativamente con la frecuencia de
larvas con alteraciones morfolgicas a las 48 h post-
fecundacin (P > 0,05), pero si se observ una
moderada pero significativa asociacin negativa (P <
0,05) entre dichas variables en la medicin realizada a
mediados del cultivo (Fig. 7). En cambio, las tasas de
autofecundacin ni la temperatura media del agua se
asociaron con la mortalidad larval (P > 0,05).
DISCUSIN
La presencia de una hendidura muy marcada en el
contorno de la concha de las larvas a las 48 h post-
fecundacin es similar a las alteraciones descritas por
Avendao et al. (2001). Estas alteraciones persisten al
menos hasta mediados del periodo de desarrollo
larval, sugiriendo que ellas no seran letales en esta
etapa o que pueden generarse durante el crecimiento
de las larvas velger. Su ausencia al final del cultivo,
no obstante, parece indicar que estas alteraciones en la
332 Lat. Am. J. Aquat. Res.
Figura 4. Larvas de A. purpuratus. a las 48 h post-
fecundacin: a) normal, b) malformada; a las 251,7
U.T.A. de cultivo: c) normal, d) malformada; e) al final
del cultivo.
Figure 4. Larvae of A. purpuratus: after 48 h
fertilization: a) normal, b) malformed; after 251.7 U.T.A.
of cultivation; c) normal, d) malformed; e) at the end of
the cultivation period.
concha pueden asociarse con mortalidad selectiva
como proponen Avendao et al. (2001). No obstante,
por su baja frecuencia en los cultivos, menor al 12%,
este no parece ser un factor relevante en el xito de la
produccin de juveniles de ostin del norte en
sistemas controlados.
Las malformaciones morfolgicas se asocian con
alteraciones aleatorias en el patrn de desarrollo
ontogentico de los organismos (Waddington, 1957),
las que se suponen no heredables y distribuidas al azar
en la poblacin, fenmeno denominado inestabilidad
del desarrollo (ID; Palmer, 1994). Factores
ambientales pueden incidir en la frecuencia y
magnitud de la ID en las poblaciones (Markow, 1995;
Dethlefsen et al., 1996; Jezierska et al., 2000) y la
temperatura ha sido descrita como uno de ellos en
distintos organismos (Zimmerman & Pechenik, 1991;
Nomaguchi et al., 1997; Hallare et al., 2005).
Nuestros resultados muestran que el incremento de
temperatura, dentro de los rangos estudiados, tendera
a favorecer una mayor estabilidad de desarrollo en A.
purpuratus. Temperaturas ms altas aumentan las
tasas de desarrollo en moluscos (Barra et al., 2005), y
en particular en pectnidos (Tettelbach & Rhodes,
Figura 5. Distribucin de frecuencia de familias con
diferentes nmero de larvas malformadas por muestra: a)
al inicio, b) a mediados del periodo de cultivo (251,7
8,9 U.T.A.). (N = 50 larvas por familia).
Figure 5. Frequency distribution of families with
different number of malformed larvae per sample: a) at
the beginning, b) at the middle of the cultivation period
(251.7 8.9 U.T.A). (N = 50 larvae for family).
1981; Di Salvo et al., 1984; He et al., 1999), y se
puede presumir que al abreviarse ciertas etapas crticas
de la ontogenia se reduce la probabilidad de accidentes
causantes de malformaciones en los procesos de
morfognesis. No obstante, como se ha observado en
Ciona savignyi, temperaturas superiores al ptimo
para el desarrollo embrionario de la especie podran
favorecer el incremento de la ID (Nomaguchi et al.,
1997).
La frecuencia de larvas malformadas en A.
purpuratus se distribuy al azar entre familias, y se
correlacion negativamente con la tasa de
autofecundacin. Este resultado contradice los
resultados de estudios previos sobre el efecto de la
consanguinidad en especies con reproduccin cruzada,
en las que el incremento en la ID en las progenies
suele ser una de las primeras manifestaciones de la
depresin por consanguinidad (Smouse, 1986; Deng et
al., 2005; Park et al., 2006). No obstante, en
cruzamientos entre especies o poblaciones conespe-
 Autofecundacin y malformacin larval en ostin Argopecten purpuratus
Figura 6. Asociacin entre el porcentaje de
autofecundacin y frecuencia de larvas malformadas en
91 familias de A. purpuratus. a) al inicio, b) mediados
(251,7 8,9 U.T.A.) del periodo de cultivo.
Figure 6. Association between the self-fertilization
proportion and the frequency of malformed larvae in 91
families of A. purpuratus. a) at the beginning, b) the
middle (251.7 8.9 U.T.A.) of the cultivation period.
cficas genticamente divergentes (subespecies, razas
geogrficas, etc.) tambin se ha observado incremento
en las tasas de malformaciones, fenmeno conocido
como depresin por exogamia (Alibert & Auffray,
2003). En ambos casos el fenmeno se asocia a una
reduccin de la homeostasis del desarrollo (HD) de las
progenies respecto de sus parentales, es decir, de
capacidad del genoma para compensar alteraciones
causadas por el ambiente en el plan de desarrollo
ontogentico contenido en los genes de un organismo
(Wadington, 1957). La base gentica de la prdida de
HD se ha vinculado con menores niveles de
coadaptacin genmica, es decir, de la capacidad del
genoma de los individuos para actuar
coordinadamente para producir el fenotipo normal. En
el caso de la consanguinidad se atribuye al incremento
de la homocigosis y una mayor probabilidad de
expresin de alelos recesivos deletreos al estado
homocigoto (Woolf & Markow, 2003). En los cruces
exogmicos, en cambio, se producira por la
incompatibilidad entre ambos genomas parentales para
controlar eficientemente los procesos de morfognesis
individual (Alibert & Auffray, 2003).
A. purpuratus es una especie con alta fecundidad,
pero slo una proporcin muy baja de los cigotos
producidos completa su desarrollo larval, y an menos
sobreviven hasta la edad reproductiva (Di Salvo et al.,
333
Figura 7. Asociacin entre la temperatura promedio del
agua de cultivo y la frecuencia de larvas malformadas en
91 familias de A. purpuratus a mediados del periodo de
cultivo.
Figure 7. Association between the average water
temperature and the frequency of malformed larvae in 91
A. purpuratus families at the middle of the cultivation
period.
1984; Avendao et al., 2001; Winkler & Estvez,
2003; Martnez et al., 2007). Durante el desarrollo
ontogentico de A. purpuratus, la proporcin de
individuos generados por autofecundacin dentro de
familias se reduce significativamente (Toro et al.,
2009, 2010), as como la homocigosis en loci
aloenzimticos (Winkler et al., 2009), indicando la
ocurrencia de fuertes efectos selectivos contra los
ejemplares con ms alta consanguinidad dentro de la
poblacin. No obstante, si dentro de una poblacin
diferentes genotipos multiloci producen fenotipos
similarmente adaptados, mientras que otras
combinaciones genotpicas tienen menor adecuacin
biolgica relativa, en un escenario de intensa seleccin
natural sobrevivirn y se reproducirn preferentemente
los individuos con genotipos que otorguen los mejores
niveles de coadaptacin genmica, y las progenies
producidas por autofecundacin tendrn una mejor
oportunidad de reunir combinaciones allicas
ventajosas que aquellas producidas por reproduccin
cruzada al azar. La tendencia hacia menores tasas de
malformaciones en larvas de familias con mayores
niveles de autofecundacin se podra asociar al efecto
de la seleccin natural en la generacin parental y la
probabilidad que se reproduzcan en las progenies
algunos de estos genotipos particularmente ventajosos.
La consanguinidad produce desequilibrios de fase
gamtica entre loci no ligados fsicamente y favorece
la conformacin de complejos genticos particu-
larmente coadaptados (Endler, 1977, Templeton,
1986), lo que puede contribuir a acentuar este
fenmeno.
Los niveles de autofecundacin observados en este
trabajo variaron ampliamente entre individuos y, en
promedio, superan lo informado previamente para esta
334 Lat. Am. J. Aquat. Res.
especie utilizando la misma metodologa de desove y
cuantificacin (Winkler & Estvez, 2003; Toro et al.,
2009, 2010). En la reproduccin artificial de esta
especie con fines comerciales se suelen recoger
separadamente los gametos de ambos sexos y la
fecundacin se realiza usando pools de gametos de
varios reproductores (Bellolio et al., 1994), o bien se
usan cruces masivos en que un gran nmero de
reproductores desovan en un estanque y la
fecundacin ocurre espontneamente. En ambos casos,
los primeros pulsos de liberacin de ovocitos, en los
que la autofecundacin es mayor (Winkler & Estvez,
2003), no se descartan. As, es esperable que los
niveles de autofecundacin durante la reproduccin
artificial de la especie, y por lo tanto de
consanguinidad, sean mayores an que los estimados
en este trabajo. En la naturaleza, en cambio, se
presume que las tasas de autofecundacin seran ms
bajas que en cultivo (Martnez et al., 2000). Coherente
con este supuesto, los estudios de gentica poblacional
no han mostrado una tendencia hacia exceso de
homocigotos sobre mltiples loci (Von Brand &
Kijima, 1990; Galleguillos & Troncoso, 1991;
Moragat et al., 2001), sugiriendo que dentro de los
bancos naturales la reproduccin se ajustara a un
modelo panmctico. Dado que la autofecundacin
parcial no incrementa progresivamente la
consanguinidad de las poblaciones, si no que sta
alcanza un equilibrio (Falconer & Mackay, 1996), con
tasas de autofecundacin de 10%, el coeficiente de
consanguinidad al equilibrio (Feq) por esta causa ser
aproximadamente de 5% (Winkler & Estvez, 2003).
Con un 43% de autofecundacin por generacin,
como se estim en el presente trabajo, Feq 0,27,
presumiendo que dicho valor no ha sido afectado por
otros factores.
Por otra parte, en este estudio no se observ
evidencias de depresin por consanguinidad en la
supervivencia o crecimiento larval, a diferencia de lo
informado por Martnez et al. (2007) y por Toro et al.
(2010), pero consistente con lo informado por Winkler
& Estvez (2003). Estas diferencias en resultados se
han observado entre estudios con otras especies de
pectnidos hermafroditas (Beaumont & Budd, 1983;
Betancourt et al., 1994; Ibarra et al., 1995; Zheng et
al., 2008). Considerando que la magnitud de la
depresin por consanguinidad en pectnidos puede
verse afectada por el nivel de endogamia acumulado
en la poblacin estudiada (Zheng et al., 2005, 2008) y
una variada gama de factores pueden dificultar la
deteccin de diferencias verdaderas entre grupos de
individuos con diferente niveles de autofecundacin,
como la edad de los individuos (Toro et al., 2010) o la
varianza de los datos, la constatacin de depresin por
consanguinidad en una especie es particularmente
significativa. Lo que destaca este trabajo, sin embargo,
es que en una especie con autofecundacin parcial, los
efectos negativos de la consanguinidad en algunos
rasgos, podran ser balanceados por efectos positivos
en otros.
AGRADECIMIENTOS
Los autores agradecen a quienes brindaron su apoyo
tcnico en el trabajo, Johanna Tamayo, Janette Aliaga
y Miguel Rivera; a William Faras, Manuel Carmona y
Ricardo Garca por su apoyo en las labores de cultivo
larval; al Prof. Hctor Flores por las fructferas
discusiones y al Biol. Sergio Cortez (SERNAPESCA)
por la informacin sobre el banco de Tongoy. Trabajo
parcialmente financiado por el Proyecto INNOVA
05CR11PPT-18.
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DOI: 10.3856/vol39-issue2-fulltext-15

Research Article

Use of antioxidants on rainbow trout Oncorhynchus mykiss (Walbaum, 1792)

sperm diluent: effects on motility and fertilizing capability

Andrea Ubilla1 & Ivn Valdebenito1

1
Universidad Catlica de Temuco, Facultad de Recursos Naturales
Escuela de Acuicultura. P.O. Box 15-D, Temuco, Chile

ABSTRACT. The present investigation determined how different antioxidants incorporated into the sperm
diluent for cold storage of semen affected sperm motility and spermatozoan fertility capabilities of the rainbow
trout. For the evaluations, fresh semen (C) and semen that had been stored without diluents (T1) were used as
control groups. The diluents were prepared using a base of UCT diluents (T2), adding grape polyphenol (0.1 g
100 mL-1) (T3), trolox C (0.1 g 100 mL-1) (T4), polyphenol (0.1 g 100 mL-1) plus trolox (0.1 g 100 mL-1) (T5),
and vitamin C (0.018 g 100 mL-1) (T6). The incorporation of antioxidants into sperm diluents prolongs
motility and fertility of rainbow trout semen. The results show that by day two, all of the treatments showed
level 5 sperm motility. After seven days of storage, only T3 and T6 dropped to level 4 sperm motility. The
duration of flagellate activity on this day was maximal for T3 with 36.87 0.51 s and minimal for T6 with
29.78 0.52 s. On day seven, fertility was maintained with no statistically significant differences between the
control and T2 (92.80 0.62%), T3 (83.66 2.52%), T4 (90.46 1.60%), T5 (83.57 2.75%), and T6 (83.57
2.30%). By days 10 and 17 of storage, the fertility of T1 was zero and that of T2 was significantly lower
than the control group. On day 17, the highest percentage of fertilization was 97.38 1.85% for T5 and the
lowest value was 64.69 3.76% for T2. The results allow concluding that the sperm viability of semen stored
with different antioxidants is significantly prolonged.
Keywords: Oncorhynchus mykiss, polyphenol, trolox C, vitamin C, fertilizing capability, sperm motility.

Uso de antioxidantes en el diluyente espermtico para trucha arcoiris Oncorhynchus

mykiss (Walbaum, 1792): efecto en la motilidad y capacidad fecundante

RESUMEN. En la presente investigacin se determin el efecto en la motilidad espermtica y la fertilidad del

espermatozoide de trucha arcoiris, de diferentes antioxidantes incorporados en el diluyente espermtico para el
almacenamiento en fro de semen. Para las evaluaciones se utiliz como control semen fresco (C) y semen
almacenado sin diluir (T1), los diluyentes fueron preparados utilizando como base el diluyente UCT (T2) al
que se le incorpor polifenol de uva (0,1 g 100 mL-1) (T3), trolox C (0,1 g 100 mL-1) (T4), polifenol ms
trolox (0,1 g 100 mL-1 + 0,1 g 100 mL-1), respectivamente (T5) y vitamina C (0,018 g 100 mL-1) (T6). La
incorporacin de antioxidantes en los diluyentes espermticos, prolongan la motilidad y fertilidad del semen
de trucha arcoiris. Los resultados muestran que al da dos todos los tratamientos presentaban un nivel 5 de
motilidad. Despus de 7 das de almacenamiento, slo T3 y T6 bajaron a un nivel 4 de motilidad. La duracin
de la actividad flagelar en este da fue mxima en T3 con 36,87 0,51 s y mnima en T6 con 29,78 0,52 s.
Al da 7 la fertilidad se mantuvo sin diferencias estadsticamente significativas con el control en T2 (92,80
0,62%), T3 (83,66 2,52%), T4 (90,46 1,60%), T5 (83,57 2,75%) y T6 (83,57 2,30%). Los das 10 y 17
de almacenamiento, la fertilidad de T1 fue cero y la de T2 fue significativamente menor al control. Al da 17 el
mayor porcentaje de fecundacin fue de 97,38 1,85% para T5 y el menor valor fue de 64,69 3,76% para
T2. Los resultados permiten concluir que el semen almacenado con distintos antioxidantes prolonga
significativamente la viabilidad espermtica.
Palabras clave: Oncorhynchus mykiss, polifenol, trolox C, vitamina C, capacidad fecundante, motilidad
espermtica.
___________________
Corresponding author: Andrea Ubilla (cubilla@uct.cl)
339 Use of antioxidants in rainbow trout Oncorhynchus mykiss sperm diluents
INTRODUCTION
Sperm extender diluents improve motility and
fertilization percentages of cold stored semen (Stoss,
1983; McNiven et al., 1993; Billard, 1990; Snchez &
Rubilar, 2001; Valdebenito et al., 2009). These
solutions prevent the oxidization of the plasmatic and
mitochondrial membrane, delivering energetic
substrates and allowing the maintenance of sperma-
tozoa at stable pH and osmolarity conditions of the
extracellular mediums (Morisawa & Susuki, 1980;
Morisawa et al., 1983; Batellier et al., 2001). Gametes
are aerobic cells where oxygen plays an essential role
for their performance. Oxygen free radicals are
continuously generated in the different metabolic
pathways, and are capable of interacting with different
biomolecules, causing cell damage. Oxidative stress is
a consequence of the unbalance produced between the
production of free radicals and the anti oxidizing
capabilities of an organism, where this can become
very harmful if there is a high production of oxygen
reactive species (ORS) (Saleh et al., 2002; Membrillo
et al., 2003).
In mammals, sperm motility can become seriously
affected by ORSs. At a molecular level they can
obstruct the phosphorylation of proteins, preventing
sperm movement (De Lamirande et al., 1998).
Reactive species also exist, that are produced naturally
by the cell, these are in low concentrations intervening
in processes like capacitation, acrosomic reaction and
the union of the spermatozoa to the pellucid zone
(Sharman & Agarwal, 1996; De Lamirande et al.,
1997, 1998; Aitken et al., 2004; Allamaneni et al.,
2004).
Antioxidants are molecules that prevent the
uncontrolled production of free radical or inhibit their
reactions with biological structures (Halliwell &
Chirico, 1993). In seminal plasma and in spermatozoa
of teleostei fish there are different types of
antioxidants (Liu et al., 1995; Ciereszko et al., 2000;
Lahnsteiner et al., 2010a), which are important for the
in vivo maintenance of sperm viability, and that could
have relevance for the practice of supplementation of
the semen storage and cryopre-servation mediums to
improve the quality of the spermatozoa. Ascorbic acid
(Ciereszko & Dabrowski, 1995; Metwally & Fouad,
2009) and Uric acid (Ciereszko et al., 1999) are
considered important antioxidants in teleostei semen.
In rainbow trout and carp semen, methionine sulfoxide
reductase and methionine can have antioxidant
functions (Lahnsteiner, 2009).
Experimentally, to reduce the levels of ORS in
mammals, ascorbic acid and/or catalase have been
added to sperm extender diluents, where satisfactory
results have been obtained (Ball et al., 2001a), since
the enzymes present in seminal plasma are not always
efficient enough to reduce the effects of ORSs
(Lamirande et al., 1997; Peeker et al., 1997).
The objective of this present investigation was to
evaluate the effects of the incorporation of three
antioxidants applied to semen of rainbow trout
(Oncorhynchus mykiss) during cold storage for 17
days.
MATERIALS AND METHODS
Gamete recollection and semen storage
To simulate the conditions of the fish farms, a pool
of semen was uses (1 mL per male and six ml total)
with maximum motility was obtained from six adult
male rainbow trouts (Oncorhynchus mykiss) that were
at their second spawning from the Quetro S.A. fish
farm (332332S, 714047W) in the south of
Chile. The semen samples were obtained by
abdominal massage, avoiding contamination with
feces and urine. An initial motility evaluation was
carried out at the same center, according to the
Snchez-Rodrguez & Billard (1977) scale, that
considers zero as the minimum and five as the
maximum score. The selected samples (all with level
5) were taken to the Reproduction Laboratory of the
Universidad Catlica de Temuco (UCT) in sterilized
containers with oxygen, at 4C and in the absence of
light.
Sperm density
Sperm density of the semen (N of spermatozoa/mL),
was determined in four aliquots, by a counting
Neubauer chamber using the methodology described
by Oppenheim (1973) for blood cells.
Sperm count
Sperm count was determined in five samples. Semen
was put into five microhematocrit. Then, these were
centrifuged at 10.000 rpm for a 10 min period. Later,
by means of a table, the percentage of spermatozoa
was determined from the semen samples.
Sperm diluents
To evaluate the effectiveness of the antioxidants
polyphenol, trolox C and vitamin C, one part of the
pool semen was diluted into two parts of diluent (1:2)
according to the following treatment group: fresh
semen control (C) of different male; undiluted stored
semen (T1); semen diluted with UCT medium (UCT
with KCl to inhibit motility) (T2); T2 + polyphenol
(0.1 g 100 mL-1l) (T3); T2 + trolox C (0.1 g 100 mL-1)
 Lat. Am. J. Aquat. Res.
(T4); T2 + polyphenol (0.1 g 100 mL-1) + trolox C
(0.1 g 100 mL-1) T5; T2 + vitamin C (0.018 g 100
mL-1) (T6). Osmolarity was determined same day
using a Micro-Sample Osmometer model Fiske 210
and the pH values were measured with a digital
pHmeter model pH 21 and the value that were
obtained are indicated in Table 1.
Evaluation of the level and duration of sperm
motility of rainbow trout semen with different
sperm diluents
Once at the reproduction laboratory, the semen
samples were diluted at a 1:2 ratio with the applied
diluents and maintained at 4C in an incubation
chamber, with permanent agitation and in the absence
of light.
For sperm activation, an activating solution with
280 mOsmol kg-1 osmolarity and 9.0 pH level,
prepared with NaCl 9% was used. The evaluations
were carried out in the reproduction laboratory of the
UCT at room temperatures (10C), where flagellate
activity of the spermatozoa was observed through a
Nikon Eclipse E400 microscope; at 10x to determine
the level of motility, and at 40x to determine the
duration (in seconds) of this flagellate activity,
considering the moment the spermatozoa initiate
linear movement and ending when they begin local
rotation movements. The evaluation was carried out in
20 aliquots for each treatment. These evaluations were
carried out on days 2, 4, 7, 9, 11, 14 and 17 of storage.
Fertilizing capabilities
The evaluation of the fertilizing capability was done
after 7, 10 and 17 days of storage, on a pool of
recently extracted fish eggs, from six females during
their second spawning, raised at the same fish farm.
The eggs were deposited into plastic containers (five
replicas per treatment) with approximately 100 eggs
each. Coelomic fluid was extracted and fertilization
was carried out by adding 10 L of semen from the
control (C) and T1 group. For diluted semen of group
T2, T3, T4, T5 and T6, 20 L were used for each
replica.
Five minutes after fertilization, river water was
added to the gametes and semen residues were
cleaned. Then, hydration of the eggs was carried out
for 30 min followed by the introduction of the eggs
into enumerated micro-incubaters and into containers
with an open flow system at 9C, according to the fish
farm protocols.
Determination of fertilizing percentages
After 14 days of incubation, the percentage of
fertilization was determined using acetic acid 10%, by
depositing 30 random fish eggs and considering those
that have observed neural tubes as fertilized eggs.
340
Statistical analysis
To establish the level of motility of the semen, the
mode of each treatment was used. For the rest of the
parameters, the average values and standard deviations
were used. Using the statistical software GaphPad
Prism 5, an ANOVA and Kruskall-Wallis tests were
applied to identify the existence of statistically
significant differences between the group (P 0.05).
RESULTS
Sperm motility and sperm count
The sperm density obtained from the pool of semen
was of 16 2,3 x 109 spermatozoa/mL and the average
percentage of the sperm count obtained during the
experiment was of 33,2 1,1%. The mode that was
registered for motility on day 2 in all of the treatment
group was level 5. On day 7; T3 and T6 had lowered
to level 4. By day 9; T1 and T2 had level 0 and on day
17; T3, T4, T5 and T6 maintained level 3 (Fig. 1).
The duration of motility observed on day 2 (Fig. 2)
was of 37.07 0.24 s, for T4 and the minimum value
of 34.04 0.35 s for T5. On day 17 T1 and T2 did not
present flagellate activity, the highest value was of
7.08 1.02 s for T5 and the lowest was of 2.34
0.48 s for T3. The differences that were observed
between both treatment group were statistically
significant.
Fertilizing capabilities
The sperm density that was used for fertilization was
of 1.600.000 spermatozoa/oocyte in all of the
treatment group. The average fertilization percentages
on day 7 were 83.15 6.10% for C and 66.42 4.06%
for T1 (Fig. 3). Treatments T2, T3, T4, T5 and T6 did
not present statistically significant differences. On day
10, T1 presented 0% of fertilization and T2 presented
68.02 1.40%. T3, T4, T5 and T6 did not present
statistically significant differences. By day 17, T1 did
not present fertilization, and T2 presented 64.69
3.76%. T3, T4, T5 and T6 did not present statistically
significant differences in their fertilizing capability
(Fig 3).
DISCUSION
The results of the present investigation show that the
use of vitamin C, trolox and polyphenol in sperm
diluents for rainbow trout, preserves sperm motility,
improving significantly the fertilizing capability of
semen and increasing spermatozoa storage times.
341 Use of antioxidants in rainbow trout Oncorhynchus mykiss sperm diluents
Table 1. Osmolarity and pH values for the treatments used in the storage of rainbow trout semen.
Tabla 1. Valores de osmolaridad y pH para los tratamientos utilizados en el almacenamiento de semen de trucha arcoiris.
Treatments Information
C Fresh semen
T1 Undiluted stored semen
T2 Semen diluted with UCT medium
T3 T2 + polyphenol
T4 T2 + trolox
T5 T2 + polyphenol + trolox
T6 T2 + vitamin C
Figure 1. Level of motility (Mode) in rainbow trout
spermatozoa, submitted to different antioxidant treat-
ments. Different letters seen a same day indicate that
statistically significant differences exist (n = 20).
Figura 1. Nivel de motilidad (Moda) en espermatozoides
de trucha arcoiris sometidos a diferentes tratamientos con
antioxidantes. Letras dife-rentes en un mismo da indica
diferencias estads-ticamente significativas (n = 20).
Sperm motility in all the antioxidant treatment
group is considerably improved in T5, which presents
the highest value of 7.08 1.02 s at day 17, this can be
explained since the combined use of polyphenol and
trolox can increase their actions as antioxidants (Ball
et al., 2001b). Polyphenols on their part, act mainly by
chelating metals and capturing in vitro the ORSs and
nitrogen reactive species (NRS) in a more efficient
manner than vitamin C (Larkins, 1999). The same
occurs with the separate use of trolox and vitamin C,
this last element is the main antioxidant found in
plasma and in the cells, that by donating electrons to
the tocoperoxil radical of the oxidized vitamin E, it
recycles the antioxidant function of -tocopherol,
Osmolarity mOsmol kg-1 pH
300 8.0
300 8.0
288 8.0
280 7.5
290 7.8
288 7.7
260 7.5
Figure 2. Motility (s) of rainbow trout spermatozoa
submitted to different antioxidant treatments. The values
are given as averages SD (n = 20). Different letters
indicate that statistically significant differences exist for
a same day (P < 0.05).
Figura 2. Motilidad (s) en espermatozoides de trucha
arcoiris sometidos a diferentes tratamientos con
antioxidantes. Los valores se entregan en promedio SD
(n = 20). Letras diferentes indica que existen diferencias
estadsticamente significativas para un mismo da (P <
0,05).
helping to protect the lipid membrane from
peroxidation (May, 1999). -tocopherol can act as an
antioxidant or pro-oxidant, since it inhibits or
facilitates lipid peroxidation of the low density
lipoproteins. The pro-oxidizing activity of -
tocopherol is prevented by ascorbate, for which
vitamin E can only be effective in combinations with
vitamin C (Carr et al., 2000). The combination of
vitamin E, a lipophilic antioxidant, with vitamin C, a
hydrophilic antioxidant and/or selenium, desintoxicate
the lipids from the peroxides (Schwenke & Behr,
1998).
 Lat. Am. J. Aquat. Res.
Figure 3. Fertilizing capabilities of rainbow trout
spermatozoa submitted to different antioxidant treat-
ments. The values are given as averages SD (n = 15).
Different letters indicate that statistically significant
differences exist for a same day (P < 0.05).
Figura 3. Capacidad fecundante en espermatozoides de
trucha arcoiris sometidos a diferentes tratamientos con
antioxidantes. Los valores se entregan en promedio SD
(n = 15). Letras diferentes indica que existen diferencias
estadsticamente significativas en un mismo da (P <
0,05).
Lahnsteiner et al. (1997) studied aging in rainbow
trout Oncorhynchus mykiss semen, during cold storage
for 2 h, and he found a decrease in fertilizing
capabilities, motility and metabolism of the
spermatozoa, regarding recently extracted semen. This
decrease was mainly due to the energetic increase that
the spermatozoa requires during fertilization and to an
increase of polyunsaturated fatty acids, where they
become vulnerable to the attack of free radicals.
In the present investigation, variations in motility
times were present in the first two days of storage of
semen with antioxidants, regarding undiluted semen.
On the other hand, this is not reflected for the
fertilizing capabilities of the treatment group with
antioxidants (T3, T4, T5 and T6) by day 17, which
registered high fertilization percentages without
significant differences among them. Hoysak & Liley
(2000) report that these variations in flagellate activity
do not affect fertility, since in sockeye salmon, it only
takes 5-10 s for the spermatozoa to have contact with
the oocyte to fertilize it.
Lahnsteiner et al., (2010a) and Lahnsteiner et al.,
(2010b) incorporated different antioxidants for
defense from the ORSs into a sperm diluent, finding
positive effects on sperm viability (sperm motility,
membrane integrity and lipid peroxidation) in stored
342
semen of different teleostei fish for 72 to 120 h with
uric acid and 72 h with methionine.
There is limited information on antioxidant
systems in teleostei fish spermatozoa to be able to
define which antioxidant is the most adequate one for
semen storage. It is because of this, that in this work,
the effect of adding antioxidants that are soluble in
water and lipids, into the sperm diluents is evaluated
to maintain the integrity of the spermatozoa,
protecting the cells and reducing the risk of lipid
peroxidation which would affect sperm motility
(Ciereszco & Dabrowski, 1995).
Due to its positive effects on motility parameters,
fertilizing capabilites, stability and low price, the use
of polyphenol, trolox and vitamin C can be a useful
compliment for the storage of salmonid spermatozoa.
ACKNOWLADGEMENTS
Financed by the FONDEF D06I1020 Project and
collaboration of the Quetro S.A. and Dropco S.A.
companies.
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DOI: 10.3856/vol39-issue2-fulltext-16

Research Article

Solapamiento trfico entre el lobo marino de un pelo Otaria flavescens y la

pesquera de arrastre demersal del golfo San Matas, Patagonia, Argentina

Mara Alejandra Romero1, Silvana Dans2, Ral Gonzlez1, Guillermo Svendsen1

Nstor Garca2 & Enrique Crespo2
1
Instituto Multidisciplinario de Investigacin y Desarrollo de la Patagonia Norte (IDEPA)
CONICET/Universidad Nacional del Comahue, Gemes 1030, 8520
San Antonio Oeste-Ro Negro, Argentina
2
Centro Nacional Patagnico (CENPAT), CONICET/Universidad Nacional de la Patagonia
San Juan Bosco, Boulevard Brown 2915, 9120 Puerto Madryn-Chubut, Argentina

RESUMEN. A nivel internacional, paralelo a la declinacin y al colapso de pesqueras de gran escala, surgi
un inters creciente por el estudio de las interacciones entre mamferos marinos y pesqueras. El golfo San
Matas (Patagonia, Argentina) es considerado un ecosistema pesquero independiente de las aguas de la
Plataforma Continental Argentina, con condiciones oceanogrficas y biolgicas particulares. La condicin de
sistema semi-cerrado podra generar escenarios particulares para la interaccin entre la flota pesquera de
arrastre de fondo y la poblacin de lobos marinos de un pelo Otaria flavescens. En el presente trabajo se
caracteriz la dieta del predador y la composicin de las capturas pesqueras a fin de evaluar el solapamiento
trfico entre ambos componentes. A partir de este anlisis y la comparacin de las tallas de las presas
consumidas, se encontr que la posibilidad de una interaccin competitiva entre la flota pesquera y los lobos
marinos, a partir de la utilizacin de recursos similares, sera baja en el ecosistema del golfo San Matas.
Palabras clave: Otaria flavescens, lobo marino, golfo San Matas, pesquera de arrastre, solapamiento trfico,
Patagonia argentina.

Trophic overlap between the South American sea lion Otaria flavescens and the
demersal trawl fishery in San Matas Gulf, Patagonia, Argentina

ABSTRACT. As world fisheries began to decline and massive collapses were observed, the competition
between marine mammals and fisheries became an issue of growing concern. San Matas Gulf (Patagonia,
Argentina) is considered to be a fishery ecosystem independent of the Argentine Continental Shelf waters,
with particular oceanographic and biological properties. As a semi-enclosed ecosystem, this gulf may generate
particular scenarios for interactions between the demersal trawl fishery fleet and the population of South
American sea lions Otaria flavescens. In this paper, the diet of the top predator and the composition of fishery
catches were characterized in order to assess the trophic overlap between these two components. This analysis
and a comparison of the sizes of prey consumed revealed a low probability of competition for similar
resources between the fishing fleet and the marine mammals in the San Matas Gulf ecosystem.
Keywords: Otaria flavescens, sea lion, San Matas gulf, trawl fishery, trophic overlap, Patagonia, Argentina.
___________________
Corresponding author: Mara Alejandra Romero (aromero@ibmpas.org)

INTRODUCCIN funcionamiento de los ecosistemas (Bowen, 1997;

La dieta y los hbitos alimentarios de una especie
determinan su ubicacin dentro de una red trfica, y
definen su rol ecolgico (Pauly et al., 1998a). En
general, los mamferos marinos estn posicionados
cerca o en la parte superior de la estructura trfica, y
se considera que pueden tener un rol importante en el
Pauly et al., 1998a). Durante las ltimas dcadas, se
ha especulado que los efectos a largo plazo producto
de la grave disminucin en la abundancia de muchas
poblaciones de mamferos marinos, como conse-
cuencia de impactos de origen antrpico (caza,
contaminacin de los ambientes, capturas
incidentales), podran haber afectado de modo
345 Solapamiento trfico lobo marino-pesquera de arrastre, golfo San Matas, Argentina
permanente a los ecosistemas marinos (Parsons, 1992;
Pauly et al., 1998b; Springer et al., 2003).
Por otro lado, paralelo a la profundizacin de la
crisis pesquera mundial, tambin se ha discutido
acerca de los efectos que los mamferos marinos
podran generar sobre la pesca, compitiendo
directamente por los recursos disponibles (Butterworth
et al., 1988; Bowen, 1997). De forma simple, se
pensaba que disminuyendo las poblaciones de
mamferos marinos, las capturas pesqueras se
incrementaran en una proporcin directa a lo
consumido por los mamferos, ahora disponible para
la pesca (Yodzis, 1998). Esta interpretacin fue
utilizada para promover la reduccin en el tamao de
algunas poblaciones de mamferos marinos (Wickens
et al., 1992).
La controversia acerca de este argumento se centr
en la pregunta bsica sobre cunto consumen
realmente los mamferos marinos y surgi la
necesidad de estudiar el rol que cumplen en el
ecosistema (Yodzis, 2001). Otro debate surgi a partir
del reconocimiento que este simple esquema est
incluido en una red trfica mucho ms compleja de
interacciones que pueden afectar los resultados
(Lavigne, 1995), y en la cual los efectos de las
interacciones indirectas propagados a travs de la red
trfica pueden ser ms importantes que los efectos
propios de las interacciones directas (Yodzis, 2000).
El estudio del rol ecolgico de los mamferos
marinos y su grado de interaccin con las pesqueras
se convirti en foco de inters de muchos estudios
(Northridge, 1984, 1991; Bowen, 1997; De Master et
al., 2001; Koen-Alonso & Yodzis, 2005; Kaschner &
Pauly, 2005; Dillingham et al., 2006; Morissette et al.,
2006). Sin embargo, una evaluacin dirigida a estudiar
la competencia real entre las pesqueras y los
mamferos marinos es difcil de realizar, en parte
debido al supuesto subyacente que para que exista
competencia, la remocin de uno de los competidores
debe resultar en un incremento mensurable en la
disponibilidad de alimento para el otro componente
(Cooke, 2002). Asimismo, el desarrollo de modelos
suficientemente detallados para demostrar de forma
inequvoca la existencia de una interaccin
competitiva, est en gran medida, limitado por la
complejidad de las interacciones trficas en los
ecosistemas marinos y la dificultad para obtener datos
fiables de cada uno de los componentes (Yodzis,
2000; Plagnyi & Butterworth, 2002).
Consecuentemente, la mayor parte de los esfuerzos
en investigacin han apuntado a estudiar el grado de
solapamiento trfico, es decir, la medida en que las
especies de mamferos marinos y la pesca hacen uso
de los mismos recursos alimenticios. A pesar que los
ndices de solapamiento trfico no miden directamente
competencia, la similitud en la biologa trfica entre
los componentes involucrados puede ser un indicador
de potenciales interacciones competitivas.
El golfo San Matas es considerado un ecosistema
pesquero independiente de las aguas de la Plataforma
Argentina, siendo administrado en forma autnoma
por el gobierno de la Provincia de Ro Negro-
Argentina. Desde hace ms de tres dcadas se
desarrolla una pesquera dirigida al complejo de
especies demersales y demersal-pelgicas. De acuerdo
a sus propiedades oceanogrficas y biolgicas, se ha
sugerido que algunas de las especies forman unidades
demogrficas diferentes a las existentes en la
Plataforma Continental Argentina, como es el caso de
la merluza comn Merluccius hubbsi, principal
especie blanco de la pesquera (Di Gicomo et al.,
1993; Sardella & Timi, 2004; Gonzlez et al., 2007).
Esta condicin de sistema semi-cerrado del golfo San
Matas podra generar escenarios particulares para la
interaccin entre la flota pesquera de arrastre demersal
que opera en el golfo y algunos predadores tope del
ecosistema.
A lo largo de la costa del golfo San Matas, se
asientan durante todo el ao numerosos apostaderos de
lobos marinos de un pelo Otaria flavescens, aunque su
nmero y localizacin exacta pueden variar estacional-
mente (Grandi et al., 2008). Estos apostaderos
pertenecen a lo que se denomina la unidad funcional
del Norte de Patagonia, la cual ha mostrado una
tendencia positiva cercana al 6% anual (Dans et al.,
2004). Los apostaderos del golfo San Matas son
algunos de los que han registrado las mayores tasas de
incremento, tanto en el nmero total como en la
produccin de cras. Esta especie puede realizar viajes
de alimentacin extensos, especialmente los machos.
Las hembras estaran ms restringidas a alimentarse en
reas cercanas a la costa y a los lugares de cra (Koen-
Alonso et al., 2000), con lo cual se espera que preden
con mayor regularidad dentro de las aguas del golfo.
En este contexto, el objetivo de este trabajo fue
analizar en forma comparativa la dieta del lobo marino
de un pelo y la composicin de las capturas pesqueras
de la flota de arrastre demersal. Este anlisis abarc
tanto la comparacin de las especies presa como las
tallas consumidas/capturadas.
MATERIALES Y MTODOS
Dieta del lobo marino de un pelo
La muestra consisti de un total de 34 estmagos
colectados en el golfo San Matas entre 2006 y 2009
 Lat. Am. J. Aquat. Res.
(Fig. 1). Los estmagos fueron obtenidos a partir de
animales encontrados muertos en la costa y
provenientes de capturas incidentales (Tabla 1). Las
capturas fueron realizadas por barcos arrastreros de
fondo dirigidos a la captura de merluza comn.
Previo a la necropsia se registr la longitud
estndar (LS, cm) de los individuos y se revis
externamente para constatar la presencia de heridas.
Los estmagos una vez removidos fueron
almacenados en bolsas de polietileno en fro (-20C),
para su posterior anlisis. El tamao corporal de los
individuos vari entre 170 y 220 cm, con una edad
entre 2 y 18 aos (Grandi et al., 2009).
Los contenidos estomacales fueron descongelados
y lavados utilizando tamices secuenciales de
diferentes tamaos de malla (de 0,5 a 10 mm). En el
caso de encontrar presas intactas fueron
inmediatamente identificadas, medidas y pesadas. Las
partes diagnsticas remanentes (otolitos, huesos y
picos de cefalpodos) fueron recuperadas y
almacenadas en etanol 70%. Las presas fueron
identificadas al nivel taxonmico ms bajo posible,
utilizando colecciones de referencia (colecciones
depositadas en el CENPAT y en el IDEPA), y
catlogos publicados (Menni et al., 1984; Roper et al.,
1984; Clarke, 1986; Boschi et al., 1992; Gosztonyi &
Kuba, 1996; Boltovskoy, 1999; Volpedo &
Echevarra, 2000; Garca-Godos, 2001).
El nmero total de peces consumidos por individuo
fue determinado a partir del conteo de otolitos,
discriminando en derechos, izquierdos y otolitos no
asignados. El nmero mnimo de otolitos por especie
fue obtenido como la suma del nmero mayor de
otolitos identificados (ya sean izquierdos o derechos),
ms la mitad de los otolitos no identificados. El
nmero de cefalpodos fue estimado a partir del
mximo nmero de picos superiores o inferiores
encontrados en cada estmago (Pierce & Boyle,
1991).
La longitud (LT, longitud total de los peces y
LDM, longitud dorsal del manto de los cefalpodos,
cm) y peso hmedo (g) de las presas al momento de la
ingestin fue estimado a partir de las piezas duras
remanentes, utilizando regresiones alomtricas
(Pineda et al., 1996; Bassoi, 1997; Koen-Alonso et al.,
2000). A fin de minimizar la subestimacin de los
parmetros, slo los otolitos y picos no daados
fueron medidos. Cuando en los estmagos se
encontraron piezas digeridas o destruidas, las medidas
de estos elementos fueron asignadas a partir de una
muestra al azar de las piezas enteras y no digeridas de
cada especie, encontradas dentro del mismo estmago
(Koen-Alonso et al., 1998).
346
La importancia relativa de las presas en la dieta fue
evaluada mediante la frecuencia de ocurrencia (%FO),
la dominancia numrica o porcentaje en nmero (%N),
la dominancia en peso o porcentaje en peso (%W) y el
ndice de importancia relativa porcentual (%IRI). El
IRI (Pinkas et al., 1971; Corts, 1997) es una medida
comnmente utilizada ya que provee un resumen de la
composicin de la dieta y se obtiene como:
IRIi = (%Wi + %Ni) % FOi (1)
Los ndices fueron calculados por especie, por
grupo zoolgico (peces, moluscos y crustceos) y por
grupo ecolgico. Los grupos ecolgicos considerados
fueron: pelgico, bentnico y demersal. Este ltimo
fue subdividido en demersal-pelgico (presas que
tienen un patrn de migracin diario, dispersndose en
la columna de agua durante la noche y permaneciendo
cerca del fondo durante las horas de luz) y demersal-
bentnico (presas que no realizan migraciones
verticales).
Para cuantificar la incertidumbre debida al
muestreo, se generaron intervalos de confianza no
paramtricos de 95% para los ndices de porcentaje en
nmero (%N) y porcentaje en peso (%W), mediante
una tcnica de remuestreo (bootstrap) (Efron, 1979).
La rutina para ejecutar el bootstrap fue escrita en
lenguaje de programacin R. Las muestras al azar
fueron extradas con reemplazo, y el procedimiento
fue repetido 1000 veces.
Composicin de las capturas de la flota de arrastre
demersal
Los datos sobre composicin especfica de las
capturas y distribucin de frecuencias de tallas de las
especies capturadas fueron obtenidos de los informes
peridicos del Programa de Observadores Pesqueros
(POP) de la Provincia de Ro Negro. Los observadores
son embarcados desde los puertos de San Antonio
Oeste y San Antonio Este, siguiendo un criterio de
seleccin al azar de las embarcaciones. Tpicamente,
los viajes de pesca de la flota de arrastre tienen una
duracin promedio de 3 a 6 das, realizando entre 2 y
5 lances por da de pesca (duracin del lance 2-5 h).
El esfuerzo de muestreo del POP, en relacin a los
desembarcos anuales de merluza comn y el esfuerzo
de pesca (medido en nmero de lances y horas
efectivas de pesca), se indica en la Tabla 2.
El muestreo sobre la composicin especfica de las
capturas consisti en la recoleccin de una muestra al
azar de la captura (al menos 6 cajones de 40 kg cada
uno), previo a la seleccin y descarte por parte de la
tripulacin. Posteriormente, la muestra fue clasificada
y cuantificada por especie. Los observadores
repitieron esta rutina en uno/dos lance/s de pesca por
347 Solapamiento trfico lobo marino-pesquera de arrastre, golfo San Matas, Argentina

Figura 1. rea de estudio. Los crculos indican los lugares de varamientos o capturas incidentales de lobo marino de un
pelo Otaria flavescens.
Figure 1. Area of study. The circles indicate South American sea lion Otaria flavescens sampling sites.

Tabla 1. Resumen de las muestras de lobo marino de un pelo Otaria flavescens consideradas para el estudio de dieta. En
parntesis se indica el nmero de estmagos vacos.
Table 1. Summary of samples of South American sea lion Otaria flavescens considered for the study of the diet. The
number of empty stomachs is shown in parenthesis.

Machos Hembras
Muerto en la costa Captura incidental Muerto en la costa Captura incidental
2006 3 (2) 1 1 0
2007 2 (1) 7 10 (3) 0
2008* 3 1 1 (1) 3
2009 0 0 1 (1) 0
* se captur incidentalmente un animal de sexo indeterminado

da. El conjunto de datos disponible para caracterizar
la composicin de las capturas abarc el periodo
2006-2008. As como en el caso del lobo marino de un
pelo se consider a cada estmago como unidad de
muestreo, asumiendo que el contenido representa una
ingesta diaria, en el caso de la pesquera se consider a
cada lance de pesca como unidad de muestreo. La
importancia relativa de las diferentes especies
capturadas fue calculada mediante la frecuencia de
ocurrencia y el porcentaje en nmero. Los ndices de
porcentaje en peso e importancia relativa (%IRI) no
fueron utilizados al no disponer de los datos sobre el
peso capturado por especie a nivel de lance.
Adems, se analizaron las tallas consumidas por la
pesquera para algunas especies en particular. Los
observadores separaron una muestra al azar de entre 6
y 10 cajones de la captura total de merluza comn,
savorn Seriolella porosa y calamar Illex argentinus
(nicas especies muestreadas por el POP). Se registr
 Lat. Am. J. Aquat. Res. 348

Tabla 2. Esfuerzo de muestreo anual del Programa de Observadores Pesqueros en funcin del nmero de lances,
desembarque de merluza comn y horas efectivas de pesca. Los totales de cada una de las variables fueron obtenidos de
las estadsticas pesqueras recopiladas por la Direccin de Pesca (Milln, 2009).
Table 2. Annual sampling effort of the Fishery Observer Program in terms of the number of hauls, common hake landings
and fishing effort. The totals of each variable were obtained from the fishery statistics compiled by the Direccin de Pesca
(Milln, 2009).

Total Muestra Porcentaje de cobertura

Lances Desembarque Esfuerzo Lances Desembarque Esfuerzo Lances Desembarque Esfuerzo
Ao (ton) (h) (h)
(N) (N) (ton) (N) (ton) (h)
2006 3097 4549,2 9561 167 276 534 5,39 6,08 5,59
2007 3612 7324,21 10874 130 281 393 3,6 3,83 3,61
2008 3871 7735,58 11777 85 209 260 2,2 2,7 2,21

el sexo y la talla (medido aproximando al centmetro s

inferior) de los peces (longitud total) y calamares nij
(longitud dorsal del manto). Esta rutina se repiti en c j = i =1
s
uno/dos lance/s de pesca por da. El periodo de Ni
muestreo se extendi entre 2006 y 2008. Los i =1 y
muestreos sobre composicin especfica de las nij
capturas y distribucin de frecuencias de tallas se pij =
realizaron en forma alternada a lo largo de cada Ni
jornada de pesca. Donde s es el nmero total de predadores, r es el
nmero total de clases de recurso, nij es el nmero de
Anlisis del solapamiento trfico ocurrencias de la presa j en el predador i, y Ni es la
El anlisis del solapamiento trfico entre el lobo sumatoria de los nij en el predador i. La hiptesis nula
marino de un pelo y la pesquera de arrastre demersal de un solapamiento completo (Ho: GO = 1 versus Ha:
del golfo San Matas involucr el clculo de dos GO 1) se puso a prueba utilizando el estadstico V.
ndices de solapamiento: el ndice de solapamiento Este estadstico se calcula como:
( ) lnGO
general (GO) y el ndice de solapamiento especfico
s
(SO) (Petrakis, 1979; Ludwig & Reynolds, 1988). v=2 N
i =1 i
(3)
Estos ndices fueron elegidos porque tienen
propiedades estadsticas que permiten poner a prueba el cul sigue una distribucin Chi-cuadrado con
la hiptesis nula de un solapamiento total (Petraitis (s-1)(r-1) grados de libertad (Ludwig & Reynolds,
1979, 1985; Ludwig & Reynolds, 1988). Por otro 1988).
lado, el GO es uno de los ndices que presenta la El SO es un ndice asimtrico que evala la
menor cantidad de sesgos, ya sea debido a la probabilidad de obtener la curva de utilizacin de un
variabilidad en la equitabilidad de los recursos o a predador i a partir de la curva de utilizacin de un
variaciones en el tamao muestral (Smith & Zaret, predador m. Se calcula como:
1982).
r
( ) ( )
r
El GO es un ndice simtrico (GOBA = GOAB) que pij ln p mj pij ln pij (4)
representa la probabilidad de que la curva de j =1
= e
j =1
utilizacin de cada predador provenga de la curva de
SOim
utilizacin comn a todos ellos. A los efectos
comparativos, el GO se ajusta para que vare entre 0 y donde pmj se define para la presa j del predador m, de
1, obtenindose un ndice ajustado (GOa) (Ludwig & la misma forma que pmj se define para la presa j del
Reynolds, 1988). El GO se define como: predador i. La hiptesis nula de un solapamiento
especfico completo (Ho: SOim = 1 versus Ha: SOim
s r
n ln c ln p 1) fue puesta a prueba utilizando el estadstico U
i = 1i = 1 ij j ij
(Ludwig & Reynolds, 1988). Este estadstico se
s calcula como:
N i
GO = e i = 1 Uim = -2NilnSOim (5)
(2) siendo
349 Solapamiento trfico lobo marino-pesquera de arrastre, golfo San Matas, Argentina
el cul sigue una distribucin Chi-cuadrado con (r-1)
grados de libertad.
Los datos utilizados para el anlisis de
solapamiento trfico fueron la frecuencia de
ocurrencia de aquellas especies con un %N > 1% en la
muestra total, ya sea en la dieta del predador o en las
capturas pesqueras.
La comparacin de las tallas de las presas
consumidas por el lobo marino de un pelo con las
capturadas por la flota pesquera se bas en las tallas
estimadas a partir de las regresiones alomtricas y las
muestreadas por los observadores pesqueros. Las
diferencias estadsticas se evaluaron mediante la
prueba U de Mann-Whitney.
RESULTADOS
Dieta del lobo marino de un pelo
Del total de estmagos colectados, 26 contuvieron
restos de alimento. El estado de digestin de las presas
fue mayor en los animales varados en las costas que
en los capturados incidentalmente, en los cuales fue
comn encontrar presas recin ingeridas. Un total de
1.030 presas fueron recuperadas e identificadas a
partir de las muestras, correspondiendo a una biomasa
total estimada de 115,11 kg. El nmero medio ( error
estndar, ES) de presas por estmago fue 39,6
11,43; con un peso medio de 4,47 0,9 kg. De
acuerdo al origen de las muestras, el nmero medio de
presas por estmago fue 58,06 15,83 para animales
capturados incidentalmente y 39,65 11,43 para
animales hallados muertos en las costas.
Veinticuatro especies presa fueron identificadas,
correspondientes a tres grupos zoolgicos: peces (15
especies), cefalpodos (6 especies) y crustceos (3
especies) (Tabla 3). Los peces fueron el grupo ms
importante, con un %IRI de 93%; mientras que los
moluscos slo representaron el 6,95% de la dieta. En
el caso de los crustceos, no fue posible calcular el
valor del %IRI debido a que no se pudo reconstruir el
peso de las presas al momento del consumo.
El nmero medio de especies presa por estmago
fue 3,46 0,46. La merluza comn fue la presa ms
importante, con un %IRI de 55,42%, representando el
39,67% en nmero y el 37,09% en peso del total de
presas consumidas. La raneya Raneya brasiliensis y el
savorn tambin fueron presas significativas en la dieta
del lobo marino de un pelo, con un %IRI de 15,14% y
9,57% respectivamente. Adems, seis especies presa
(pampanito Stromateus brasiliensis, abadejo
Genypterus blacodes, anchota Engraulis anchoita,
calamar Illex argentinus, pulpo colorado Enteroctopus
megalocyathus) tuvieron un %IRI entre 1 y 5%,
constituyendo temes frecuentes en la dieta del
predador.
Con referencia a los grupos ecolgicos, el mayor
componente correspondi a presas de hbitos
demersal-pelgicos (Fig. 2), aunque la frecuencia de
ocurrencia de las presas demersal-bentnicas y
bentnicas fueron igualmente altas. La merluza, el
savorn, el pampanito y el calamar fueron las
principales especies de hbitos demersal-pelgicos. La
alta frecuencia de ocurrencia del grupo demersal-
bentnico se atribuy a la presencia de la raneya y el
abadejo; mientras que el componente bentnico estuvo
dado por el aporte de varias especies.
La LT media de los peces consumidos por el lobo
marino de un pelo present un rango de 6,85 a 65,21
cm. El rango de LDM de los cefalpodos presa fue
estimado entre 5,13 y 30,80 cm. Considerando todas
las especies presa, la longitud total estimada vari
entre 5,13 y 65,21 cm y la biomasa reconstruida entre
0,34 y 3444,27 g.
La distribucin de frecuencias de tallas fue
unimodal para la merluza, raneya y savorn (Figs. 3 y
4). La merluza fue la presa que present el rango de
tallas consumidas ms amplio, aunque prevalecieron
las tallas pequeas, con una moda en 21 cm (Fig. 3).
Aproximadamente el 90% de las merluzas ingeridas
tuvieron una talla menor a 35 cm, correspondientes a
individuos juveniles menores de 3 aos (Ocampo-
Reinaldo, 2010). El peso medio ( DS) de la merluza
fue 104,4 133,29 g.
Figura 2. Composicin de la dieta Otaria flavescens en
el golfo San Matas de acuerdo al grupo ecolgico de las
presas. %N: porcentaje en nmero, %W: porcentaje en
peso, %FO: frecuencia de ocurrencia, %IRI: ndice de
importancia relativa porcentual.
Figure 2. Diet composition of Otaria flavescens in the
San Matas gulf based on the ecological group of prey.
%N: percentage by number; %W: percentage by
regression-estimated wet weight; %FO: percent
frequency of occurrence; %IRI: percent of Index of
Relative Importance.
 Lat. Am. J. Aquat. Res.
Figura 3. Distribucin de frecuencias de tallas de
merluza comn Merluccius hubbsi consumida por Otaria
flavescens, capturada por la flota de arrastre de fondo y
palangre que operan en el golfo San Matas. La
estructura poblacional fue obtenida de la campaa de
prospeccin de los recursos demersales del golfo 2007
(REDE07, Ocampo-Reinaldo et al., 2008).
Figure 3. Length-frequency distribution of common hake
Merluccius hubssi consumed by Otaria flavescens,
caught by the trawl demersal fleet in the San Matas gulf.
The population structure was obtained from a trawl
demersal survey carried out in 2007 (REDE07, Ocampo-
Reinaldo et al., 2008).
La longitud promedio de las raneyas fue 15,54
3,37 cm, con un peso medio de 20,2 13,06 g. La
moda de la distribucin de frecuencias de tallas se
ubic en 17 cm. En el caso del savorn, la moda se
ubic en 37 cm, con una talla media de 37,73 4,23
cm y un peso medio de 551,78 170,07 g (Fig. 4).
Segn el patrn de maduracin sexual de la especie,
las tallas de savorn consumidas corresponden a
individuos adultos (Perier & Di Gicomo, 2002).
Composicin de las capturas de la flota de arrastre
demersal
Para evaluar la composicin de las capturas de la flota
de arrastre de fondo que opera en el golfo San Matas
se analiz un total de 114 lances de pesca. Se
identificaron 33 especies en las capturas (Tabla 3), sin
embargo algunos individuos no pudieron ser
identificados a nivel de especie y fueron agrupados
segn su proximidad taxonmica (por ejemplo los
lenguados y rayas). Los peces fueron el componente
en nmero ms importante de la captura, con 30
grupos taxonmicos identificados, seguido por
moluscos (%N = 1,67%) y crustceos (%N = 0,11).
Tambin se identificaron otras especies de moluscos,
anlidos, tunicados y cnidarios, pero con una
frecuencia de ocurrencia y un %N muy bajo.
La merluza, especie blanco de la pesquera, fue la
principal especie capturada, con una %FO = 99%, y
represent el 72% del nmero total capturado (Tabla
3). El grupo lenguados, conformado por varias
350
Figura 4. Curvas de selectividad de las tallas de savorn
Seriolella porosa y calamar Illex argentinus consumidos
por Otaria flavescens (Of), capturado por la flota de
arrastre de fondo que opera en el golfo San Matas (datos
obtenidos a partir de los registros del Programa de
Observadores Pesqueros).
Figure 4. Size selectivity curves of silver warehou
Seriolella porosa and squid Illex argentinus preyed by
Otaria flavescens (Of), caught by the trawl demersal fleet
in the San Matas gulf (data obtained from the Fishery
Observer Program).
especies (entre ellas Paralichthys isosceles, Xistreuris
rasile y Paralichthys patagonicus), estuvo presente en
el 98,24% de los lances muestreados y represent el
5,98% en nmero de la captura. Del total de grupos
taxonmicos identificados slo 10 tuvieron un %N
mayor al 1%. Los restantes grupos fueron poco
importante respecto del nmero de individuos
capturados, aunque algunos tuvieron una alta
frecuencia de ocurrencia.
La distribucin de frecuencias de tallas de la
captura de merluza fue unimodal, con una moda en 28
cm en 2006 y 33 cm en 2007 (Fig. 3). El rango de
tallas de savorn vari entre 14 y 61 cm, pero la
mayora de las capturas se registraron entre los 24 y
40 cm (Fig. 4). La distribucin de frecuencias de tallas
de calamar present un rango de 10 a 36 cm, con una
moda en 17 cm (Fig. 4). Crespi (2010) estim la talla
de primera madurez para esta especie en el golfo San
Matas y encontr que para el grupo desovante de
verano fue 13,92 y 18,92 cm para los machos y
hembras respectivamente; mientras que para los
individuos capturados el resto del ao fue 21,15 cm
para machos y 26,91 cm para hembras. De esta forma,
la flota pesquera de arrastre captura tanto individuos
juveniles como adultos, de acuerdo a la poca del ao.
Anlisis del solapamiento trfico
A partir de la caracterizacin de la dieta de Otaria
flavescens y de la composicin de las capturas
pesqueras se identificaron ms de 60 especies presa,
correspondientes a peces cartilaginosos, telesteos e
 351

Tabla 3. Composicin de la dieta de Otaria flavescens y de las capturas pesqueras de la flota de arrastre de fondo en el golfo San Matas. GE: grupo ecolgico,
B: bentnico, DB: demersal-bentnico, DP: demersal-pelgico, P: pelgico, NA: no asignado, %FO: frecuencia de ocurrencia, %N: porcentaje en nmero, %W:
porcentaje en peso, %IRI: ndice de importancia relativa porcentual, N: nmero de presas, IC: intervalo de confianza.
Table 3. Diet composition of Otaria flavescens and composition of the catches of the trawl demersal fishery in the San Matas gulf. GE: ecologic group, B:
benthic, DB: demersal-benthic, DP: demersal-pelagic, P: pelagic, NA: not assigned, %FO: percent frequency of occurrence; %N: percentage by number; %W:
percentage by regression-estimated wet weight; %IRI: percent of Index of Relative Importance; N: number of prey items; CI: confidence intervals.

Lobo marino de un pelo Pesquera de arrastre

Composicin en nmero Composicin en peso Composicin en nmero
Presa GE %FO %N IC %W IC %IRI N %FO %N IC N
Peces 81,48 92,63 90,19 93 955 97,41
Merluccius hubbsi DP 44,44 39,67 14,38-70,38 37,09 17,25-59,85 55,42 409 99,12 72,28 67,77-76,20 40733
Raneya brasiliensis DB 29,63 26,67 1,52-55,26 4,79 0,08-16,92 15,14 275 0,88 0 0,00-0,01 2
Seriolella porosa DP 22,22 4,46 1,11-13,04 22,05 7,53-44,35 9,57 46 33,33 4,30 2,15-7,01 2423
Stromateus brasiliensis DP 18,52 3,78 0,34-13,56 12,41 0,46-32,04 4,87 39 61,40 4,11 2,80-6,06 2317
Genypterus blacodes DB 22,22 2,13 0,50-6,50 8,89 2,47-21,53 3,98 22 45,61 0,26 0,19-0,35 149
Engraulis anchoita P 14,81 10,57 0,29-28,43 1,93 0,02-6,96 3,01 109 19,30 2,07 0,81-3,81 1165
Porichthys porosissimus B 22,22 1,84 0,69-4,03 0,42 0,14-1,02 0,82 19 20,18 0,10 0,06-0,16 57
Macruronus magellanicus DP 7,41 0,48 0,00-1,88 1,34 0,00-4,64 0,22 5 38,60 1,97 0,99-3,44 1111
Xystreuris rasile B 7,41 0,39 0,00-1,57 0,21 0,00-0,65 0,07 4
Trachurus picturatus P 3,70 0,87 0,00-2,25 0,23 0,00-0,89 0,07 9
Prionotus nudigula B 7,41 0,29 0,00-0,89 0,24 0,00-0,95 0,06 3 42,11 1,35 0,85-2,08 758
Paralichthys patagonicus B 7,41 0,29 0,00-1,07 0,11 0,00-0,50 0,05 3
Cynoscion guatucupa DB 3,70 0,29 0,00-1,48 0,14 0,00-0,53 0,03 3
Psammobatis lentiginosa B 3,70 0,10 0,00-0,50 0,33 0,00-1,22 0,03 1
Paralichthys isosceles B 3,70 0,58 0,00-2,68 6
Lenguados B 98,25 5,99 5,16-6,88 3373
Rayas DB 79,82 1,16 0,95-1,42 651
Callorhinchus callorhynchus DB 71,05 1,74 1,21-2,45 978
Solapamiento trfico lobo marino-pesquera de arrastre, golfo San Matas, Argentina

Acanthistius brasilianus DB 48,25 0,53 0,31-0,92 296

Mustelus schmitti DB 23,68 0,28 0,15-0,45 158
Parona signata P 29,82 0,26 0,17-0,40 149
Sebastes oculatus DB 5,26 0,26 0,02-0,92 145
Congiopodus peruvianus DB 26,32 0,18 0,10-0,30 101
Pseudopercis semifasciata DB 34,21 0,13 0,09-0,18 75
 Lobo marino de un pelo Pesquera de arrastre
Composicin en nmero Composicin en peso Composicin en nmero
Presa GE %FO %N IC %W IC %IRI N %FO %N IC N
Cheilodactylus bergi DB 4,39 0,10 0,01-0,33 56
Percophis brasiliensis DB 20,18 0,08 0,05-0,12 37
Salilota australis DB 7,02 0,07 0,04-0,10 35
Squatina guggenheim DB 15,79 0,06 0,02-0,15 22
Mullus argentinae DB 5,26 0,04 0,02-0,06 22
Pagurus pagrus DP 3,51 0,04 0,01-0,09 21
Dules auriga DB 3,51 0,04 0,01-0,11 16
Galeorhinus galeus DP 6,14 0,03 0,00-0,08 15
Micropogonia furnieri DB 1,75 0,03 0,01-0,06 12
Squalus acanthias DP 3,51 0,02 0,00-0,06 6
Milyobatis spp. DB 4,39 0,01 0,00-0,03 5
Notorhynchus cepedianus DB 0,88 0,01 0,00-0,02 2
Pez no indentificado NA 11,11 0,10 0,00-0,48 1
Moluscos 66,67 6,89 9,81 6,95 71 1,67
Illex argentinus DP 37,04 3,39 1,08-7,65 4,27 1,46-9,44 4,61 35 78,95 1,41 1,10-1,74 794
Lat. Am. J. Aquat. Res.

Loligo sanpaulensis DP 14,81 1,26 0,13-3,69 0,55 0,09-1,55 0,44 13 27,19 0,26 0,15-0,39 145
Loligo gahi DP 11,11 0,87 0,00-3,45 0,21 0,03-0,34 0,20 9
Enteroctopus megalocyathus B 14,81 0,68 0,06-2,91 4,57 0,34-13,30 1,26 7 3,51 0,01 0,00-0,02 4
Eledone massyae B 11,11 0,39 0,00-1,23 0,12 0,00-0,47 0,09 4
Octopus tehuelchus B 7,41 0,29 0,00-0,93 0,09 0,00-0,34 0,05 3
Crustceos 18,52 0,48 5 0,11
Tumidotheres maculatus B 7,41 0,19 0,00-1,57 2
Pterygosquilla armata armata B 3,70 0,10 0,00-0,40 1
Cangrejo B 3,70 0,10 0,00-0,51 1 26,32 0 63
Eucopia sp. DP 3,70 0,10 0,00-0,54 1
Pleoticus muelleri DP 3,51 0 4
1030 55900
352
353 Solapamiento trfico lobo marino-pesquera de arrastre, golfo San Matas, Argentina

invertebrados. Sin embargo, slo 14 grupos
taxonmicos tuvieron un %N > 1% en la dieta del
predador o en las capturas de la flota de arrastre,
teniendo en cuenta que el grupo rayas y grupo
lenguados podran abarcar a ms de una especie
(Tabla 3).
El ndice de solapamiento general indic que las
curvas de utilizacin de O. flavescens y de las capturas
pesqueras difirieron significativamente de la curva de
utilizacin comn a ambos componentes (Tabla 4).
Asimismo, mediante el anlisis de solapamiento
especfico se encontr que los solapamientos de a
pares fueron significativamente diferentes al
solapamiento total. Esto significa que la curva de
utilizacin de los recursos de cada uno de los
consumidores no puede obtenerse a partir de la curva
de utilizacin de ninguno de los dems consumidores
(ya sea el predador o la flota pesquera).
El test estadstico asociado a este tipo de pruebas
slo pone a prueba la hiptesis que el solapamiento
general o especfico sea igual a 1. Cuando esta
hiptesis se rechaza, el resultado indica que existen
evidencias estadsticamente significativas para
asegurar que el solapamiento es distinto de 1. No
obstante, el valor del ndice podra ser igualmente alto.
En el caso de estudio, el ndice de solapamiento
general ajustado (GOa) fue 0,65, mientras que los
valores de las comparaciones de a pares (SOik) fueron
muy inferiores a este valor. Sin embargo, cuando se
analiz el solapamiento especfico de la flota pesquera
de arrastre sobre los lobos marinos (Tabla 4), se
encontr un mayor valor del SOik que en sentido
inverso.
Del total de especies utilizadas para realizar el
anlisis de solapamiento trfico, se seleccionaron
aquellas presas que fueron importantes y comunes
para ambos grupos a fin de realizar la comparacin de
las tallas consumidas. Estas especies fueron merluza,
savorn y calamar. El pampanito fue otro recurso
importante para ambos consumidores, sin embargo
esta especie no pudo ser incluida en el anlisis al no
disponer de sus datos pesqueros.
La comparacin de las tallas de merluza
consumidas/capturadas indic diferencias altamente
significativas (U = 2063024, P < 0,0001). La flota de
arrastre captur tallas ms grandes que aquellas
consumidas por O. flavescens. Una comparacin
interesante surge al incluir a las series de datos sobre
las capturas pesqueras y el consumo del predador, la
estructura de tallas estimada para el efectivo pesquero
de merluza en el golfo San Matas (Fig. 3). Estos datos
fueron obtenidos del informe de la campaa de
prospeccin de recursos demersales realizada en 2007
(Ocampo-Reinaldo et al., 2008). La distribucin de
frecuencias de tallas de la subpoblacin de merluza
fue bimodal, con modas en 14 y 33 cm. Las clases de
tallas ms abundantes (medido en nmero de
individuos) fueron juveniles de 1 y 2 aos de edad
(Ocampo-Reinaldo, 2010). La distribucin de
frecuencias de tallas de las merluzas consumidas fue
la ms cercana a la estimada para el stock del golfo,
con una moda en 21 cm. La pesca de arrastre centr su
esfuerzo de captura sobre la moda superior de la
subpoblacin de merluza.

Tabla 4. Solapamiento trfico entre Otaria flavescens y la flota pesquera de arrastre de fondo que opera en el golfo San
Matas. GO: ndice de solapamiento general, GOa: ndice de solapamiento general ajustado, V: valor del estadstico para
poner a prueba la hiptesis nula de GO = 1, gl: grados de libertad, P: probabilidad del estadstico, SOik: ndice de
solapamiento especfico del grupo i sobre el grupos k, U: valor del estadstico para poner a prueba la hiptesis nula de
SOik = 1.
Table 4. Diet overlap analyses between Otaria flavescens and trawl demersal fishery that operates in the San Matas gulf.
GO: general overlap index, GOa: adjusted general overlap index, V: the statistic to test the null hypothesis that GO = 1,
df: degrees of freedom, P: probability of the statistic, SOik: specific overlap of group i onto group k, U: statistic to test the
null hypothesis that SOik = 1.

ndice de solapamiento general

GO GOa V gl P
0,97 0,65 3323,14 14 < 0,001
ndice de solapamiento especfico
i k SOik U gl P
Lobo marino Pesca arrastre 0,0004 15365,87 14 < 0,001
Pesca arrastre Lobo marino 0,3566 111978,29 14 < 0,001
 Lat. Am. J. Aquat. Res.
En el caso del savorn, los lobos consumieron tallas
significativamente ms grandes (U = 72876, P <
0,0001) que aquellas capturadas por la flota pesquera
de arrastre. Estos resultados fueron opuestos a lo
encontrado para el calamar, dado que las tallas
capturadas por la flota fueron significativamente
mayores (U = 4583, P < 0,0001) a las consumidas por
O. flavescens.
DISCUSIN
El estudio del solapamiento trfico entre predadores
tope y pesqueras, representa una primera
aproximacin para evaluar el grado de potencial
competencia consuntiva que se puede generar
producto de la intervencin humana en los
ecosistemas marinos. Particularmente, en el golfo San
Matas se dispona de buena informacin sobre los
desembarcos, distribucin espacial, abundancia y
aspectos biolgicos de las mayora de los peces
demersales (Gonzlez et al., 2004), aunque se
desconoca casi por completo las relaciones trficas
entre los eslabones superiores, y entre stos y las
pesqueras. El presente anlisis constituye la primera
evaluacin global de las interacciones trficas entre la
principal especie de mamfero marino del golfo y la
pesquera de especies demersales.
El anlisis de la dieta del predador mostr a O.
flavescens como un predador generalista,
consumiendo una amplia variedad de recursos. No
obstante, el nmero de presas con importancia
relativamente alta en la dieta fue bajo. El 80% de la
dieta (%IRI) estuvo determinado por el aporte de
merluza, savorn y raneya. A su vez, se lo defini
como un predador de hbitos mixtos, ya que se
aliment tanto de presas asociadas a la columna de
agua como al fondo, y utilizara los recursos de
acuerdo a su disponibilidad en el ambiente. Aunque en
este estudio debido a las caractersticas de las muestra
(tamao y procedencia de las muestras) no fue posible
analizar la dieta segn el sexo del predador, Koen-
Alonso et al. (2000) seal que el marcado
dimorfismo de esta especie podra generar
restricciones en sus comportamientos de alimentacin,
lo que llevara a las hembras a alimentarse en aguas
ms costeras y someras que los machos. Por lo tanto,
machos y hembras de esta especie pueden ser
considerados como especies trficas distintas y
podran tener una interaccin diferente con la
pesquera.
En las capturas de la flota de arrastre se identific
un nmero elevado de especies (33 especies), que
incluyeron invertebrados, peces cartilaginosos y
telesteos, aunque la mayora registr una baja
354
representatividad en nmero. La merluza, especie
blanco de la pesquera, domin ampliamente las
capturas. De acuerdo a los hbitos alimenticios de las
especies capturadas, la flota pesquera sera equivalente
a un predador tope natural del ecosistema. No
obstante, la pesquera podra considerarse como un
predador no eficiente, ya que parte de los recursos
explotados son descartados e ingresan nuevamente al
sistema como detritos o son aprovechados por otros
predadores que se comportan como comensales
oportunistas.
Aunque muchos de los recursos utilizados fueron
comunes a ambos consumidores, el anlisis de
solapamiento trfico y la comparacin de las tallas
consumidas indicaron que, a pesar de aprovechar
recursos similares, lo haran de forma diferente. El
principal recurso para ambos componentes fue la
merluza comn, sin embargo la pesca centr su
esfuerzo de captura sobre tallas ms grandes que
aquellas consumidas por los lobos, indicando una
separacin en el uso del recurso. Al mismo tiempo, el
mayor valor obtenido al analizar el solapamiento
especfico de la flota pesquera de arrastre sobre los
lobos marinos sugerira que stos tienen un nicho
trfico ms amplio que la pesquera. Estas diferencias
podran asociarse a los dominios del ambiente donde
consumen/capturan a las presas y a restricciones
propias de cada consumidor.
O. flavescens estara limitado tanto fsica (tamao
del predador) como ecolgicamente (la presencia de la
cra en tierra), lo que acotara su rango de accin y
espectro de presas disponible. Adems, estas
diferencias y restricciones tienden a separar los nichos
trficos de las especies, disminuyendo la posibilidad
real de una competencia intra e interespecfica. La
pesquera tambin tiene ciertas restricciones respecto a
su rango de accin, ya sean de ndole interna
(limitaciones en la capacidad de la bodega, poder de
pesca, selectividad de la red o posibilidad de operar
sobre ciertos sustratos) o externa (restricciones
impuestas por el manejo pesquero o el mercado), que
determinan la forma en la que utiliza cada recurso.
En trminos generales, el escaso solapamiento
trfico entre la flota pesquera de arrastre del golfo y el
lobo marino, y la diferencia en las tallas de las presas,
sugirieron que la posibilidad de potenciales efectos
competitivos a partir de la utilizacin de recursos
similares podra ser baja en el ecosistema del golfo
San Matas. Estos resultados son equivalentes a lo
observado en el litoral patagnico de la Plataforma
Continental Argentina, donde se encontr una baja
probabilidad de competencia por los recursos entre la
pesquera de merluza y varias especies de predadores
tope, entre los que se incluyen mamferos marinos y
elasmobranquios (Dans et al., 2003).
355 Solapamiento trfico lobo marino-pesquera de arrastre, golfo San Matas, Argentina
Sin embargo, el uso de recursos similares pero con
diferencias espacio-temporales o en un rango de tallas
distinto no necesariamente mitiga la intensidad de la
interaccin (Harwood, 1987). El anlisis previo slo
considera los efectos indirectos ms obvios, como la
competencia consuntiva (una sola especie
intermediaria, la presa), pero descarta los efectos
producidos a travs de las conexiones de mayor
longitud (ms de una especie intermediaria) presentes
en la red trfica (Yodzis, 2000).
Ms an, el anlisis de solapamiento trfico
implica una visin esttica de las interacciones. En un
sistema donde la pesca estara regulada a corto plazo
por los patrones biolgicos y oceanogrficos que
ocurren en el golfo San Matas (Romero et al., 2008a),
es esperable que la dinmica de las interacciones que
se dan en el ecosistema cambie estacional y
espacialmente. A largo plazo es an ms probable que
se generen modificaciones en la forma en que
interactan los componentes del sistema, donde
tpicamente el nivel de intervencin humana vara en
el tiempo. En un anlisis retrospectivo, se encontr
que la actividad pesquera en el golfo San Matas ha
estado histricamente determinada por las
fluctuaciones en las condiciones de mercado (Romero
et al., 2008b), y esto podra haber conducido a
diferentes escenarios de interaccin, principalmente
con aquellos predadores con vnculo ms directo.
O. flavescens es la principal especie de mamfero
marino que depende del recurso merluza en el
ecosistema patagnico. Analizando especficamente la
relacin entre lobos y pesca se podra dar una
dinmica ambigua, pero no mutuamente excluyente,
que modifique el resultado de la interaccin en
funcin de la historia y evolucin del sistema.
Por un lado, se podra suponer que la poblacin de
lobo marino se vera afectada negativamente por la
actividad pesquera, tanto por las interacciones
operacionales (captura incidental) como ecolgicas
(competencia). El hecho que en la actualidad, los
estimadores de estas interacciones (la captura
incidental por lance y el solapamiento trfico) sealen
una baja intensidad para el ecosistema del golfo San
Matas, no implica que en el mediano plazo se puedan
producir modificaciones.
Adems, podra darse una relacin de comen-
salismo por los lobos. La pesca, desde sus inicios,
podra haber subsidiado parcialmente a la poblacin
de lobo marino en el golfo, facilitando a travs del
descarte y la reduccin del canibalismo (por remocin
de adultos), la disponibilidad de juveniles de merluza.
Algunos aspectos de este tipo de dinmica entre la
pesca de especies demersales, lobo marino y merluza,
ya fue sugerido por Koen-Alonso & Yodzis (2005) y
Drago et al. (2009) para la Plataforma Continental
Argentina.
En el escenario actual del ecosistema del golfo San
Matas se encuentra una poblacin de O. flavescens en
crecimiento, con una tasa anual de incremento de
5,7% (Dans et al., 2004). La pesquera de especies
demersales del golfo registr, durante los ltimos
aos, una expansin en su nivel de actividad, con
rendimientos consecutivamente superiores, y una
tendencia hacia la diversificacin de los desembarques
(Romero et al., 2008b). Paralelamente, el descarte de
merluza tambin mostr un incremento durante el
periodo 1995-2008 (Romero et al., 2010).
Respecto del estado del recurso, estimaciones
recientes sugirieron que el efectivo pesquero de
merluza del golfo parece encontrarse en buen estado
de conservacin, manteniendo una estructura
demogrfica equilibrada (Ocampo-Reinaldo, 2010).
Las proyecciones de diferentes escenarios pesqueros,
bajo un rgimen de anlisis monoespecfico,
demostraron que duplicando y cuadruplicando la
mortalidad por pesca, se produciran cambios
negativos en la abundancia y estructura etaria de la
poblacin (Ocampo-Reinaldo, 2010). Esta situacin
hipottica para el golfo es similar a la observada
durante las ltimas dcadas en los dos efectivos
pesqueros de merluza de la Plataforma Continental
Argentina, los cuales fueron declarados en emergencia
pesquera en 1999 (Boletn Oficial de la Repblica
Argentina, Decreto 189/1999).
S a estas proyecciones se le incorpora el efecto de
las relaciones trficas y la propagacin a lo largo de la
red, los resultados pueden ser inesperados. Las
tendencias de los componentes de una comunidad ante
distintos escenarios (perturbaciones) estn caracteri-
zadas por altos niveles de incertidumbre (Yodzis,
1988). Esto implica que tanto la magnitud como el
sentido de los cambios pueden contradecir lo esperado
a priori. Los modelos multiespecficos permiten
estudiar dinmicamente los cambios y sus impactos
sobre las diferentes especies involucradas, mientras
que en un enfoque uniespecfico se asumen
constantes. El desarrollo de modelos multiespecficos
es especialmente importante para el ecosistema del
golfo San Matas, donde pareciera que an se
encuentran efectivos pesqueros en buen estado de
conservacin, acompaado de una actividad pesquera
en expansin y un crecimiento en el tamao de las
poblaciones de mamferos marinos.
CONCLUSIONES
El golfo San Matas es considerado un ecosistema
pesquero semi-cerrado, incluso algunas especies de
 Lat. Am. J. Aquat. Res.
peces forman sub-poblaciones independientes de las
existentes en las aguas de la Plataforma Continental
Argentina. Esta condicin podra generar escenarios
particulares para la interaccin entre las colonias de
lobo marino de un pelo y la principal flota pesquera
que opera en el golfo. Sin embargo, mediante el
anlisis de solapamiento trfico y la comparacin de
las tallas consumidas se encontr una baja interaccin
entre ambos consumidores (considerando a la flota
pesquera de arrastre como un predador), sugiriendo
que la posibilidad de potenciales efectos competitivos
a partir de la utilizacin de recursos similares podra
ser baja en el golfo San Matas. Estos resultados
representan la primera evaluacin global de las
interacciones ecolgicas entre mamferos marinos y
pesqueras en el golfo, y son equivalentes a lo
registrado para la Plataforma Continental Argentina.
O. flavescens fue identificado como un predador
generalista, siendo la merluza comn la presa ms
importante. En las capturas de la flota pesquera de
arrastre se registr un nmero elevado de especies,
aunque la merluza comn domin ampliamente las
capturas. La pesquera fue considerada equivalente a
un predador natural del sistema, a pesar de un
aprovechamiento no eficiente de los recursos ya que
parte son devueltos al mar como descarte.
Los estudios de solapamiento trfico representan
una primera aproximacin para estudiar la competen-
cia entre dos consumidores, y son tiles cuando no se
dispone de informacin suficiente para llevar adelante
una evaluacin directa acerca de la competencia. Por
esta razn, a pesar que el anlisis de solapamiento
seal una baja interaccin trfica entre O. flavescens
y la pesquera de arrastre demersal en el golfo San
Matas, es fundamental avanzar en el estudio de las
relaciones trficas que se dan en un ecosistema donde
an parecen encontrarse efectivos pesqueros en buen
estado de conservacin y donde las poblaciones de
lobos marinos se estn recuperando. El nfasis debera
centrarse en la trada ms importante identificada en
este estudio: el lobo marino de un pelo, la pesquera de
arrastre y la merluza comn, mediante la construccin
de modelos multiespecficos.
AGRADECIMIENTOS
Este estudio fue realizado a cabo gracias al soporte
logstico del Centro Nacional Patagnico (CENPAT-
CONICET) y el Instituto de Biologa Marina y
Pesquera Almirante Storni (IBMPAS). Los autores
agradecen a las siguientes entidades que financiaron el
estudio: GEF/PNUD, Fundacin BBVA (BIOCON
04), CIUNPAT, Agencia Argentina para la Promocin
356
de la Ciencia y la Tecnologa (ANPCyT), Proyecto
PID371, Cetacean Society International, y al Centro
para la Conservacin Marina, en nombre del Grupo de
Especialistas en Cetceos (IUCN). Tambin se
agradece a Paul Osovnikar, al Programa de
Observadores a Bordo y a la Direccin de Pesca de la
Provincia de Ro Negro por el aporte de informacin.
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Lat. Am. J. Aquat. Res., 39(2): 359-377, 2011Distribution of medusae in Aysn region, southern Chile 359
DOI: 10.3856/vol39-issue2-fulltext-17

Research Article

Seasonal and vertical distribution of medusae in Aysn region, southern Chile

Viviana Bravo1,2, Sergio Palma1 & Nelson Silva1

1
Escuela de Ciencias del Mar, Pontificia Universidad Catlica de Valparaso
P.O. Box 1020, Valparaso, Chile
2
Departamento de Oceanografa, Universidad de Concepcin
P.O. Box 160-C, Concepcin, Chile

ABSTRACT. Medusae collected in winter and spring 2007 were analyzed in a longitudinal transect made
between the Boca de Guafo and Elefantes Fjord, southern Chile. A total of 30 species were identified,
Hydromedusae (29) and Scyphozoa (1), where Bougainvillia macloviana, Hybocodon chilensis, Hydractinia
tenuis, Laodicea pulcra, L. undulada, Modeeria rotunda and Chrysaora plocamia represent new records for
the area. A significant increase in the jellyfish abundance was higher in spring than in winter (fourteen times
higher), with 68% of common species in both seasons. The specific diversity was slightly higher in winter (3.4
bits) than spring (3.2 bits), the species richness instead was higher in spring than in winter, with a mean of 5
and 12 species, respectively. The vertical distribution showed the presence of surface (H. borealis), deep (A.
apicata, C. peregrina and R. velatum) and wide bathymetric distribution (B. muscoides and B. muscus)
species. Results from the area were compared with previous results (2002-2003) thus proving that most
species identified are common in southern Chilean fjords and channels.
Keywords: Cnidaria, hydromedusae, scyphozoa, seasonal distribution, vertical distribution, southern Chile.

Distribucin estacional y vertical de medusas en la regin de Aysn, sur de Chile

RESUMEN. Se analizaron las medusas colectadas en invierno y primavera de 2007, en una transecta
longitudinal efectuada entre la boca del Guafo y fiordo Elefantes, sur de Chile. Se identific un total de 30
especies, Hydromedusae (29) y Scyphozoa (1), de las cuales Bougainvillia macloviana, Hybocodon chilensis,
Hydractinia tenuis, Laodicea pulcra, L. undulada, Modeeria rotunda y Chrysaora plocamia constituyen
nuevos registros para esta rea. Se determin un fuerte incremento en la abundancia de medusas en primavera
respecto a invierno y (14 veces mayor), con un 68% de especies comunes en ambas estaciones. La diversidad
especfica fue levemente mayor en invierno (3.4 bits) que primavera (3.2 bits), en cambio la riqueza de
especies fue mayor en primavera que en invierno, con una media de 5 y 12 especies, respectivamente. La
distribucin vertical mostr en ambas estaciones la presencia de especies superficiales (H. borealis), profundas
(A. apicata, C. peregrina y R. velatum) y de amplia distribucin batimtrica (B. muscoides y B. muscus). Los
resultados obtenidos en esta rea se compararon con resultados obtenidos anteriormente (aos 2002 y 2003) y
se confirm que la mayora de las especies identificadas son comunes en fiordos y canales australes de Chile.
Palabras clave: Cnidaria, hidromedusas, escifozoos, distribucin estacional, distribucin vertical, sur de
Chile.
___________________
Corresponding author: Sergio Palma (spalma@ucv.cl)

INTRODUCTION very primitive though highly diverse planktonic group.

An increasing concern on the explosive proliferation
of gelatinous organisms in diverse marine areas has
been observed during the last years, given their
significant role in the organization of the coastal
ecosystems and impact on human activities (Mills,
2001; Brodeur et al., 2002). Jellyfish are among the
most conspicuous gelatinous organisms, which are
Some groups, as Lepto- and Anthomedusae have
metagenic life cycles with benthic stages, alternating
sexual and asexual reproductive processes that may
lead to seasonally jellyfish blooms in coastal waters
(Palma & Rosales, 1995; Palma & Apablaza, 2006;
Purcell et al., 2007). Such blooms are mainly
promoted by temperature and food availability
fluctuations, factors that play a predominant role in the
360 Lat. Am. J. Aquat. Res.
composition and abundance of zooplankton in the
oceans (Parsons & Lalli, 2002; Kehayias, 2004).
These blooms may cause a seasonal dominance of the
zooplanktonic biomass by the gelatinous organisms in
a given geographical area (Mianzn & Guerrero, 2000;
Genzano et al., 2008; Miglietta et al., 2008).
Medusae are important planktonic predators that
fed on copepods, invertebrate larvae, and fish larvae
(Purcell, 1985, 1997). Due to their predatory nature,
food competition, parasite transmission, distribution
and seasonal abundance, jellyfishes may have
economic implications, as they may compete for food
with commercial fish and/or cause negative impacts
on fish farming activities.
Economic activities have been developed in inner
waters of southern Chile since mid 80s, which are
associated to tourism, maritime transport and
aquaculture. The latter has particularly shown a
significant growth in the regions of Chilo (4131-
4339S) and Aysn (4339-4629S), due to the
intensive cage culture of salmon species, which have
occasionally been affected by mortalities involving
jellyfish proliferations, as observed between February-
June 2002 (S. Palma, unpublished).
The phylum Cnidaria has been widely studied in
the Chilo region (Galea, 2007; Galea et al., 2007;
Palma et al., 2007a, 2007b, 2011; Villenas et al.,
2009a), which is characterized by high biological
production reflected on high values of chlorophyll-a
(Gonzlez et al., 2011) and zooplanktonic biomass,
mainly supported by copepods, euphausiids and
carnivorous jellyfish (Palma & Silva, 2004). In this
area, strong seasonal fluctuations have been
established in jellyfish abundance in winter and
spring, observing 33 species with a summer
dominance of Amphogona apicata, Bougainvillia
muscoides, Clytia simplex, Cunina peregrina,
Hydractinia tenuis, Obelia spp. and Solmundella
bitentaculata (Villenas et al., 2009a; Palma et al.,
2011). In Aysn region, the available data exclusively
involve spring and indicate the presence of 31 species,
with a dominance of Amphogona apicata, Clytia
simplex, Lizzia blondina (= Hydractinia minuta),
Proboscidactyla ornata and Solmundella bitentaculata
(Palma et al., 2007a, 2007b). These regions are
separated by the Boca de Guafo (4339S), which
corresponds to the main water exchange route between
the Pacific Ocean and the inner water ecosystem.
Aysn shows peculiar oceanographic charac-
teristics influenced by the Meninea constriction-sill
which, due to its shallow depth (50-60 m), gives origin
to the formation of two microbasins with different
oceanographic characteristics. On one hand, the
northern microbasin is about 250 m deep, and
communicates with the adjacent Pacific through the
Boca de Guafo, where more saline waters penetrate
and mix with less saline waters coming from
precipitations, rivers, and glacial contributions (Palma
& Silva, 2004; Palma et al., 2007a, 2007b; Silva &
Palma, 2008). This constant exchange has allowed the
entry of oceanic planktonic species that have
successfully colonized the inner waters (Palma, 2008).
On the other hand, the southern microbasin appears
more shallow, with a mean depth of 150 m, and is
semi-isolated from the oceanic influence as a result of
the dam effect exerted by the Meninea constriction-
sill that plays a fundamental role over circulation,
residence period and physical and chemical
characteristics of both microbasins (Silva et al., 1997,
1998).
Considering the relevance attained by cnidarians in
the marine ecosystems and their seasonal abundance
fluctuations associated to environmental factors, this
study aims to analyse (i) the spatial and temporal
variability of jellyfish in winter and spring 2007 in
order to establish the spatial/temporal variability of
such organisms and (ii) the comparison of the results
obtained for spring 2007 with 2002-2003 springs in
the same area.
MATERIALS AND METHODS
The CIMAR 13 Fiordos cruise was carried out
between the Boca de Guafo (4346S) and Elefantes
Fjord (4629S) (Fig. 1), where two oceanographic
campaigns were undertaken, one in winter (July 23-
August 7, 2007) and the other in spring (October 29-
November 14, 2007). During each campaign, a
northern-southern longitudinal transect was assessed,
allocating 23 oceanographic stations. However, due to
meteorological problems during the winter campaign,
only 19 stations were sampled.
A CTDO Sea-Bird model SBE 25 was used at each
station to record the oceanographic variables
(temperature, salinity and dissolved oxygen content)
in the water column, which were used to develop
vertical profiles for the oceanographic characterization
of the studied area. Salinity and dissolved oxygen
records were corrected using the results from the
chemical analysis of discrete samples collected in the
water column during the CTDO casting.
Zooplankton samples were obtained through
oblique tows at three different depth strata: superficial
(0-25 m), medium (25-50 m) and deep (50 to a
maximum of 200 m, depending on the bottom depth),
using a 350 m mesh sieve Tucker trawl net, provided
with flowmeters to estimate the filtered water
 Distribution of medusae in Aysn region, southern Chile 361

Figure 1. Location of the oceanographic stations during the Cruise CIMAR 13 Fiordos.
Figura 1. Localizacin de las estaciones oceanogrficas durante el Crucero CIMAR 13 Fiordos.

volume. These strata were chosen considering the
oceanographic features of two layers characterizing
the inner region of fjords and channels (Silva et al.,
1997, 1998). The zooplankton samples were fixed
immediately after collection and preserved in 5%
neutral formaldehyde in seawater buffered with borax.
Jellyfishes were sorted, identified and counted
from a total of 53 zooplankton samples collected in
winter and 64 samples collected in spring. Taxonomic
identifications were done using specialised
bibliographies (mainly Kramp, 1959, 1968; Bouillon,
1999). The specific abundance was expressed in
individuals per 1000 m3 (ind 1000 m-3), based on the
water volume filtered through the net. Seasonal and
vertical patterns were determined considering only the
dominant species (> 5% of the specimen total) in
winter and spring. The vertical distribution was
expressed according to the specimen percentage
collected per stratum with respect to the total of
specimens in the water column and its graphical
representation was associated to the salinity values,
which is the parameter with higher vertical variability
in inner waters (Palma et al., 2007). The specific
richness index, which is the number of species in a
community and the Shannon-Wiever diversity index,
was used for the community analysis (Pielou, 1977).
The establishment of areas with higher fauna affinity
was done through the Bray-Curtis similarity analysis
(Bloom, 1981), standardizing the relative abundance
data by the expression log (x+1). Finally, the
relationship between the dominant species abundance
and the oceanographic parameters was analyzed using
the Pearson correlation analysis.
RESULTS
Environmental conditions
Winter cruise
The Moraleda Channel and Boca del Guafo water
columns (Fig. 2a) were almost homothermal, with
temperatures around 9C. Salinity showed a highly
362 Lat. Am. J. Aquat. Res.
stratified low saline (29-33 psu) surface layer (0-25
m), but with a nearly homogeneous high oxygen
content (> 6 mL L1), whereas the deep layer (25 m to
bottom) was less stratified than the surface one, being
more saline (32-34 psu) and less oxygenated (3-5 mL
L1).
At the Costa Channel (Fig. 2a), a vertical
stratification was present, with a surface layer with
low temperature (> 9.5C) and salinity (25-29 psu),
thus giving rise to a strong halocline. The deep layer
was comparatively slightly warmer (> 9.5C) and
more saline (29-32 psu). The oxygen content in the
whole water column was nearly homogeneous ( 6
mL L1). At the Elefantes Fjord (Fig. 2a), the water
column was almost vertically mixed, with low
temperatures ( 8 C) and salinities (22-28 psu,
depending on the station location) and high dissolved
oxygen content ( 6 mL L1). Aysn Fjord surface
layer was highly stratified, with a shallow inverted
thermocline and a normal halocline, both stronger at
its head (Fig. 2a). In this fjord, the surface layer was
cool (7-9C) and less saline (10-29 psu), but with a
high dissolved oxygen content (6-9 mL L1). The deep
layer was comparatively warmer (9-11C), more saline
(29-31 psu), and less oxygenated (2-5 mL L1).
Spring cruise
The water columns of both Moraleda Channel and
Boca del Guafo (Fig. 2b) were slightly homothermal,
with temperatures around 9-10C. The salinity,
showed a highly stratified low saline (28-32 psu)
surface layer, but with a nearly homogenoeus high
oxygen content (> 6 mL L1), whereas the deep layer,
was less stratified than the surface one, being more
saline (29-34 psu) and less oxygenated (4-6 mL L1).
At the Costa Channel (Fig. 2b), a vertical
stratification occurred, with a surface layer with low
temperatures (> 9.5 C), salinities (27-31 psu), and
high dissolved oxygen (> 6 mL L1). The deep layer
was comparatively cooler (< 9.5 C) and more saline
(29-31 psu). The oxygen content in the whole water
column was nearly homogeneous ( 6 mL L1). At the
Elefantes Fjord (Fig. 2b), the water column was
almost vertically homogeneous, with low temperatures
( 9C) and salinities (22-28 psu, depending on the
station location), and high dissolved oxygen ( 6 mL
L1). Aysn Fjord surface layer was highly stratified
(Fig. 2b), with a strong shallow halocline (10-29 psu).
In this fjord, the surface layer was also almost
homothermal ( 9C), with high dissolved oxygen (6-
7 mL L1). The deep layer was comparatively warmer
(9-10C), more saline (29-31 psu), and less
oxygenated (2-5 mL L1).
Seasonal faunistic composition and distribution
patterns
In all, thirty medusa species (21 in winter and 30 in
spring) were identified in the studied area (Table 1).
Sixty seven percent of the species were collected
during both periods, with a larger richness of species
in spring. Jellyfish abundance significantly varied
between winter and spring, being higher on the latter
season. The hydromedusae Bougainvillia macloviana,
Hybocodon chilensis, Hydractinia tenuis, Laodicea
pulcra, L. undulata, Modeeria rotunda and the
scyphomedusa Chrysaora plocamia were recorded for
the first time for this geographical area. During spring,
ephirae probably of C. plocamia, were collected at
26% on the analyzed oceanographic stations.
Winter cruise
The jellyfish number during winter ranged between 17
and 1630 ind 1000 m-3, with an average of 442 ind
1000 m-3. The highest densities were recorded in the
central area of the Moraleda Channel and Aysn
Fjord. Dominant species were Bougainvillia muscus
(29.7%), B. muscoides (28.8%), Cunina peregrina
(7.5%), Amphogona apicata (6.8%), Hydractinia
borealis (6.1%) and Rhopalonema velatum (5.4%).
The highest occurrence of frequency percentages (>
70%) included B. muscoides (84%), B. muscus (74%)
and C. peregrina (74%) (Table 1).
Bougainvillia muscus (= B. pyramidata) was the
most abundant and more frequent species (an average
of 138 ind 1000 m-3) although it was not observed in
both transect ends (Fig. 3a). The highest densities
were recorded in the central area of the Moraleda
Channel and close to the Aysn Fjord, reaching a
maximum at station 45 (464 ind 1000 m-3). The other
species belonging to the same genus, B. muscoides,
showed a mean of 134 ind 1000 m-3 and was the most
common species during winter. The higher densities
were obtained in the same areas as for B. muscus, with
a maximum of 605 ind 1000 m-3 close to the head of
Aysn Fjord (Fig. 3b). Among the remaining species,
C. peregrina was the only species found at both ends
of the transect; additionally, A. apicata, H. borealis
and R. velatum showed a more reduced geographical
distribution and none was collected at the Elefantes
Fjord, especially A. apicata, whose populations were
mainly concentrated at the Aysn Fjord, an area where
all species showed the highest densities (Figs. 3c-3f).
Spring cruise
Abundance in spring ranged between 68 and 35,616
ind 1000 m-3 at stations 49 and 80, respectively, with
an average of 3,667 ind 1000 m-3. The highest
densities were recorded in the north of Moraleda
 Distribution of medusae in Aysn region, southern Chile 363

Figure 2. Vertical distribution of temperature, salinity and dissolved oxygen between Boca del Guafo to Elefantes Fjord.
a) Winter 2007, b) Spring 2007.
Figura 2. Distribucin vertical de temperatura, salinidad y oxgeno disuelto entre Boca del Guafo y fiordo Elefantes.
a) invierno 2007, b) primavera 2007.

Channel, at Aysn Fjord and the head of the Elefantes
Fjord. The dominant species were B. muscoides
(34.1%), Proboscidactyla ornata (17.5%), Clytia
simplex (10.8%), A. apicata (7.2%) and P. stellata
(7.2%). Except for A. apicata (39%), which was not
collected at the stations located at the Boca de Guafo
and Moraleda Channel, all the remaining species
showed high occurrence frequency percentages: P.
ornata (100%), C. simplex (100%), P. stellata (100%)
and B. muscoides (96%) (Table 1).
B. muscoides was the only dominant species during
both seasons, being extremely abundant in spring,
reaching a mean of 1,602 ind 1000 m-3 and a
maximum of 24,365 ind 1000 m-3 (Stat. 80) near the
head of the Aysn Fjord (Fig. 4a).
Proboscidactyla ornata showed a high frequency
and abundance, with a mean of 974.6 ind 1000 m-3 and
maximums close to the head of both Aysn and
Elefantes fjords (Fig. 4b). Clytia simplex presented a
wide geographical distribution, with mean densities of
601.0 ind 1000 m-3 and two nuclei of high
concentration at the Corcovado Gulf and Elefantes
Fjord (Fig. 4c). Amphogona apicata, with a mean
density of 401.8 ind 1000 m-3, was found with low
frequency and abundance at all oceanographic
stations, except close to the head of Aysn Fjord,
 364

Table 1. Total abundance, mean abundance, percentage of abundance and frequency of occurrence of species collected between the Boca del Guafo and Elefantes
Fjord. The asterisk (*) indicates the first records for this area.
Tabla 1. Abundancia total, abundancia promedio, porcentaje de abundancia y frecuencia de ocurrencia de las especies colectadas entre la Boca del Guafo y fiordo
Elefantes. El asterisco (*) indica las especies registradas por primera vez en esta rea.

Winter Spring
Species Total abundance Mean abundance Percentage Frequency Total abundance Mean abundance Percentage Frequency
(ind 1000 m-3) (ind 1000 m-3) (%) (%) (ind 1000 m-3) (ind 1000 m-3) (%) (%)
Hydromedusae
Amphinema rugosum - - - - 221 9.6 0.2 35
Amphogona apicata 602 31.7 6.8 42 9242 401.8 7.2 39
Bougainvillia macloviana* - - - - 170 7.4 0.1 17
Bougainvillia muscoides 2551 134.3 28.8 84 43752 1902.3 34.1 96
Bougainvillia muscus 2628 138.3 29.7 74 4893 212.7 3.8 65
Bougainvillia sp. 193 10.1 2.2 53 1792 78.0 1.3 26
Clytia simplex 68 3.6 0.8 32 13824 601.0 10.8 100
Coryne eximia 207 10.9 2.3 58 1235 55.6 1.0 65
Cunina peregrina 661 34.8 7.5 74 2658 115.6 2.1 30
Ectopleura dumortieri - - - - 739 32.1 0.6 52
Euphysa aurata 121 6.4 1.4 37 671 29.2 0.5 39
Gossea brachymera - - - - 10 0.4 0.0 4
Halopsis ocellata - - - - 715 31.1 0.6 26
Heterotiara sp. 12 0.6 0.1 11 566 24.6 0.4 4
Lat. Am. J. Aquat. Res.

Hybocodon chilensis* 53 2.8 0.6 32 577 25.1 0.4 52

Hydractinia borealis 539 28.4 6.1 68 4755 206.7 3.7 100
Hydractinia tenuis* 198 10.4 2.2 47 1663 72.3 1.3 78
Laodicea pulcra* - - - - 22 0.9 0.0 13
Laodicea undulada* - - - - 153 6.6 0.1 17
Leuckartiaria octona 127 6.7 1.4 58 1750 76.1 1.4 78
Modeeria rotunda* - - - - 848 36.8 0.7 61
Obelia spp. - - - - 953 41.5 0.7 61
Proboscidactyla ornata 91 4.8 1.0 42 22415 974.6 17.5 100
Proboscidactyla stellata 17 0.9 0.2 16 9217 400.8 7.2 100
Rophalonema velatum 475 25.0 5.4 58 192 8.3 0.2 26
Sarsia coccometra 4 0.2 0.1 5 569 24.7 0.4 65
Solmundella bitentaculata 278 14.6 3.1 32 1536 66.8 1.2 30
Total 8652 125604
Scyphomedusae
Chrysaora plocamia* - - - - 758 32.9 0.6 52
Ephyrae 21 1.1 0.2 16 185 8.0 0.1 26
 Distribution of medusae in Aysn region, southern Chile 365

Figure 3. Winter distribution of dominant species. a) Bougainvillia muscus, b) B. muscoides, c) Cunina peregrina,
d) Amphogona apicata, e) Hydractinia borealis, f) Rhopalonema velatum.
Figura 3. Distribucin invernal de las especies dominantes. a) Bougainvillia muscus, b) B. muscoides, c) Cunina
peregrina, d) Amphogona apicata, e) Hydractinia borealis, f) Rhopalonema velatum.

where the highest concentrations were recorded (Fig.
4d). Finally, P. stellata showed a high occurrence
frequency, with mean densities slightly inferior to A.
apicata (400.8 ind 1000 m-3), with maximums near the
heads of Aysn Fjord and Elefantes Fjord (Fig. 4e).
Similarity analysis
Based on the Bray-Curtis similarity analysis, two
groups of stations were distinguished in winter (Fig.
5a): a) the group A, involving most of the stations
located at the Corcovado Gulf, Moraleda channels and
Aysn Fjord, which are characterised by high densities
of B. muscus and B. muscoides, and high frequencies
of A. apicata, H. borealis and R. velatum; and b) the
group B, formed exclusively by the stations located at
the Costa Channel and Elefantes Fjord, which were
characterised by the presence of C. peregrina and the
absence of many species that were only distributed
until the Maninea Constriction-sill.
366 Lat. Am. J. Aquat. Res.

Figure 4. Spring distribution of dominant species. a) Bougainvillia muscoides, b) Proboscidactyla ornata, c) Clytia
simplex, d) Amphogona apicata, e) P. stellata.
Figura 4. Distribucin primaveral de las especies dominantes. a) Bougainvillia muscoides, b) Proboscidactyla ornata,
c) Clytia simplex, d) Amphogona apicata, e) P. stellata.

Like for the winter, during the spring, two groups of
stations were also distinguished (Fig. 5b): a) the group
A, formed by most stations located at the Corcovado
Gulf, Moraleda Channel and Aysn Fjord, where high
densities of all dominant species were established (A.
apicata, B. muscoides, C. simplex, P. ornata, P.
stellata); and b) the group B, comprising the stations
located at the Elefantes Fjord, where minimums of
abundance for all dominant species were recorded.
Species richness and diversity
The species richness in winter ranged between 1 and 7
species per station, with an average of 5 species. The
highest values were recorded at the Moraleda Channel
and Aysn Fjord, while the lowest occurred at the
Boca de Guafo, Costa Channel and Elefantes Fjord
(Fig. 6a). Conversely, spring showed a higher species
richness, ranging from 5 to 17 species per station, with
an average of 12. The highest values were recorded at
 Distribution of medusae in Aysn region, southern Chile 367

Figure 5. Similarity dendrograms based on Bray-Curtis Index between the sampling stations. a) Winter, b) Spring.
Figura 5. Dendrogramas de similitud basados en el ndice de similitud de Bray-Curtis entre las estaciones analizadas.
a) invierno, b) primavera.

the Corcovado Gulf, southern area of the Moraleda
Channel, Aysn and Elefantes fjords.
The Shannon-Weaver specific diversity rate showed
the values ranged between 0.2 and 3.4 bits during
winter, with maximums at the Corcovado Gulf and
Moraleda Channel (Fig. 6b). In spring, however, these
values ranged between 0.9 and 3.2 bits, with a main
maximum at the Boca de Guafo, followed by high
values at the Costa Channel and Elefantes Fjord.
Correlation coefficient
The results of the Pearson correlation index (P < 0.05)
showed that the abundance of A. apicata, B.
muscoides, C. peregrina and R. velatum was
positively correlated with temperature. The abundance
of A. apicata, C. peregrina and R. velatum was,
however, negatively correlated with the concentration
of the disolved oxygen (Table 2). During summer, the
Pearson index (P < 0.05) showed, in general, a limited
correlation between species and oceanographic
parameters. Only the abundance of P. ornata was
observed to show a negative correlation with the
temperature, and the abundance of A. apicata showed
a negative correlation with the dissolved oxygen
(Table 2).
Vertical distribution
Winter Cruise
In general, the vertical distribution showed that the
dominant species were mainly distributed under 25 m
deep during the winter (Fig. 7). The most superficial
species was H. borealis, which was generally found in
the first 50 m, with a higher abundance at the 25-50 m
stratum. C. peregrina, A. apicata, and R. velatum were
collected at greater depth, with abundance maximums
at the 50-100 m stratum. Meanwhile, the species of the
genus Bougainvillia, B. muscus and B. muscoides
showed a wider vertical distribution between the
surface and 100 m of depth, with the highest specimen
percentage above 25 m.
368 Lat. Am. J. Aquat. Res.

Figure 6. a) Species diversity, b) richness species during the CIMAR 13 Fjords Cruise.
Figura 6. a) Diversidad especfica, b) riqueza de especies durante el Crucero CIMAR 13 Fiordos.

Table 2. Pearson correlation values between the abundance of dominant species and the oceanographic variables in winter
cruise. Significant values are indicated in bold (P < 0.05).
Tabla 2. Valores correlacin de Pearson entre la abundancia de las especies dominantes y las variables oceanogrficas en
el crucero de invierno. Los valores significativos se indican en negrita (P < 0,05).

Temperature Salinity D. oxygen A. apicata B. muscoides B. muscus C. peregrina H. borealis R. velatum

Temperature 1.00
Salinity 0.33 1.00
Oxygen -0.91 -0.20 1.00
A. apicata 0.56 0.02 -0.67 1.00
B. muscoides 0.29 -0.21 -0.28 0.23 1.00
B. muscus 0.16 -0.20 -0.09 -0.09 0.62 1.00
C. peregrina 0.28 -0.24 -0.46 0.82 0.12 -0.16 1.00
H. borealis 0.16 -0.18 -0.15 -0.03 0.68 0.73 -0.12 1.00
R. velatum 0.27 0.22 -0.37 0.60 0.17 -0.07 0.56 -0.19 1.00

Temperature Salinity D. oxygen

A. apicata 0.01 0.44 0.99
B. muscoides 0.02 0.94 0.98
B. muscus 0.13 0.93 0.75
C. peregrina 0.02 0.95 0.99
H. borealis 0.14 0.9 0.85
R. velatum 0.03 0.94 0.9
 Distribution of medusae in Aysn region, southern Chile 369

Figure 7. Vertical distribution of dominant species in winter. a) Bougainvillia muscus, b) B. muscoides, c) Cunina
peregrina, d) Amphogona apicata, e) Hydractinia borealis, f) Rhopalonema velatum. Grey columns: diurnal tows, black
colums: nocturnal tows.
Figura 7. Distribucin vertical de las especies dominantes en invierno. a) Bougainvillia muscus, b) B. muscoides,
c) Cunina peregrina, d) Amphogona apicata, e) Hydractinia borealis, f) Rhopalonema velatum. Columnas en gris:
muestreos diurnos, columnas en negro: muestreos nocturnos.

Spring Cruise nata and P. stellata) showed a wide bathymetric

Only Amphogona apicata was collected under 50 m, distribution (0-100 m). In the latter group, only C.
both in spring and winter (Fig. 8), while the other simplex showed a continuous distribution in the water
dominant species (B. muscoides, Clytia simplex, P. or- column (0-100 m) in the longitudinal transect. Addi-
370 Lat. Am. J. Aquat. Res.

Figure 8. Vertical distribution of dominant species in spring. a) Bougainvillia muscoides, b) Proboscidactyla ornata,
c) Clytia simplex, d) Amphogona apicata, e) P. stellata. Grey columns: diurnal tows, black columns: nocturnal tows.
Figura 8. Distribucin vertical de las especies dominantes primaveral. a) Bougainvillia muscoides, b) Proboscidactyla
ornata, c) Clytia simplex, d) Amphogona apicata, e) P. stellata. Columnas en gris: muestreos diurnos, columnas en negro:
muestreos nocturnos.

tionally, B. muscoides, P. ornata and P. stellata were
absent and collected at low densities in the surface
stratum (0-25 m) along the Moraleda Channel.
DISCUSSION
Environmental conditions
During winter and spring cruises, the vertical
distribution of salinity, which govern the density
structure in the study area, showed a stratified
distribution consisting of two layers: a surface layer (
25 m), more variable in temperature and salinity, and
therefore in density, frequently presenting thermo-
clines and/or haloclines, and a deep layer (from ca. 25
m to the bottom), less variable, being occasionally
almost homothermal and/or homohaline (Fig. 2). The
intensity of this vertical stratification showed a
latitudinal gradient, being less intense at the Boca del
 Distribution of medusae in Aysn region, southern Chile
Guafo, where the oceanic influence is higher, and
more intense at the Aysn and Elefantes fjords, where
the freshwater input from continental rivers and
glacier melting are more relevant (Palma & Silva
2004; Calvete & Sobarzo, 2011) .
Seasonally, the water column temperature showed
minor seasonal differences (< 1C) between both
seasons, with the exception of Aysn Fjord surface
layer, where this difference increased up to almost
3C. The Aysn Fjord winter cooler surface water, due
to the input of winter coldest river fresh water, gave
origin to an inverted thermocline, which was not
observed during spring, as the surface water was
warmer (Fig. 2), but not enough to form a normal
thermocline. This variation of the temperature
corresponds to a normal seasonal fluctuation pattern
for the Aysn Fjord, as established by Silva et al.
(1997).
In both seasonal cruises, surface layer salinities of
Moraleda-Costa Channels and Elefantes-Aysn fjords,
remained lower than at the bottom layer (Fig. 2),
giving origin to a surface strong halocline, and
consequently to a very stable water column. Even
though the study area shows seasonal differences in
river water input (Calvete & Sobarzo, 2011), being
higher inspring than in winter, the water column
salinity did not show significant differences between
cruises, which were generally low ( 1 psu; Fig. 2). A
possible explanation for this lack of differences may
be associated to a similar river flow during the days
preceding the sampling.
The water column stratification was lower at the
Boca del Guafo than at the Moraleda-Aysn-Costa
channels, where the surface/bottom salinity
differences in the former were low ( 1 psu v/s 3-20
psu; Fig. 2). At the stations 50 to 52 in the Elefantes
Fjord, an almost vertical homogeneous structure was
present (Fig. 2), giving origin to a much less stable
water column, compared with the rest of the study
area. These differences are a characteristic oceano-
graphic pattern of the Aysn area, since it has been
observed in most of the cruises performed in this area
(Silva et al., 1997; Calvete & Sobarzo, 2011).
Dissolved oxygen in the surface layer of Boca del
Guafo-Moraleda Channel was well oxygenated and
with similar contents in both cruises (> 6 mL L1).
Beneath the surface layer, around 100 m, the dissolved
oxygen dropped below 4 mL L1 (Fig. 2), due to
consumption caused by the degradation of autoch-
thonous and allochthonous particulate organic matter
coming from the surface layer (Silva, 2008). Low
oxygen concentrations (2-4 mL L1) have been
recorded at mid depth close to the head of Aysn
Fjord ( 75-150 m; Fig. 2). Similar low dissolved
371
oxygen content has been also recorded in Reloncav,
Puyuguapi, Quitralco, and Cupqueln fjords, all of
which, as in Aysn Fjord, receive fluvial contributions
carrying particulate organic matter (Silva et al., 1997;
Silva & Guzmn, 2006).
Two oceanic water masses were detected adjacent
to the Chilo zone, between the surface and 300 m
depth: Subantarctic Water (SAAW) above 150 m, and
remnants of Equatorial Subsurface Water (ESSW)
between 150 and 300 m.
Both of these water masses penetrate into the
region mainly through the Boca del Guafo, the SAAW
through the surface and the ESSW through the
subsurface layer, spreading as far as the bathymetry of
the gulfs and channels allows them. As the SAAW
penetrates, it mixes with the fresh water (FW) in
different proportions, according to the contributions
from rivers, glaciers, coastal runoff, pluviosity, and
the distance or proximity of the FW sources (Sievers
& Silva, 2008). The water resulting from this process,
having salinities between 31 and 33 psu, is known as
Modified Subantarctic Water (MSAAW) and the
lower-salinity water to as Estuarine Water (EW). The
ESSW enters by the subsurface (below 150 m), but its
displacement to the inland region is limited by the
submarine topography and, when it reaches the
Menina constriction-sill (50-60 m high), it does not
allow the ESSW to go further south into the Aysn-
Elefantes fjords (Fig. 2), thus impeding the passage of
ESSW with low dissolved oxygen content towards the
southern microbasins.
Jellyfish species composition
Thirty jellyfish species were recorded at the Aysn
region, which involves the area between the Boca del
Guafo and the Elefantes Fjord, a quantity very similar
(30 species) to that recorded in the same area in spring
2002 and 2003 (Table 4; Palma et al., 2007a, 2007b).
Seven out of the total species identified correspond to
new records for the study area (Bougainvillia
macloviana, Hybocodon chilensis, Hydractinia tenuis,
Laodicea pulcra, L. undulata, Modeeria rotunda and
Chrysaora plocamia) (Table 1). It is worth noting the
presence of C. plocamia from this group of species,
which showed a marked increase in the ephyrae
(probably of C. plocamia) and adult quantities (Table
1). This species is currently more frequently found in
inner waters and sometimes, as in February-June
2002, it has represented a negative effect on salmon
cage farming in Chilo (S. Palma, unpublished).
Jellyfish fauna of the inner waters is made up by
common species of the ecosystems of the southern
channels and fjords between Puerto Montt and the
372 Lat. Am. J. Aquat. Res.
Cape Horn (genera Bougainvillia, Hybocodon,
Hydractinia and Proboscidactyla) (Pags & Orejas,
1999; Galea, 2006, 2007; Galea et al., 2007; Palma et
al., 2007a, 2007b, 2011; Villenas et al., 2009a), as
well as diverse common species in subantarctic waters
from the Humboldt Current System (genera
Amphogona, Clytia, Coryne, Ectopleura, Obelia,
Rhopalonema, Sarsia and Solmundella) (Fagetti,
1973; Palma, 1994; Palma & Rosales, 1995; Palma &
Apablaza, 2004), which have penetrated and settled
with more or less success in the inner zone of the
Chilean Patagonia fjords, and where some of them
prove quite frequent and abundant (Table 4). Some
subantarctic species have successfully populated inner
waters, adapting to a highly stratified environment,
with a low salinity (3-32 psu), surface layer ( 25 m),
generally avoided by many species that spread in the
deep, more homogeneous and saline (32-34 psu) layer,
as shown by the vertical distribution patterns in both
seasons (Figs. 7 and 8).
Seasonal distributions patterns of jellyfish
A high seasonal difference in the jellyfish abundance
was determined, which was 14 times higher in spring
with respect to winter (Table 1). Sixty four species
were common for both seasons, which entails a
significant change in the seasonal specific
composition. A latitudinal increase in the abundance
was detected in winter, from Boca del Guafo up to the
Aysn Fjord, where the abundance maximums were
recorded. Such latitudinal variation may be associated
to the constant entrance of SAAW that mixes with the
EW, causing less vertical stability in the water column
of the northern sector (Boca del Guafo, Corcovado
Gulf and northern area of the Moraleda Channel)
(Silva & Guzmn, 2006), and a higher stability in the
southern zone (Aysn and Elefantes fjords), where the
continental freshwater input is higher. In spring,
however, no geographical distribution pattern was
observed, as there is a generalized abundance in the
whole study area probably due to a higher trophic
availability as a result of the elevated biological
productivity caused by a larger solar radiation and
temperature increase typical of the beginning of the
summer period (Gonzlez et al., 2011), which
promotes jellyfish reproduction and proliferation in
the study area.
In all oceans, it has been observed that seasonal
fluctuations of temperature play a fundamental role in
the zooplankton composition and abundance,
promoting the proliferation of various species,
particularly juvenile stages (Parsons & Lalli, 2002;
Kehayias, 2004). These seasonal changes are quite
marked for jellyfishes due to their reproductive cycles,
which mainly occur in spring and summer, when the
asexual reproduction is influenced to a greater extent
by temperature increases (Palma, 1994; Palma &
Rosales, 1995; Bouillon, 1999). In fact, the Pearson
analysis showed significant positive correlations (P >
0.5) between the abundance of some dominant species
and the temperature values (Table 2). These
abundance fluctuations have also been ascribed to the
trophic availability and inter-specific competence in
highly productive systems (Edwards & Richardson,
2004). Studies on inner waters have shown a high
biological productivity in inner waters during spring,
especially in the Moraleda Channel, reflected in high
primary productivity values and zooplanktonic
biomass (Palma & Silva, 2004; Gonzlez et al., 2011).
Besides, it has also been suggested the simultaneous
occurrence of two or more species in the community
reflects some degree of consistency in the ecological,
environmental or biological requirements with a
tendency to form more or less compact groups
according to their requirement similarities (Lie et al.,
1983; Gasca et al., 1996). This is also observed in this
zone, where a positive association among various
dominant species sharing their spatial and vertical
distribution was seen, such as the species belonging to
genera Bougainvillia and Proboscidactyla (Figs. 4 and
8). Among the most abundant species, only
Bougainvillia muscoides and Amphogona apicata
showed dominance in both seasons. B. muscoides was
highly abundant, with high dominance percentages in
winter (28.84%) and spring (34.14%), a period where
its abundance was highly superior to that observed in
winter (Table 1). This species was gathered at the
stations remote from the influence of the SAAW, and
presented its maximums at the Aysn Fjord, under 50
m thus avoiding the low salinity EW superficial layer.
Such distribution pattern of B. muscoides supports
results obtained in the same geographical area (Palma
et al., 2007a, 2007b), as well as in all the southern
ecosystem of inner waters (Pags & Orejas, 1999;
Villenas et al., 2009a; Palma et al., 2011).
In both seasons A. apicata showed a limited
frequency as it was generally absent in areas with
higher temperature and salinity, and the maximums
were recorded at the Aysn Fjord (Figs. 3 and 4). Its
presence in this area confirms its wide distribution in
the northern ecosystem of interior waters (Palma et
al., 2007a, 2007b; 2011; Villenas et al., 2009a). This
is a common species in tropical and subtropical waters
in all oceans (Segura-Puertas, 1984), and has a wide
distribution in the northern area of the Humboldt
Current System (HCS) (Pags et al., 2001; Palma &
Apablaza, 2004; Apablaza & Palma, 2006).
 Distribution of medusae in Aysn region, southern Chile 373

It may be pointed out that except the other
dominant species collected in both winter and spring,
the presence of Bougainvillia muscus, Cunina
peregrina, Hydractinia borealis, Rhopalonema
velatum, Clytia simplex, Proboscidactyla ornata and
P. stellata confirms the results previously obtained for
this geographical area (Palma et al., 2007a, 2007b), as
well as those obtained for the northern sector
(Reloncavi Fjord to Boca del Guafo) (Villenas et al.,
2009a; Palma et al., 2011). It is worth noting about
this group that most of the species are common to
inner waters, except for R. velatum which is quite
uncommon, although widely spread in HCS oceanic
and Cape Horn current subantarctic waters (Kramp,
1966; Fagetti, 1973; Pags & Orejas, 1999; Pags et
al., 2001; Palma & Apablaza, 2004).
Diversity values were slightly superior in winter,
although the species richness was higher (58%) in
spring. Such obvious contradiction may be explained
by the strong increase of almost all jellyfish species
during spring (> 14 times), which results in a
disguising of the diversity values, as the Shannon-
Wiever index includes the specific abundance, which
was extremely high for Bougainvillia muscoides,
Proboscidactyla ornata, P. stellata and Clytia simplex.
The higher diversity values during both seasons (> 3.2
bits) was recorded at the Moraleda Channel, which
receives a regular supply of SAAW from the adjacent
Pacific, thus promoting the entry of oceanic species
not common in interior waters, thus increasing their
diversity, confirming the results by Palma & Rosales
(1997) and Palma et al. (2007a). The lower diversity
(< 1 bits) and specific richness values were recorded at
the Elefantes Fjord, where the low salinity,
temperature and stratification conditions prevailed,
which affected not only the abundance, but also the
diversity and species richness (Fig. 6).
In general, it has been shown that the vertical
distribution of jellyfishes in all the analyzed area
showed a preference for deeper strata (> 25 m), thus
avoiding the superficial and more stable layer of EW,
though low in salinity, that characterizes the
superficial stratum (0-25 m). The latter was especially
obvious for those species typical of HCS oceanic
subantarctic waters (A. apicata, C. peregrina, R.
velatum; Figs. 7 and 8), which were distributed at
greater depths (> 50 m). The deeper distribution of A.
apicata is consistent with the negative association
observed in winter and the dissolved oxygen
concentration (r = -0.67; Table 2), especially at the
Aysn Fjord, where its abundance maximums were
observed in winter and spring. A positive association
among species from the same genus was observed at
depth, such as Bougainvillia muscoides and B. muscus
(r = 0.62; Table 2), Proboscidactyla ornata and P.
stellata (r = 0.69; Table 3), which coexisted in the
water column in winter and spring, respectively.
Furthermore, it has been pointed out that P. stellata is

Table 3. Pearson correlation values between the abundance of dominant species and the oceanographic variables in spring
cruise. Significant values are indicated in bold (P < 0.05).
Tabla 3. Resultados del anlisis de correlacin de Pearson entre la abundancia de las especies dominantes y las variables
oceanogrficas en el crucero de primavera. Los valores significativos se indican en negrita (P < 0,05).

D. oxygen Salinity Temperatura A. apicata B. muscoides C.simplex P. ornata P. stellata

Oxygen 1.00
Salinity -0.,44 1.00
Temperature 0.03 0.33 1.00
A. apicata -0.48 0.03 0.10 1.00
B. muscoides 0.10 -0.46 -0.22 -0.01 1.00
C. simplex 0.22 0.00 0.14 -0.04 0.09 1.00
P. ornata 0.22 -0.55 -0.15 -0.01 0.57 0.32 1.00
P. stellata -0.15 -0.42 -0.13 0.55 0.39 0.27 0.69 1.00

Temperature Salinity D. oxygen

A. apicata 0,21 0,41 1,00
B. muscoides 0,96 1,00 1,00
C. simplex 0,13 0,50 0,04
P. ornata 0,88 1,00 0,04
P. stellata 0,84 1,00 0,87
374 Lat. Am. J. Aquat. Res.

Table 4. Mean abundance (ind 1000 m-3) in the springs 2002, 2003 and 2007 and winter 2007 between Boca del Guafo
and Elefantes Fjord. Data for springs 2002 (Palma et al., 2007a), 2003 (Palma et al., 2007b) and 2007 (present study). (-):
Species not registered.
Tabla 4. Abundancia media (ind 1000 m-3) en las primaveras 2002, 2003 y 2007 e invierno 2007 entre Boca del Guafo y
fiordo Elefantes. Datos de primavera 2002 (Palma et al., 2007a), 2003 (Palma et al., 2007b) y 2007 (presente estudio). (-):
Especies no registradas.

Spring Spring Spring Winter

Species 2002 2003 2007 2007
Hydromedusae
Aglaura hemistoma 1.5 - - -
Amphinema rugosum 2.2 - 9.6 -
Amphogona apicata 413.9 440.9 401.8 31.7
Bougainvillia macloviana - - 7.4 -
Bougainvillia muscoides - 107.9 1902.3 134.3
Bougainvillia muscus - 1.92 212.7 138.3
Bougainvillia sp. 60.9 80.9 - -
Calycopsis sp. - 0.4 - -
Clytia simplex 882.1 699.2 601.0 3.6
Coryne eximia 1.3 2.8 55.6 10.9
Cunina peregrina 2.9 1.1 115.66 34.8
Cunina sp. - 4.4 - -
Dipurena ophiogaster 0.2 - - -
Ectopleura dumortieri 0.4 63.7 32.1 -
Euphysa aurata 23.7 178.2 29.2 6.4
Gossea brachymera - 4.0 0.4 -
Halopsis ocellata 13.3 17.4 31.1 -
Heterotiara minor 0.3 - 24.6 0.6
Hydocodon chilensis - 90.0 25.1 2.8
Hydractinia borealis 7.3 163.5 206.7 28.4
Hydractinia tenuis - - 72.3 10.4
Laodicea pulchra - - 0.9 -
Laodicea undulata - - 6.6 -
Leuckartiaria octona 14.4 21.7 76.1 6.7
Liriope tetraphylla 10.0 55.2 - -
Lizzia blondina 7.9 26.0 - -
Modeeria rotunda - - 36.8 -
Obelia spp. 135.0 20.1 41.5 -
Phialella quadrata 26.3 14.0 26.0 0.2
Proboscidactyla mutabilis 3.1 6.5 72.2 0.9
Proboscidactyla ornata 56.2 527.4 974.6 4.8
Proboscidactyla stellata 10.0 195.9 400.8 0.9
Proboscidactyla sp. - 39.2 - -
Rophalonema velatum 27.6 20.9 8.3 25.0
Sarsia coccometra - 4.8 24.7 0.2
Solmundella bitentaculata 611.3 380.8 66.8 14.6
Scyphomedusae
Chrysaora plocamia - - 32.9 -
Ephyrae - - 8.0 1.1
 Distribution of medusae in Aysn region, southern Chile
an euryhaline species common in cold waters of the
Irish coast where, during the year, concentrates under
20 m depth (Ballard & Myers, 1997). It has been
observed in some planktonic species that the
bathymetric distribu-tion tends to favour the
reproductive processes of some species (i.e. Sagitta
tasmanica) (Villenas et al., 2009b), as it may also
represent a strategy to reduce the mortality rates, thus
decreasing predation and loss by planktonic species
advection (Gorsky et al., 2000).
ACKNOWLEDGEMENTS
This work was supported by Servicio Hidrogrfico de
la Armada through projects CONA-C13F 07-04 and
CONA-C13F 07-07 Comit Oceanogrfico Nacional.
We are indebted to the crew of the AGOR Vidal
Gormaz, who greatly facilitated sampling and field
work. We also thank Mara Ins Muoz, who was in
charge of all zooplankton sampling at sea, Pablo
Crdova for his support in the identification of
medusae, as well as, Paola Reinoso who performed
the dissolved oxygen analyses in the laboratory. We
are also indebted to two anonymous reviewers for
helping us to improve the paper.
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DOI: 10.3856/vol39-issue2-fulltext-18

Short Communication

Crecimiento del camarn excavador Parastacus pugnax (Poeppig, 1835)

determinado mediante tcnica de marcaje

Mauricio Ibarra1 & Patricio M. Arana1

1
Escuela de Ciencias del Mar, Pontificia Universidad Catlica de Valparaso
P.O. Box 1020, Valparaso, Chile

RESUMEN. Para determinar el crecimiento en el camarn excavador (Parastacus pugnax) en la zona centro
sur de Chile se utiliz un marbete tipo cinturn. Los parmetros longitud cefalotorcica asinttica (Lc) y la
velocidad de incremento en longitud y peso (K), se establecieron mediante el mtodo de Gulland & Holt
(1959). El parmetro t0 se determin mediante la ecuacin inversa del modelo de von Bertalanffy,
establecindose que las curvas de crecimiento en longitud y peso fueron definidas por los parmetros K = 0,35
mm ao-1, t0 = -0,38 aos, Lc = 55,9 mm y W = 83,8 g, valores similares a los de Samastacus spinifrons,
especie chilena de alto potencial de cultivo, y de otros parastcidos sudamericanos, tales como P. brasiliensis
y P. deffosus.
Palabras clave: crecimiento, marcaje-recaptura, camarn excavador, Parastacus pugnax, Chile.

Growth of burrowing crayfish Parastacus pugnax (Poeppig, 1835)

determined by marking technique
ABSTRACT. A modified tag belt type was used in the burrowing crayfish (Parastacus pugnax), in the
central-south of Chile. The parameters asymptotic carapace length (Lc) and rate of increase (K) were
determined through the Gulland & Holt (1959) method. The parameter t0 was determined by the inverse
equation of von Bertalanffy model, which allowed to establish that the growth curves in length and weight are
defined by the parameters K = 0.35 mm yr-1, t0 = -0.38 years, Lc = 55.9 mm and W = 83.8 g. These values
were similar to those of Samastacus spinifrons, Chilean species with high potential for aquaculture, and
similar to those of other South American parastacids such as P. brasiliensis and P. deffosus.
Keywords: growth, mark-recapture, burrowing crayfish, Parastacus pugnax, Chile.
___________________
Corresponding author: mauricio.ibarra.m@mail.ucv.cl

La implementacin de la tcnica de marcaje-recaptura
es especialmente importante en el estudio del
crecimiento de crustceos, ya que no presentan
estructuras seas en las que se puedan visualizar
marcas diarias o anuales vs el tiempo, y de este modo
estimar la edad, como ocurre en los peces seos u
otros organismos con estructuras calcreas (Garca &
Le Reste, 1986). Esta tcnica permite individualizar
los ejemplares, y as determinar variaciones de
longitud y/o peso que muestran entre el marcaje y la
recaptura (Parrack, 1979; Kimker et al., 1996;
Ulmestrand & Eggert, 2001; Moser et al., 2002; Le
Vay et al., 2007).
En Chile son escasos los trabajos realizados sobre
el crecimiento de crustceos mediante marcaje-
recaptura (Pavez & Arana, 1982; Riesco, 1984; Arana
& Toro, 1985; Arana & Venturini, 1989; Ernst et al.,
2008). En general, los trabajos se han centrado en
estudios dirigidos a establecer desplazamientos,
abundancia, mortalidad y comportamientos indivi-
duales (Labarca, 1971; Geaghan, 1973; Campodonico
et al., 1983; Campodonico & Lpez, 1988; Arana,
1992; Muoz et al., 2006; Gallardo et al., 2007).
En esta investigacin, se estudi el crecimiento del
camarn excavador o de vega (Parastacus
pugnax), crustceo endmico de Chile, que se
distribuye desde el ro Aconcagua (3250'S, 7059'W)
hasta la localidad de Carahue (3840'S, 7309'W), en
la zona centro-sur del pas (Rudolph, 1997). En
temporadas invernales este recurso es explotado
artesanalmente, como alternativa de ingreso para
agricultores locales (Arias & Muoz, 1991; Rudolph
379 Crecimiento de Parastacus pugnax en la zona centro-sur de Chile

et al., 1991; Rudolph, 1997). Debido al alto nivel de ejemplares marcados se recapturaron 45, equivalente
extraccin a que es sometido y al deterioro sostenido al 27% (Tabla 1).
de su hbitat, ha sido catalogado como vulnerable en Para determinar los parmetros de la curva de
toda su rea de distribucin (Bahamonde et al., 1998; crecimiento K y Lc, se utiliz el mtodo establecido
Rudolph & Crandall, 2007), por lo que es necesario por Gulland & Holt (1959), en machos y hembras,
conocer aspectos de su dinmica poblacional, para donde la tasa de crecimiento declina linealmente
establecer regulaciones en su extraccin y determinar conforme crecen los individuos, alcanzando valor cero
posibilidades de cultivo. cuando llega a su mxima longitud.
Para definir el crecimiento de P. pugnax, se Con la longitud cefalotorcica promedio (Lc(r))
implement la llamada marca o marbete tipo como variable independiente y la variacin de Lc en
cinturn (Fig. 1), que es una adaptacin de las marcas un determinado perodo de tiempo (Lc/t) como
tipo alambre utilizadas por Kourist et al. (1964), variable dependiente, la ecuacin lineal qued
Meyer-Waarden & Tiews (1965) y Tiews (1967) para
representada como Lc/t = a + b Lc , donde K = -b y
el estudio de Crangon crangon. Esta marca tipo
cinturn ha sido utilizada en Chile en camarn de Lc = -a/b. Los parmetros de este modelo lineal
roca, Rhynchocinetes typus (Riesco, 1984) y en fueron obtenidos utilizando el mtodo de Estimadores
camarn de ro del norte, Cryphiops caementarius Mximos Verosmiles (Aldrich, 1997), cuya funcin
(Arana & Toro, 1985), para efectuar estudios de de densidad est dada por:
mortalidad y crecimiento. Esta marca es de bajo costo 1 1 y X T 2
f ( y i / xi ) = exp i i
y fcil de construir, permite identificar indivi- 2 2 2



dualmente a los animales, presenta bajo porcentaje de
desprendimiento, presumiblemente no provoca donde XiT, corresponde a la matriz de (Lc(r))
mortalidad adicional, perdura con las mudas y no transpuesta, yi es el vector de respuestas Lc/t y es
cuenta con protuberancias que interfieran en el el vector de parmetros que se desea estimar. De esta
comportamiento del camarn y lo haga susceptible de forma la funcin de verosimilitud qued definida
sufrir predacin o ser selectivamente vulnerado por los como:
artes o aparejos de pesca.
l ( , 2 , y ) =

( )
n
1 1 2
yi X i
T
exp
2
2
Los muestreos, se efectuaron mensualmente en la i =1 2 2
localidad de Tiuquilemu (3622S, 7652W), ubicada Desarrollando esta funcin, luego derivando
en el extremo norte de la regin centro-sur de Chile, respecto a e igualando a cero, se obtuvo la matriz de
entre agosto 2007 y agosto 2008, exceptuando enero parmetros:
MLE = (X T X ) X T Y
2008, por la escasez de agua existente en el rea de 1
estudio. Para realizar los muestreos, se seleccion un
sector de una vega de 900 m de superficie, donde se Posteriormente se compararon las rectas obtenidas
capturaron y marcaron 166 ejemplares. La marca se empleando el test F(1-; 2; n1+n2-4) (Neter & Wasserman,
confeccion en forma manual, utilizando hilo nailon 1974):
de 0,3 mm de dimetro y pequeos trozos de plsticos SSE CA +TQ SSE T
cilndricos y huecos, obtenidos de envoltura de 2
alambre elctrico de diferentes colores, asignando a F* =
SSE T
cada uno de ellos un dgito. Combinando varios de
n1 + n 2 4
estos se organiz un cdigo numrico que
individualiz cada ejemplar. La marca se coloc donde SSEM+H es la suma del cuadrado de los errores
alrededor del camarn entre el cefalotrax y el primer de la regresin combinada de los ejemplares de ambos
segmento abdominal, cuidando que el cdigo quedase sexos y SSET la suma del cuadrado de los errores de
ubicado en la regin dorsal (Fig. 1). Se procur que los ejemplares de machos y hembras. Para probar la
cada cdigo comenzara con color negro (0), para que igualdad de ambas regresiones se debe cumplir que
la lectura fuese realizada slo desde ese extremo y no F* F(1-; 2; n1+n2-4).
se repiti sucesivamente el mismo color para facilitar
Una vez determinada la Lc asinttica, la estimacin
su diferenciacin.
de t0 se realiz mediante el grfico y la ecuacin
Los individuos fueron extrados desde sus cuevas propuesta por von Bertalanffy (1934) cuya expresin
con bomba de vaco artesanal utilizada para su corresponde a:
captura. En cada ejemplar se registr la longitud
cefalotorcica (Lc), peso (W) y sexo, siendo liberados L(t )
ln 1 = K t0 + K t
en el mismo lugar una vez marcados. De los L
 Lat. Am. J. Aquat. Res. 380

Figura 1. Marbete tipo cinturn colocado entre el cefalotrax y abdomen de Parastacus pugnax.
Figure 1. Tag belt type located between the cephalothorax and abdomen of Parastacus pugnax.

Tabla 1. Nmero de ejemplares muestreados, marcados y recapturados.

Table 1. Namber of individuals sampled, tagged and recaptured.

Fecha de N de ejemplares N de ejemplares N de ejemplares

muestreo muestreados marcados recapturados

10-ago-07 39 39 -
08-sep-07 197 13 1
29-oct-07 212 14 3
21-nov-07 220 17 2
18-dic-07 225 14 3
23-feb-08 242 13 4
26-mar-08 325 11 2
29-abr-08 307 8 6
26-may-08 444 13 3
22-jun-08 479 13 7
27.jul-08 460 11 8
26-ago-08 362 - 6
Total 3.512 166 45

Los resultados obtenidos, mostraron que las rectas defini una regresin lineal, donde el intercepto que
de declinacin de la tasa de crecimiento en el tiempo fue establecido como a = K t 0 . De all, el valor
vs la talla media no variaron significativamente entre estimado de t0 correspondi a -0,38 aos. Con los
machos y hembras (F* = 0,66 < F(1-; 2; n1+n2-4) = 3,21). parmetros determinados, la curva de crecimiento en
De esta forma, el modelo lineal (machos + hembras) longitud qued definida por la ecuacin
qued establecido como Lc / t = 1,63 0,029 Lc
(Fig 2). Los parmetros Lc y K correspondieron a (
Lct mm = 55,9 mm 1 e (0,35 ( mmao ) (t +0,38 aos )) (Fig. 3a).
1
)
55,9 y 0,35 mm ao-1 respectivamente. De acuerdo a la relacin talla-peso determinada por
Ibarra (2010), la curva de crecimiento en peso se
Con la edad t (aos) como variable independiente, represent por la funcin:
la cual fue asignada en forma arbitraria, de acuerdo a
Ibarra (2010), y el logaritmo del lado izquierdo de la
ecuacin como variable dependiente (y), la ecuacin (
Wt g = 83,8 g 1 e (0,35 mmao
1
(t +0,38 aos))
)
2.98
(Fig. 3b).
381 Crecimiento de Parastacus pugnax en la zona centro-sur de Chile

Figura 2. Determinacin de la Lc y K en P. pugnax,

mediante el mtodo de Gulland & Holt (1959).
Figure 2. Determination of Lc and K in P. pugnax, by
Gulland & Holt method (1959).

De acuerdo a los resultados obtenidos, se deduce

que la marca tipo cinturn es adecuada para el estudio
del crecimiento de este camarn, ya que perdura por
perodos de tiempo prolongados. Esto ltimo, se
comprueba porque uno de los ejemplares de P. pugnax
fue extrado nueve meses despus de ser marcado,
permitiendo la lectura de la marca y la identificacin
del individuo sin dificultad, confirmando los
beneficios de esta marca y su utilizacin crustceos de
pequeo tamao.
En general, los parmetros Lc y K obtenidos en P.
pugnax son mayores a los estimados en las especies
brasileas P. defossus (Noro & Buckup, 2009) y P.
brasiliensis (Fries, 1984; Fontoura & Buckup, 1989),
pero inferiores a los determinados en otros crustceos
dulceacucolas explotados comercialmente, como
Procamburus clarkii (Anastcio & Marques, 1995;
Fidalgo et al., 2001; Chiesa et al., 2006; Scalici &
Gherardi, 2007; Scalici et al., 2009), y Cherax
quinquecarinatus (Beatty et al., 2005) (Tabla 2).
Tomando en cuenta los estudios realizados sobre
P. pugnax por Arias & Muoz (1991) y Rudolph
(1997) el valor de Lc estimado en la presente
investigacin, resulta concordante con los valores de
Lc mximos obtenidos en las capturas realizadas por
dichos autores. De esta manera, P. pugnax alcanzara
un peso comercial de 30 g en aproximadamente tres
aos, al igual que Samastacus spinifrons, otro
parastacido chileno, catalogado como de alto potencial
para ser cultivado (Rudolph et al., 2010).
Los parmetros de crecimiento obtenidos podran
ser utilizados en diversos modelos aplicados a futuras
evaluaciones de stocks de esta especie. Cabe
mencionar, que adems de determinar el estado en que
se encuentra este recurso es necesario considerar otros
Figura 3. Curvas de crecimiento (a) en longitud y (b) en
peso, estimadas en P. pugnax.
Figure 3. Growth curves (a) in length and (b) in weight,
estimated in P. pugnax.
factores que afectan a las poblaciones de P. pugnax,
tales como el deterioro de su hbitat (Rudolph &
Crandall, 2007) y la actual aplicacin de un perodo de
veda entre el 1 de diciembre y el 30 de abril de cada
ao (D.S. N145 de abril de 1986), sin contar con
antecedentes acabados respecto a la reproduccin de
esta especie. Esta regulacin igualmente involucra a
otras cinco especies de parastcidos chilenos, medida
que tiene su base en la normativa aplicada al camarn
de ro del norte (Cryphiops caementarius) (Jara et al.,
2006), sin ninguna relacin con estos organismos. Al
igual que lo sealado en S. spinifrons (Rudolph,
2002), la prcticamente inexistente fiscalizacin en la
extraccin permite la comercializacin de hembras
ovferas y de ejemplares que no han alcanzado la
madurez sexual; situacin que para una especie de
baja fecundidad, como P. pugnax (Ibarra, 2010),
representa un impacto negativo para su conservacin.
Tambin es importante sealar, que la bomba
camaronera utilizada para su extraccin tiene escasa o
nula selectividad, lo que podra provocar alta
mortalidad de cras.
 Lat. Am. J. Aquat. Res. 382

Tabla 2. Parmetros de crecimiento individual de crustceos dulceacucolas.

Table 2. Parameter estimates of individual growth curve in freshwater crustaceans.

Autor(es) Especie L(mm) K(mm ao-1) Sexo

Noro & Buckup (2009) Parastacus defossus 30,98 0,0026 Ambos

Fries (1984) Parastacus brasiliensis 42,89 0,002 Ambos
Fontoura & Buckup (1989) Parastacus brasiliensis 57,37 0,23 Ambos
Anastcio & Marques (1995) Procamburus clarkii 56,00 0,68 Ambos
Fidalgo et al. (2001) Procamburus clarkii 62,00 0,23 Ambos
Chiesa et al. (2006) Procamburus clarkii 64,30 0,70 Hembras
63,30 0,66 Machos
Scalici & Gherardi (2007) Procamburus clarkii 65,50 0,69 Hembras
62,60 0,62 Machos
Scalici et al. (2009) Procamburus clarkii 74,60 0,32 Hembras
68,30 0,33 Machos
Beatty et al. (2005) Cherax quinquecarinatus 66,70(*) 0,27 Ambos

(*) Longitud asinttica del permetro del capazn

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Lat. Am. J. Aquat. Res., 39(2):Antifouling activity from sea anemone extracts Heteractis magnifica and H. aurora
385-389, 2011 385
DOI: 10.3856/vol39-issue2-fulltext-19

Short Communication

Antifouling activity by sea anemone (Heteractis magnifica and H. aurora)

extracts against marine biofilm bacteria

Subramanian Bragadeeswaran1, Sangappellai Thangaraj2, Kolandhasamy Prabhu2

& Solaman Raj Sophia Rani2
1
Centre of Advanced Study in Marine Biology, Annamalai University Parangipettai
608 502, Tamil Nadu, India
2
Ph.D., Research Scholars, Centre of Advanced Study in Marine Biology
Annamalai University Parangipettai - 608 502, Tamil Nadu, India

ABSTRACT. Sea anemones (Actiniaria) are solitary, ocean-dwelling members of the phylum Cnidaria and
the class Anthozoa. In this study, we screened antibacterial activity of two benthic sea anemones (Heteractis
magnifica and H. aurora) collected from the Mandapam coast of southeast India. Crude extracts of the sea
anemone were assayed against seven bacterial biofilms isolated from three different test panels. The crude ex-
tract of H. magnifica showed a maximum inhibition zone of 18 mm against Pseudomonas sp. and Escherichia
coli and a minimum inhibition zone of 3 mm against Pseudomonas aeruginosa, Micrococcus sp., and Bacillus
cerens for methanol, acetone, and DCM extracts, respectively. The butanol extract of H. aurora showed a
maximum inhibition zone of 23 mm against Vibrio parahaemolyticus, whereas the methanol extract revealed a
minimum inhibition zone of 1 mm against V. parahaemolyticus. The present study revealed that the H. aurora
extracts were more effective than those of H. magnifica and that the active compounds from the sea anemone
can be used as antifouling compounds.
Keywords: anemones, bioactive metabolites, novel antimicrobial, biofilm, natural antifouling, India.

Actividades antiincrustantes de las extractos de las anmonas marinas Heteractis

magnifica y H. aurora frente a biofilm de bacterias marinas
RESUMEN. Las anmonas de mar (Actiniaria) son solitarias, habitantes ocenicos del phylum Cnidaria y de
la clase Anthozoa. En este estudio se determina la actividad antibacteriana de dos anmonas bentnicas
Heteractis magnifica y H. aurora recolectadas en la costa de Mandapam, sudeste de India. Los extractos
crudos de estas anmonas fueron ensayados frente a siete biofilms bacterianos aislados de tres paneles de
control distintos. El extracto crudo de la anmona H. magnifica mostr una zona inhibicin mxima de 18 mm
contra Psudomonas sp. y Escherichia coli y la zona de inhibicin mnima de 3 mm fue encontrada frente a
Pseudomonas aeruginosa, Micrococus sp. y Bacillus cerens de extractos de metanol, acetona y DCM
respectivamente. El extracto de butanol de la anmona H. magnifica mostr una zona de inhibicin mxima de
23 mm frente a Vibrio parahemolyticus, mientras que con el estracto de metanol se observ una zona de
inhibicin mnima de 1 mm frente a V. parahemolyticus. El presente estudio mostr que los extractos H.
aurora son ms efectivos que los de H. magnifica y que los compuestos activos de las anmonas de mar
pueden ser usados como compuestos anti-incrustantes.
Palabras clave: anmonas, metabolitos bioactivos, novela antimicrobiana, biopelcula, antiincrustantes
naturales, India.

___________________
Corresponding author: S. Bragadeeswaran (drpragathi@gmail.com)

Marine biofouling is an extensive phenomenon (Chambers et al., 2006). Until recently, antifouling
causing large penalties to engineered structures such paints containing Tributyltin (TBT) and copper
as ships and offshore platforms by way of increased compounds were effectively used to combat fouling
use of manpower, fuel, material and dry-docking time (Evans, 2001). However, these compounds, especially
386 Lat. Am. J. Aquat. Res.
TBT, were reported to be highly toxic and persistent
in the marine environment, and were proved to have
adverse effects on non-target marine organisms
(Omae, 2003; Yebra et al., 2004). Under these
circumstances, search for natural antifouling
compounds as ecologically compatible substitutes for
chemical biocides is progressing worldwide (Sipkema
et al., 2005; Raveendran et al., 2008).
Natural products and their synthetic analogs
exhibiting anaesthetic, repellent and settlement
inhibition properties, but non-toxic to the non-target
organisms, are preferred as potential antifouling
agents (Omae, 2003). In this regard, sessile, soft-
bodied marine organisms maintaining a clean surface
were identified as possible sources of natural product
antifoulants (NPAs). This was attributed mostly to the
production of secondary metabolites, presumably as a
means of protection from predation, colonization by
epizoic organisms or to reduce competition for space
(Wahl et al., 1994).
Sea anemones are evolved with rich sources of
bioactive metabolites, which could be used for novel
antimicrobial drugs, many of which exhibit structural
features, not found in terrestrial natural products
(Ireland et al., 1988). Of the natural products isolated
from marine organisms, only less than 1% has been
examined so far for pharmacological activity (Rao et
al., 1985; Fusetani, 2000). Much of the studies are
warranted to find antimicrobial activity in the resistant
strains of microorganisms. Sea anemones (Actiniaria)
are solitary, ocean dwelling member of the phylum
Cnidaria and the class Anthozoa. Among the marine
organisms, Anthozoa are ecologically important
animals, which need to protect themselves against the
lethal or debilitating consequences of microbial or
parasitic invasion (Ramalingam & Ramarani, 2006).
The ability of anthozoans to display discriminatory
tissue reactions to foreign grafts has been
demonstrated by many workers (Jokiel & Bigger,
1994; Rinkevich et al., 1994; Perma et al., 2005). The
present study was aimed and find out the efficacy
antimicrobial activity of two benthic sea anemones
against primary film forming bacteria.
Specimen collection and identification
Two species of sea anemones, Heteractis magnifica
and H. aurora were collected from Mandapam
(0916N, 7212E), Southeast coast of India by
SCUBA diving at the depth ranging from 3 to 5 m
between February and March, 2009. The samples were
thoroughly washed with sea water and removed sand,
mud and overgrowing organisms at the site of
collection, and the sample was packaged with air in
thin cover to the laboratory and maintain in culture
tank. Collected specimens were identified by
following the standard literature of Indo-Pacific coral
reef field guide (Geraled & Steene, 1998).
Preparation of crude extract
The entire body of two different sea anemones,
Heteractis magnifica and H. aurora were washed with
cleaned sea water and later for extraction; 1 kg of each
sea anemones were cut into small pieces and
approximately 200 g of sea anemone pieces were
immersed with five different solvents in separately.
Methanol, Dichloromethane, Ethanol, Acetone and
Butanol by using these solvents animal was
homogenised, extracted with respective solvents and
filtered through Whatman N1. Filter paper (0.4 m);
it was then evaporated at low pressure using an R-200
Buchi Rotavapor at 30C. The resultants were stored
at 4C for further use. These crude extracts were used
for antibacterial activity against biofilm bacterial
strains were isolated from the different test panels.
Isolation of biofilm bacteria for antibacterial
activity
The fouling bacteria used in the antibacterial assay
were isolated from the biofilm formed over
aluminium, fiber glass and wood panels by pour plate
method (Wahl, 1995). The panels were deployed for
about a month during October to November 2009 at
1m-depth in the Vellar estuary boat jetty (1129N,
7946E), southeast coast of India. The panels were
washed with sterile seawater before swabbing with
sterile cotton swabs. The swabs were placed in a tube
containing sterile seawater, serially diluted and
inoculated in marine agar plates with Zobell marine
agar media. The plates were incubated at room
temperature for 24 h. The pure bacterial strains based
on colony morphology, colour and appearance were
isolated by repeated streaking and identified up to
genus level (Holt et al., 1994). The isolated bacterial
strains were stored in slant at 4C for antibacterial
assay.
Antibacterial activity
Antibacterial activity was carried out by using the
standard disc diffusion method (Murugan & Santhana-
Ramasamy, 2003). The following seven biofilm
bacterial pathogens, Pseudomonas aurogenosa,
Micrococus sp. Bacillus cerens, Pseudomonas sp.
Escherichia coli, Vibrio cholerae and V. parahe-
molyticus were used. The extracts were applied to 6
mm sterile discs in aliquots of 30 L of solvent
allowed to dry at room temperature, and placed on
agar plates seeded with microorganisms. The bacteria
were maintained on nutrient agar plates and incubated
 Antifouling activity from sea anemone extracts Heteractis magnifica and H. aurora 387

at 37C for 24 h. The zones of growth inhibition were
measured after 24 h incubation. All extracts were
tested thrice at a concentration of 30 L disc-1.
The crude extracts from the two species of sea
anemones, Heteractis magnifica and H. aurora was
screened the antibacterial activity against seven
biofilm forming bacteria. The growth inhibition zones
of H. magnifica extracts showed (Fig. 1). The
maximum inhibition zone (16.0 1.2 mm) was
observed against Psudomonas sp. and E. coli in the
butanol extract and the minimum inhibition zone (4.0
0.8 mm) was noticed against Pseudomonas
aeruginosa, Micrococus sp. and Bacillus cerens of
methanol, acetone and DCM extracts respectively.
Whereas the extract of H. aurora, the maximum
inhibition zone (22.6 0.4 mm) showed against V.
parahemolyticus of the butanol extract and the
minimum inhibition zone was showed (1 0.8 mm)
against Vibrio parahemolyticus of the methanolic
extract shown (Fig. 2). No inhibition zones were
noticed against B. cereus, Psudomonas sp., E. coli and
V. cholerae in both methanol and dichloromethane
extracts.

Figure 1. Antibacterial activity of Heteractis magnifica Quoy & Gaimard, 1833 against biofilm bacteria.
Figura 1. Actividad antibacteriana de Heteractis magnifica Quoy & Gaimard, 1833 frente a biofilm bacteriano.

Figure 2. Antibacterial activity of Heteractis aurora Quoy & Gaimard, 1833 against biofilm bacteria.
Figura 2. Actividad antibacteriana de Heteractis aurora Quoy & Gaimard, 1833 frente a biofilm bacteriano.
388 Lat. Am. J. Aquat. Res.
The present investigation, the H. magnifica was
showed the maximum inhibition zone (16.0 1.2 mm)
against Psudomonas sp. and E. coli in the butanol
extract and minimum inhibition zone (4.0 0.8 mm)
was noticed against P. aeruginosa, Micrococus sp.
and B. cerens of methanol, acetone and DCM extracts.
Whereas the Heteractis aurora, the maximum
inhibition zone (22.6 0.4 mm) showed against V.
parahemolyticus of the butanol extract and the
minimum inhibition zone was showed (1 0.8 mm)
against V. parahemolyticus of the methanolic extract.
A similar result was considered with previous authors
work.
The crude extract of diethyl ether showed good
activity against Gram positive and Gram negative
bacteria (Ravikumar et al., 2002). Of the human
pathogens tested, Klebsiella pneumonia is highly
inhibited (20 mm) by the tissue extract of sea anemone
by using chloroform and methanol extract and 24 mm
with the hexane tissue extract against fish pathogen
reported by Prakash-Williams et al. (2007). Bhosale et
al. (2002) have reported antimicrobial property of
marine organisms against biofilm bacteria isolated
from test panels. As an earlier report has been made,
the crude extract of Stichodactyla haddoni showed
good activity against Gram-negative bacteria
(Sureshkumar et al., 2002). Hutton & Smith, (1996)
has reported the amoebocytes from the sea anemone
Actinia equine showed considerable inhibitory activity
against Gram-negative bacteria within 3 h.
Patterson-Edward & Murugan (2000) have
reported broad-spectrum antibacterial activity of
aqueous ink extract of the cephalopods Loligo
duvauceli and Sepia pharaonis against nine human
pathogens. Murugan et al. (1991) have reported the
antibacterial activity of the hypobranchial gland of
Rapana rapiformis eight human against pathogens.
Such like my result considered with previous authors
results. In the present study have shown moderate
antibacterial activity against seven marine biofilm
bacterial strains. In future the active compounds of sea
anemones can be used as a natural antifouling
compounds.
Sea anemones collected along the southeast coast
of India. This preliminary assay indicated that sea
anemones are interesting source for antibacterial
metabolites and also that H. magnifica and H. aurora
are shows the strong antibacterial activity against
marine biofouling bacteria. In order to minimize the
economic loss, fuel consumption and metal corrosion
due to the formation of biofilms, there is an urgent
need for identifying suitable natural antifouling agents
to control the biofouling bacteria which is abundant in
the marine environments. The sea anemone extract is a
good source of antifouling compounds so further
studies are being continued to purify and identify the
active fraction.
ACKNOWLEDGEMENTS
The authors thankful to Prof. Dr. T. Balasubramanian,
Director, CAS in Marine Biology, Annamalai
University for providing facilities and Department of
Biotechnology (DBT), New Delhi for financial
assistance.
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DOI: 10.3856/vol39-issue2-fulltext-20

Short Communication

Reestablecimiento de Choromytilus chorus (Molina, 1782) (Bivalvia: Mytilidae)

en el norte de Chile

Miguel Avendao1 & Marcela Cantillnez1

1
Laboratorio de Cultivo y Manejo de Moluscos, Departamento de Acuicultura
Universidad de Antofagasta. P.O. Box 170, Antofagasta, Chile

RESUMEN. Hasta fines del siglo pasado no existan registros de la presencia de Choromytilus chorus al norte
de los 23S, pese a antecedentes que sealaban su existencia en pocas pasadas. Ciertos cambios relacionados
con las masas de agua costeras de esta zona, habran generado la ausencia o escasez que presentaba el entorno
costero actual. Sin embargo, hace una dcada atrs, su presencia en el norte de Chile, comienza a tener
connotacin pesquera. En el presente trabajo se confirma su reestablecimiento en las regiones de Antofagasta
y Tarapac, mediante prospecciones realizadas en seis lugares donde se registr su presencia, as como
mediante la captacin de semilla en colectores suspendidos. Se indica interaccin con Aulacomya ater, a la
cual ha desplazado a estratos ms profundos, mientras que su reestablecimiento, iniciado en las regiones de
Atacama y Antofagasta, y que se ampli posteriormente a la regin de Tarapac; permite postular la hiptesis
que la dinmica de estos bancos, respondera a una estructura de metapoblacin, dado el sistema de corrientes
y vientos que predominan en la zona norte, permitiendo la adveccin larval de poblaciones existentes en la
regin de Coquimbo.
Palabras clave: recolonizacin, Choromytilus chorus, norte de Chile, Pacfico suroriental.

Reestablishment of Choromytilus chorus (Molina, 1782) (Bivalvia: Mytilidae)

in northern Chile
ABSTRACT. Despite indications of its presence in past ages, until the end of the last century, no records
showed Choromytilus chorus north of 23S. Certain changes related to coastal water masses in the zone could
be responsible for the present lack or scarcity of this species in the coastal area. However, a decade ago, this
species appeared in northern Chile in the context of fisheries. This study confirms the re-establishment of C.
chorus in the Antofagasta and Tarapaca regions through surveys at six sites where the species had been
registered and spat collection using suspended collectors. This species has interacted with Aulacomya ater,
displacing it towards deeper habitats. The re-establishment of C. chorus began in the Atacama and
Antofagasta regions and later extended to the Tarapaca region. Thus, we hypothesize that the dynamics of
these shoals correspond to a metapopulation structure that has allowed larval advection, given the current
system and predominant winds in the northern zone, from populations existing in the Coquimbo region.
Keywords: recolonization, Choromytilus chorus, northern Chile, southeastern Pacific.

___________________
Corresponding author: Miguel Avendao (mavendano@uantof.cl)

En el norte de Chile, a partir de 1999 se comenz a
observar, la presencia de Choromytilus chorus (Moli-
na, 1782) en la pesca comercial, desembarcndose ese
ao una tonelada tanto en la zona de Atacama (ca.
2704S) como de Antofagasta (ca. 2337S)
(SERNAPESCA, 1999). Esta cifra se increment a 3
ton el ao siguiente en Atacama, sin embargo, a partir
del 2001, su pesquera se concentr tanto en la zona de
Tarapac (ca. 2014S) como de Antofagasta, con
cifras que han variado entre 2 y 86 ton anuales en la
primera, y entre 1 y 39 ton en la segunda zona
(SERNAPESCA, 2001-2008).
Para constatar y registrar la presencia de este re-
curso en el norte Grande de Chile, se realiz el 2009
un estudio prospectivo en las localidades de Pisagua,
Chanavaya y Chipana (Regin de Tarapac), y en
Caleta Punta Arenas, Michilla y Taltal (Regin de
Antofagasta) (Fig. 1), las cuales fueron seleccionadas
391 Reestablecimiento de choro zapato Choromytilus chorus
Figura 1. Localizacin geogrfica de las reas de
estudio, en las regiones de Antofagasta y Tarapac. 1)
Pisagua, 2) Chanavaya, 3) Chipana, 4) Caleta Punta
Arenas, 5) Michilla, 6) Caleta Errzuriz, 7) Taltal.
Figure 1. Geographic location of the study areas, in the
regions of Tarapaca and Antofagasta. 1) Pisagua, 2)
Chanavaya, 3) Chipana, 4) Caleta Punta Arenas, 5)
Michilla, 6) Caleta Errzuriz, 7) Taltal.
por su accesibilidad y por contar con embarcaciones
para realizar los muestreos. En cada una de ellas se
definieron tres transectas de buceo separadas entre s
cada 100 m, en las cuales se realiz un recorrido
submarino asistido por un ordenador de buceo
Beuchat CX 2000, y un comps de buceo Cressy, de 4
a 20 m de profundidad. Tanto en caleta Punta Arenas,
como Michilla, la prospeccin fue acompaada de
muestreo extractivo y en cada transecta se extranjeron
a los 13, 10, 7 y 4 m de profundidad, todos los
ejemplares presentes en una superficie de 0,25 m2,
utilizando una cuadrata de 0,5 x 0,5 m. Los resultados
obtenidos, mostraron que en los seis sitios
prospectados existieron poblaciones de Ch. chorus,
distribudas entre 4 y 13 m de profundidad, sobre
sustrato rocoso (Fig. 2a), semienterrados en fondos
mixtos de arena y roca (Fig. 2b), y ocasionalmente
sobre fondo de arena fina, como se constat en una de
las transectas realizadas en caleta Punta Arenas (Fig.
2c), coincidiendo con lo que se seala para
poblaciones de la zona austral de Chile, donde
Figura 2. Poblaciones de Ch. chorus integradas por
individuos adultos, juveniles y semilla, distribuidas sobre
a) sustrato rocoso entre 4 y 13 m de profundidad, b)
mixto de arena y roca, y c) ocasionalmente sobre fondo
de arena.
Figure 2. Population of C. chorus composed of adult,
young and seed on a) rocky substrate distributed between
4 and 13 m depth, b) mixed sand and rock, and c) occa-
sionally on sandy substrate.
se les indica adheridos a sustratos duros y en bancos
de arena (Gajardo et al., 2007). La estructura
poblacional observada en los seis sitios, mostr
presencia de individuos adultos, juveniles y pre-
reclutas (semilla). En caleta Punta Arenas, las tallas
fluctuaron entre 8,7 y 143,6 mm, con una media de
66,88 42,55 mm, mientras que en Michilla variaron
entre 23,42 y 124,15 mm, con una talla media de
71,47 15,37 mm.
En forma paralela a la prospeccin realizada, y
considerando antecedentes de la ocurrencia de
fijaciones de mitlidos en lneas de cultivo del
pectnido Argopecten purpuratus (Lamarck), en un
centro que operaba en caleta Errzuriz (Antofagasta),
en noviembre de 2009 se procedi a instalar colectores
de redes desde lneas suspendidas tanto en ese lugar
como en caleta Punta Arenas. Los resultados
obtenidos en estos colectores, mostraron fijaciones
importantes de semilla de Ch. chorus en ambos sitios
(Fig. 3). La aplicacin del programa MIX 3.1.a
(Macdonald & Pitcher, 1979), a la talla de la semilla
fijada despus de 80 das de mantener los colectores
en el agua, permiti discriminar en caleta Punta
Arenas cinco cohortes asentadas, cuyas tallas medias
alcanzaron 5,29 0,77 mm para la cohorte C1; 3,90
0,39 mm para la C2; 2,74 0,36 mm para la C3; 1,63
0,32 mm para la C4, y 0,66 0,16 mm para la C5, que
representaron el 13,6; 28,4; 21,0; 11,9 y 25,1% de la
semilla fijada respectivamente, mientras que en
 Lat. Am. J. Aquat. Res.
Figura 3. Colectores con fijacin de semilla de Ch.
chorus en caleta Errzuriz, Antofagasta.
Figure 3. Ch. chorus spat settled on artificial collectors
used in caleta Errzuriz, Antofagasta.
caleta Errzuriz, solo se discriminaron dos cohortes,
cuyas tallas medias alcanzaron a 0,89 0,16 mm para
la C1, y 0,45 0,08 mm para la C2, en proporciones de
13 y 87% respectivamente. Los histogramas de
frecuencia de talla para este anlisis fueron
descompuestos segn una distribucin normal
(Avendao et al., 2006, 2007, 2008).
Mediante las prospecciones, se observ en los
sustratos rocosos, que la colonizacin de Ch. chorus
en el estrato (4-13 m de profundidad), estara
generando un desplazamiento de una parte importante
de la poblacin de Aulacomya ater (Molina), que
habitualmente se distribuye a partir de los 4 m de
profundidad (Gajardo et al., 2007). Los resultados
muestran que este recurso, actualmente se estara
distribuyendo a profundidades mayores de 15 m,
generndose entre 13 y 15 m, una zona de
coexistencia de ambas especies (Fig. 4a), con
presencia espordica de Ch. chorus en el veril ms
profundo de este estrato (Fig. 4b). A pesar que datos
histricos para el sector estudiado en caleta Punta
Arenas, indicaba la presencia de A. ater a partir de 8-
13 m de profundidad (Avendao et al., 1998).
Observaciones similares de desplazamiento de una
especie nativa, a estratos ms profundos, por la
aparicin de una especie invasora, han sido sealadas
por Bownes & McQuaid (2006), respecto a la
distribucin vertical de Perna perna (Linnaeus),
especie nativa de la costa sur de Sudfrica, desplazada
a zonas ms profundas por Mytilus galloprovincialis
(Lamarck), especie que en las ltimas dos dcadas se
ha convertido en un invasor, ampliando su
distribucin actual a zonas templadas de los
392
hemisferios norte y sur en gran parte del mundo (Lee
& Morton, 1985; McDonald et al., 1991; Anderson et
al., 2002; Ruiz et al., 2008). Bownes & McQuaid
(2006) indican adems, que en esta distribucin, se ha
establecido un rea de superposicin y coexistencia de
ambas especies en la zona media, que permite su
convivencia a travs de la segregacin de hbitat
parcial, similar a lo observado en el presente estudio
para Ch. chorus y A. ater. Estos mismos autores
indican tambin, la sustitucin total de A. ater, como
especie nativa de la costa oeste de Sudfrica, por la
invasora M. galloprovincialis.
El desplazamiento de A. ater por parte de Ch.
chorus, observado en los sitios prospectados, se podra
atribuir a una competencia interespecfica ms efectiva
de este ltimo, considerando que se le ha observado
no solo fijndose sobre sustratos filamentosos, sino
tambin en los bisos de ejemplares adultos de su
misma especie como de otros mitlidos (Moreno,
1995). La efectividad que muestra Ch. chorus en esta
competencia, puede verse favorecida por las mayores
tasas de crecimiento que presenta respecto de A. ater.
Se han sealado crecimientos diferenciados entre Ch.
meridionales y A. ater, para poblaciones de Sudfrica,
donde se constata el bajo crecimiento que experimenta
A. ater (Barkai & Branch, 1989).
Por otro lado, debe sealarse que hasta fines del
siglo pasado, no haba registros de esta especie al
norte de los 2914`S (Regin de Coquimbo) (Bellolio
et al., 1996), a pesar que numerosos antecedentes
demostraban que fue abundante en el norte de Chile
(Ramorino, 1974), y era importante en la dieta de las
comunidades costeras pre-hispnicas (Gorriti, 1998).
Su disminucin o desaparicin del extremo norte de su
rea de distribucin pareciera estar relacionada con
cambios en las masas de aguas costeras (Llagostera,
1979; Daz & Ortlieb, 1992; Ortlieb & Guzmn, 1994;
Ortlieb et al., 1994; Guzmn et al., 1998). Un evento
El Nio ha sido sealado por algunos autores (Daz &
Ortlieb, 1992), como la posible causa de su
desaparicin, dada su condicin de especie de aguas
fras. Por ello, su reaparicin en esta zona, podra
atribuirse al cambio climtico que afecta actualmente
la regin, el cual habra brindando condiciones
necesarias para su reestablecimiento. Los cambios
climticos, se han sucedido en el tiempo aproxima-
damente cada 120 mil aos, desarrollndose con
mayor o menor extensin temporal a lo menos cinco
veces en los ltimos 500 mil aos (Jansen et al.,
2007). Una de las manifestaciones de estos cambios,
se asocia a la temperatura, la cual ha mostrado
variaciones muy amplias a escala geolgica, con
perodos glaciares e interglaciares, que han variado de
21C hace 10 millones de aos, a 7C hace 10.000
393 Reestablecimiento de choro zapato Choromytilus chorus
Figura 4. Zona de coexistencia de Ch. chorus () y A. ater. a) Entre 13 y 15 m de profundidad, b) con presencia
espordica de Ch. chorus () a 15 m.
Figure 4. Area coexistence of Ch. chorus () and A. ater. a) Between 13 and 15 m depth, b) with occasional presence of
Ch. Chorus () at 15 m.
aos; en los ltimos 1.000 aos su variacin ha sido
entre 14 y 16C, con pronsticos muy variados
(Yez, 2010). Debe indicarse, que a partir del siglo
XX las variaciones de la temperatura media global en
la superficie terrestre y ocenica, muestran entre 1880
y 1935 un perodo de enfriamiento importante,
seguido de un perodo fro menos intenso entre 1945 y
1975 (Trenberth et al., 2007). Actualmente, la
informacin satelital de temperatura superficial del
mar del perodo 1978-2004, muestra un claro
enfriamiento frente a Chile, en contraposicin al
calentamiento generalizado de los ocanos
(Fuenzalida et al., 2007; Yez, 2010). Estas
condiciones de bajas temperaturas, que en el norte
comenzaron a manifestarse marcadamente con
posterioridad al evento de El Nio 1997-1998
(Cantillnez et al., 2005; Avendao et al., 2008), son
consecuentes con observaciones de fijaciones de
semilla de Ch. chorus, ocurridas sobre colectores de
ostiones instalados en la reserva marina de La
Rinconada (Avendao, com. pers.), y por tanto este
factor sera uno de los responsables de su
reestablecimiento.
Asociado al cambio de las condiciones am-
bientales, propicias para el asentamiento y crecimiento
de Ch. chorus en esta zona, su reaparicin podra
atribuirse a un transporte larval desde las poblaciones
existentes en la regin de Coquimbo (Bellolio, 1996),
favorecido por el agua Sub-Antrtica (ASAA) que
fluye hacia el norte. Su reestablecimiento, iniciado en
las regiones de Atacama y Antofagasta, amplindose
posteriormente a la regin de Tarapac, y en los
ltimos aos reapareciendo en Ilo-Per (ca. 1740S;
IMARPE, 2006), permite postular la hiptesis de que
la dinmica de estos bancos, estara respondiendo a
una estructura de metapoblacin, en el concepto
moderno (Hanski & Simberloff, 1997), que considera
a poblaciones espacialmente estructuradas dentro de
un ensamblaje de subpoblaciones reproductivamente
activas, que tienen algn efecto sobre las dems
poblaciones locales, incluyendo, la posibilidad de su
restablecimiento despus de la extincin. Es as como,
para larvas de Mytilus chilensis (Hupe) en el sur de
Chile, se ha sealado su capacidad de dispersin a
grandes distancias, a lo largo de la costa chilena,
permitiendo que el proceso de transporte y
asentamiento, ocurra dentro de un rango de
distribucin de metapoblacin (Toro et al., 2006).
Debe indicarse que oceanogrficamente, la zona
norte de Chile, corresponde a un ambiente de
transicin subtropical. Su orientacin geogrfica hacia
el sur y suroeste y su posicin latitudinal la exponen a
la confluencia de varios tipos de masas de agua. Entre
ellas, la predominante durante un ao normal,
corresponde a la masa de agua (ASAA), la cual
domina los 200 m superiores de la rama costera de la
corriente fra de Humboldt que se desplaza hacia el
norte. En la zona, el ASAA se mezcla con una menor
proporcin de aguas subtropicales, de mayor salinidad
y temperatura y tambin peridicamente con aguas
ms fras que provienen de mayor profundidad,
correspondientes a aguas ecuatoriales sub-
superficiales, las cuales ascienden hacia la costa
debido a procesos de surgencia inducida por los
vientos del sur y suroeste (Escribano et al., 2002;
Avendao & Cantillnez, 2008). La predominancia de
vientos suroeste en la costa norte de Chile, dominando
durante todo el ao (Bakun & Nelson, 1991; Pizarro et
al., 1994), ha sido considerada la principal fuerza
causante de la circulacin de aguas someras (0-20 m)
 Lat. Am. J. Aquat. Res.
en el ocano costero, lo cual favorece la adveccin de
larvas desde el sur, como ha sido sealado para
Concholepas concholepas (Bruguire) (Gonzlez et
al., 2005).
El transporte y posterior asentamiento larval de Ch.
chorus, queda demostrado en las fijaciones ocurridas
sobre los colectores en caleta Errzuriz (zona
desprovista de poblaciones locales), mientras que las
diferencias encontradas en las tallas medias, y en el
nmero de cohortes fijadas en ese lugar, respecto a las
registradas a un mismo tiempo en caleta Punta Arenas,
demostrara la existencia de diferentes grupos larvales
presentes a lo largo de esta costa. Ello fortalece la
hiptesis planteada anteriormente, al mostrar que la
disponibilidad larvaria en un sitio particular,
depender de las interconexiones que existan entre los
diferentes bancos que conforman las metapoblaciones,
ligados entre s por grados variables de dispersin
larval, abiertos al reclutamiento originado en otras
regiones (Narvarte, 2001). Distribuciones importantes
de larvas del pectnido Pecten maximus (Linnaeus), en
tamao y densidad en reas desprovistas de
progenitores, han sido explicadas para el Canal de la
Mancha, por un transporte horizontal que generan las
mareas y vientos, desde otros sitios de desove
(Boucher & Dao, 1990). Adems, diversos autores
(Caley et al., 1996; Warner, 1997; Neubert & Caswell,
2000; Strathmann et al., 2002; Palumbi, 2004; Harley
et al., 2006; Becker et al., 2007), consideran que el
conocimiento cuantitativo de conectividades larvales
ha revolucionado la comprensin de una amplia gama
de asuntos, incluyendo la dinmica de poblaciones
marinas, los procesos de extincin local y de nuevas
colonizaciones, las escalas de adaptacin, el diseo de
reservas marinas, la propagacin de especie invasoras
y la respuesta de las especies al cambio climtico.
Se debe sealar finalmente, que si bien la
reaparicin de Ch. chorus, en la costa del norte de
Chile, se puede entender como un efecto positivo del
cambio global que se est produciendo, su
sometimiento a un rgimen de pesquera, bajo
normativas que rigen para este recurso, basadas en
antecedentes obtenidos en poblaciones de la zona
austral (Decreto Supremo N136/86), sin conocer su
ciclo ontognico en el actual sistema ecolgico en que
se encuentra en el norte de nuestro pas, pone en serio
riesgo su permanencia, considerando que su
distribucin vertical (4 a 13 m), favorece su extraccin
por parte de buzos mariscadores. Debe indicarse que
la alta presin extractiva a la cual estuvieron
sometidos los bancos naturales de este recurso en la
zona sur, desde al menos 1938 hasta 1960, produjo su
casi extincin, situacin que gener la necesidad de
desarrollar su cultivo, con el fin de repoblar y vigilar
394
sus bancos naturales; sin embargo, a la fecha, su
cultivo an no se ha desarrollado. Tampoco se tiene
antecedentes claros, del efecto que su interaccin est
provocando sobre otros recursos nativos actuales de
esta zona de Chile, considerando lo observado con A.
ater, cuyo desembarque adems, ha descendido hasta
un 57,7% en la regin de Tarapac, y hasta un 6,4%
en la de Antofagasta, luego de la aparicin de Ch.
chorus (SERNAPESCA, 1999-2008). Todo esto
amerita emprender estudios de mayor profundidad,
para comprender el funcionamiento de estas
poblaciones que permitan establecer estrategias
adecuadas de explotacin sustentable con estos
recursos en la zona norte de Chile.
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