Journal of Fish Biology (2015) 86, 14441453

doi:10.1111/jfb.12650, available online at wileyonlinelibrary.com

Spatio-temporal isotopic signatures (13 C and 15 N) reveal

that two sympatric West African mullet species do not feed
on the same basal production sources
F. Le Loch*, J. -D. Durand, K. Diop and J. Panfili
*UMR 212 EME, IRD-IFREMER-UMII, Centre de Recherche Halieutique Mditerranenne et
Tropicale, Avenue Jean Monnet, 34203 Ste, France, UMR 6539 LEMAR,
CNRS-UBO-IRD-IFREMER, Rue Dumont dUrville, Pointe du Diable, Technopole Brest
Iroise, 29280 Plouzan, France, UMR 5119 ECOSYM, UM2-CNRS-IRD-IFREMER-UM1,
Universit Montpellier 2, cc093, Place E. Bataillon, 34095 Montpellier Cedex 05, France
and IRD, UMR 5119 ECOSYM, LABEP-AO, B. P. 1386, 18524 Dakar, Senegal
(Received 5 September 2014, Accepted 28 January 2015)
Potential trophic competition between two sympatric mullet species, Mugil cephalus and Mugil
curema, was explored in the hypersaline estuary of the Saloum Delta (Senegal) using 13 C and 15 N
composition of muscle tissues. Between species, 15 N compositions were similar, suggesting a similar
trophic level, while the difference in 13 C compositions indicated that these species did not feed from
exactly the same basal production sources or at least not in the same proportions. This result provides
the first evidence of isotopic niche segregation between two limno-benthophageous species belonging
to the geographically widespread, and often locally abundant, Mugilidae family.
2015 The Fisheries Society of the British Isles

Key words: carbon isotopes; fish diet; Mugilidae; nitrogen isotopes; trophic level.

Mugilidae is a successful fish family present in all tropical, sub-tropical and temperate
littoral aquatic ecosystems worldwide. Their biomass often dominates fish communities in intertidal areas (Gonzalez-Murcia et al., 2012), salt marshes (Lefeuvre et al.,
1999; Laffaille et al., 2002; Green et al., 2009), mangroves (Thollot et al., 1999;
Sukardjo, 2004), estuaries and lagoons (Cardona, 2006; Okyere et al., 2011). The
stomach content analyses conducted indicate that adult mugilids are omnivorous
benthic microphages, and they feed mainly on detritus [including particular organic
matter; Odum (1970); Brusle (1981)], microalgae and especially diatoms (Laffaille
et al., 2002; Almeida, 2003) and occasionally on benthic invertebrates of the meiofauna
(Lasserre, 1976; Laffaille et al., 1998) and macrofauna (Riera et al., 1999; Bouchard
& Lefeuvre, 2000; Quan et al., 2007). All stomach content analyses performed for
Mugilidae species have stressed the large overlaps in their diet (Blaber, 1976, 1977;
Ibanez-Aguirre, 1993; Cardona, 2001). Trophic competition among sympatric mullet
Author to whom correspondence should be addressed. Tel.: +33 298498701; email: francois.le.loch@ird.fr

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species was assumed to be low, however, due to (1) differences in the particle size
preferences between these species (Blaber, 1976) or (2) unlimited food availability
(Cardona, 2001). Their abundance and trophic position make them key species in the
functioning of littoral ecosystems, allowing for both the exportation of organic matter
via migration from the most productive littoral ecosystems (e.g. salt marshes and
mangroves) to the less productive ones (Lefeuvre et al., 1999; Bouillon et al., 2008),
and the exploitation of primary production by higher trophic levels through predation
(Bouillon et al., 2008). In addition to their seasonal spawning migration from estuarine
ecosystems to the sea, Mugilidae can also make tidal migrations from the shoreline
(where they feed) to farther offshore. This transfer of biomass might appear weak in
comparison to the passive transfers that occur with the tides, but the transfer of organic
matter through the trophic web is much more direct. In this context, the exportation
of organic matter by mugilids is potentially significant for the functioning of coastal
ecosystems but still little is known. This is particularly true for tropical ecosystems
where the detritivorous mugilid species are diverse and sufficiently abundant to support
substantial fisheries (Harrison & Senou, 1999; Whitfield et al., 2012).
For the most part, Mugilidae trophic ecology has been studied by analysing stomach
contents. These analyses have provided substantial data on their trophic ecology,
but are only capable of revealing what food sources have been recently ingested. In
contrast, stable-isotope analyses (carbon and nitrogen) of tissues allow determination
of what matter has been assimilated over time (Pinnegar & Polunin, 1999). Carbon
stable-isotope ratios ( 13 C) reflect the isotopic signature of the diverse organic matter
sources on which the food web relies, and nitrogen stable-isotope ratios ( 15 N) allow
the estimation of the consumers trophic level (Fry & Scherr, 1984; Peterson & Fry,
1987). These analyses are able to quantify assimilated food over periods from days to
weeks (Hesslein et al., 1993; German & Miles, 2010). Thus, stable-isotope analysis
of tissues is a powerful tool in trophic ecology that can reveal resource partitioning
among detritivorous species more efficiently than stomach content analyses (Lujan
et al., 2011). This distinction between ingested and assimilated food is especially
important for mugilids, as they are opportunistic limno-benthophageous organisms
that ingest a high diversity of food sources that have different degrees of digestibility.
Thus, the discrimination and identification of detritic food sources is complex and the
nutritional quality of ingested detritus is not easily estimated from stomach contents
(Lujan et al., 2011). Despite the overlaps in Mugilidae diet that have been highlighted
in previous stomach content studies (Luther, 1962; Blaber, 1977; Ibanez-Aguirre,
1993; Cardona, 2001), a recent stable-isotope study suggested differences in isotopic
ratios between Mugilidae species (Faye et al., 2011). As such, the analysis of carbon
and nitrogen isotopes constitutes a relevant alternative for mugilid species to better
evaluate the trophic differences that could contribute to speciation and to the sympatry
of similar species living in the same habitats.
In this study, the aim was to determine if two sympatric Mugilidae species found
in the Saloum Delta, Senegal, Mugil cephalus L. 1758 and Mugil curema Valenciennes 1836, have the same diet using stable-isotope analysis of their muscle tissues.
Although this West African estuarine ecosystem experiences extreme saline conditions
(Simier et al., 2004), mugilids are particularly abundant and often dominate fish landings in the area (Bousso, 1996). Monthly samples of both species were collected from
fish landings at three different locations (Fig. 1) between February 2006 and February
2007 (Table I). The locations were selected according to the salinity gradient of the

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1446

F. L E L O C H E T A L.

Fatick

14 15

Sibassor
Kaolack
Foundiougne

Sa

lo
um

Ndangane

14 00

Djifre

Dio

Sokone

oss
mb

10 km

13 45
Senegal

Atlantic
Ocean

iala

nd
Ba
16 45

Missirah

16 30

16 15

16 00

Fig. 1. Three sampling locations for Mugilidae, indicated in bold, in the Saloum Delta (Senegal).

Saloum, with Sibassor being hypersaline (salinity up to 100, depending on the season),
Missirah having relatively low salinity (between 30 and 42) and Foundiougne having
intermediate salinity (between 38 and 55).
Each monthly sample consisted of between three and five fish per species per location. Species were determined using the identification key from Albaret (1992).
Collectively, their fork lengths (LF ) measured between 202 and 243 mm for
M. cephalus and between 201 and 245 mm for M. curema. Due to the absence
of landings in some months, samples were not always collected at Missirah and
Sibassor. To conduct the stable-isotope analyses, samples were removed from the
dorsal musculature of freshly-dead fishes. After dissection, muscle samples were
individually frozen and stored at 20 C before being freeze dried. Once dried, each
sample was then ground to obtain a fine powder. Approximately 1 mg of this powder
was weighed into tin capsules for the stable carbon and nitrogen isotopic analyses.
The 13 C:12 C and 15 N:14 N ratios were determined by continuous-flow isotope-ratio
mass spectrometry using a Europa Scientific ANCA-NT 20-20 stable-isotope analyser
(www.sercongroup.com) together with an ANCA-NT Solid/Liquid Preparation Module (Sercon). As the samples contained >10% nitrogen, the mass spectrometer was
operated in dual isotope mode, allowing 15 N and 13 C to be measured in the same
sample. The stable-isotopic signatures were expressed in conventional notation

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I S O T O P I C S I G N AT U R E S O F T W O S Y M PAT R I C M U G I L I D A E

Table I. Number of Mugil cephalus and Mugil curema analysed for stable-isotopic composition from February 2006 to February 2007, in the locations of Missirah, Foundiougne and
Sibassor
Mugil cephalus

February 2006
March 2006
April 2006
May 2006
June 2006
July 2006
August 2006
September 2006
October 2006
November 2006
December 2006
January 2007
February 2007

Mugil curema

Missirah

Foundiougne

Sibassor

Missirah

Foundiougne

Sibassor

4
5
4
5
5

5
5
5
5
3
5
4

4
5
5
5

5
4
5
4

4
3
4
4
5

5
5
4

5
4
4

4
4

5
5

4
5
5
4
5

as parts per mille () according to the following equation: X = (Rsample Rstandard-1 1)

103 , where X is 13 C or 15 N and R is the ratio 13 C:12 C or 15 N:14 N. Analytical precision (s.d., n = 5) was 02 for both nitrogen and carbon, as estimated from standards
analysed together with the samples.
ShapiroWilk tests were performed on LF and on stable-isotope ratios to test for
normality and KruskallWallis tests were carried out to check the variance in homogeneity. A three-way mixed analysis of variance (ANOVA) model was then used to
evaluate the differences in 13 C and 15 N between the sites (Missirah, Foundiougne and
Sibassor), sampling months and species (M. cephalus v. M. curema). Post hoc pair-wise
multiple comparison Tukey tests were performed to determine whether means were
significantly different.
The individual LF of both species were similar (mean 220 mm, KruskallWallis
tests), with the exception of M. curema in December from Sibassor (slightly larger).
This allowed completion of a comparison of stable-isotope ratios without an effect
of LF on the analysis. 13 C values ranged from 184 22 (Missirah, May) to
118 16 (Foundiougne, June), and from 188 02 (Missirah, January) to
137 04 (Foundiougne, February), for M. cephalus and M. curema, respectively. 15 N values ranged from 62 04 (Foundiougne, February) to 94 08
(Missirah, October), and from 58 04 (Foundiougne, December) to 96 05
(Missirah, May), for M. cephalus and M. curema, respectively. Stable-isotope ratios
did not completely overlap between the two species at each location. The main
difference was that 13 C values were generally lower for M. cephalus by 2 (Fig. 2),
revealing that the two species rely on different food sources. The general patterns
of both ratios were similar at the saline and hypersaline locations of Foundiougne
[Fig. 2(b)] and Sibassor [Fig. 2(c)], while the Missirah location showed lower 13 C
values for both species [Fig. 2(a)]. Significant differences were observed for both
13 C and 15 N, individually considering the location (ANOVA, P < 0001), date

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F. L E L O C H E T A L.

11

(a)

10
9
8
7
6
5
4
11

(b)

10

15N ()

9
8
7
6
5
4
11

(c)

10
9
8
7
6
5
4
22

20

18

16

13C

14

12

10

()

Fig. 2. Distribution of carbon ( 13 C) and nitrogen ( 15 N) stable-isotope ratios (mean s.d.) for the two Mugilidae species ( , Mugil cephalus; , Mugil curema) and three locations: (a) Missirah, (b) Foundiougne and (c)
Sibassor. Each symbol corresponds to mean s.d. isotopic compositions of fishes collected at one sampling
period (see Table I).

(ANOVA, P < 0001) and species (ANOVA, P < 0001 for 13 C), with the notable
exception of 15 N between the species (ANOVA, P > 005). Post hoc tests confirmed
that same levels of 15 N and 13 C were present at Foundiougne and Sibassor, but
different at Missirah (Table II). Depending on their habitat, mugilids change their
feeding habits [e.g. sediment grazing or water filtering, Brusle (1981); Almeida et al.
(1993); Cardona (2001)] in order to exploit the best food resources available (Odum,
1968; Almeida et al., 1993). The Saloum Delta is an unusual example of an estuarine

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Table II. Post hoc (Tukey) comparisons of mean nitrogen ( 15 N) and carbon ( 13 C) isotope
ratios between the three study locations and for Mugil cephalus and Mugil curema
Locations/species
15 N ()
Missirah v. Foundiougne
Missirah v. Sibassor
Sibassor v. Foundiougne
M. cephalus v. M. curema
13 C ()
Missirah v. Foundiougne
Sibassor v. Missirah
Sibassor v. Foundiougne
M. cephalus v. M. curema

Difference

Standardized difference

Critical value

1272
0891
0381
0021

6027
3928
2216
0145

2362
2362
2362
1973

<0001
<0001
>005
>005

2337
2015
0322
1705

9961
8074
1699
10590

2362
2362
2362
1973

<0001
<0001
>005
<0001

ecosystem. Since the late 1960s, the salinity gradient has been permanently inverted
due to an increasing rainfall shortage in the Sahelian region (Pags & Citeau, 1990;
Tabutin & Schoumaker, 2004). At the end of the dry season, salinity in the upstream
region of the delta can reach >130 (Simier et al., 2004). Along Saloums salinity
gradient, the two mugilid species feed slightly differently and consequently, it is likely
that they do not target exactly the same sources of carbon. Mugil cephalus and M.
curema both fed on microphytobenthos, which had mean 13 C values between 159
and 173 and 15 N around 3, the 13 C values of the other sources varying from
285 16 to 253 01 for mangrove leaf, from 253 01 to 240 21
for particulate organic matter and c. 248 01 for sediment organic matter in the
Saloum Delta (Gning et al., 2010; Faye et al., 2011). The differences in the carbon
assimilation of the two species may be due to the specific organisms selected from the
microbenthos that make up their diet, as suggested by Sanchez Rueda et al. (1997)
who observed sediment granulometric differences in the stomach of M. cephalus
and M. curema. The isotopic differences between the estuarine locations and saline
or hypersaline locations may be a result of the lower diversity of primary producers
observed in the upper Saloum, as suggested by Gning et al. (2010). Furthermore,
hypersaline conditions may be stressful for estuarine species such as M. cephalus and
M. curema, thus leading to lower biomass than in the Missirah location (Simier et
al., 2004). In the two more saline locations, carrying capacity may not be reached,
allowing trophic niche overlap to occur (Cardona, 2001). A complementary explanation of the isotopic difference could be the different residence times of the species in
the estuary. As Mugilidae are migratory species, the time that these individuals spent
in the estuary may not have been sufficient to acquire the isotopic signature of the
estuary. The fact that the monthly sampling gave the same results, however, weakens
this hypothesis and also leads to the idea that these species do not undergo significant
migration in the Saloum Delta, as shown by stable-isotope differences in Missirah.
The temporal evolution of the isotope ratios at Foundiougne confirmed the similarity
of nitrogen levels for the two species during the whole year and a significant difference
between the levels of carbon, with M. curema having lower values (Fig. 3). Although
the month of sampling had a significant effect on both isotopes (ANOVA, P < 0001),
a seasonal cycle has not been clearly identified. Nitrogen levels were higher during

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F. L E L O C H E T A L.

10

(a)

15N ()

5
10

(b)

11

13C ()

12
13
14
15
16
17
December

November

October

September

Month

August

July

June

May

April

March

February

January

18

Fig. 3. Temporal trends of the mean + s.d. (a) nitrogen ( 15 N) and (b) carbon ( 13 C) stable-isotope ratios at
Foundiougne for the two Mugilidae species ( , Mugil cephalus; , Mugil curema).

the dry season (February to May), whereas the highest carbon levels occurred in the
wet season (June to October) for both species and also during February to March for
M. curema (Fig. 3).
The dietary difference between the two species may be due to both different sources
of carbon within the microphytobenthos or organic detritic matter and the timing of
carbon assimilation. Although stable-isotope analysis is considered the more powerful
tool to efficiently reveal dietary partitioning among detritivores, it was not possible to
precisely define the different carbon resources ingested by the two species in this study.
Further analysis could be performed to screen, based on size, the isotopic composition
of the different components of the organic detritic matter.
The difference in the 13 C signature between the two species was relatively constant,
both spatially and temporarily, which implies specific feeding behaviour, such as food

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partitioning (Blaber, 1976). Particle size selection could occur via differences in the
jaw teeth and the pharyngobranchial organ (PBO), for which the morphology varies
greatly between mullet species (Harrison & Howes, 1991). PBO of M. cephalus also
shows an intraspecific variability greater than the interspecific variability within the
Mugil genus, consistent with the presence in this nominal species of cryptic species
(Harrison & Howes, 1991; Shen et al., 2011; Durand et al., 2012). So, it is very difficult to know if the PBO of the West African M. cephalus is different from the PBO
of M. curema. Despite the abundance of detritus and microphytobenthos in coastal
ecosystems, trophic partitioning may be a powerful evolutionary mechanism responsible for the high diversification of the Mugilidae family. This concurs with an increasing
number of theoretical (Hall, 2004) and empirical (Blaber, 1977) studies suggesting that
even for low trophic level species, there is a partitioning of the food resources based
on nutritional quality or particle size.
The study was funded by the IRD RAP research unit (20052008). We would like to thank
P. Lopez (IRD Ste) for drawing the map, C. Scrimgeour for running the stable isotope analyses
and J. Alpine for the English editing. We would also like to thank the two anonymous referees
for their remarks and suggestions that improved the manuscript.

References
Albaret, J. J. (1992). Mugilidae. In The Fresh and Brackish Water Fishes of West Africa, Vol. 2
(Lvque, C., Paugy, D. & Teugels, G. G., eds), pp. 780788. Collection Faune Tropicale
27.
Almeida, P. R. (2003). Feeding ecology of Liza ramada (Risso, 1810) (Pisces, Mugilidae) in a
south-western estuary of Portugal. Estuarine, Coastal and Shelf Science 57, 313323.
Almeida, P. R., Moreira, F., Costa, J. L., Assis, C. A. & Costa, M. J. (1993). The feeding strategies of Liza ramada (Risso, 1826) in fresh and brackish water in the river Tagus, Portugal.
Journal of Fish Biology 42, 95107.
Blaber, S. J. M. (1976). The food and feeding ecology of Mugilidae in the St. Lucia Lake system.
Biological Journal of the Linnean Society 8, 267277.
Blaber, S. J. M. (1977). The feeding ecology and relative abundance of mullet (Mugilidae) in
Natal and Pondoland estuaries. Biological Journal of the Linnean Society 9, 259275.
Bouchard, V. & Lefeuvre, J.-C. (2000). Primary production and macro-detritus dynamics in a
European salt marsh: carbon and nitrogen budgets. Aquatic Botany 67, 2342.
Bouillon, S., Connolly, R. M. & Lee, S. Y. (2008). Organic matter exchange and cycling in mangrove ecosystems: recent insights from stable isotope studies. Journal of Sea Research
59, 4458.
Bousso, T. (1996). La pche artisanale dans lestuaire du Sine-Saloum (Sngal). Approches
typologiques des systmes dexploitation. PhD Thesis, Universit de Montpellier II,
Montpellier, France.
Brusle, J. (1981). Sexuality and biology of reproduction in grey mullets. In Aquaculture of Grey
Mullets (Oren, O. H., ed), pp. 99154. Cambridge: Press Syndicate of the University of
Cambridge.
Cardona, L. (2001). Non-competitive coexistence between Mediterranean grey mullet: evidence
from seasonal changes in food availability, niche breadth and trophic overlap. Journal of
Fish Biology 59, 729744.
Cardona, L. (2006). Habitat selection by grey mullets (Osteichthyes : Mugilidae) in Mediterranean estuaries: the role of salinity. Scientia Marina 70, 443455.
Durand, J. D., Shen, K. N., Chen, W. J., Jamandre, B. W., Blel, H., Diop, K., Nirchio, M.,
de Leon, F. J. G., Whitfield, A. K., Chang, C. W. & Borsa, P. (2012). Systematics of
the grey mullets (Teleostei: Mugiliformes: Mugilidae): molecular phylogenetic evidence
challenges two centuries of morphology-based taxonomy. Molecular Phylogenetics and
Evolution 64, 7392.

2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, 86, 14441453

1452

F. L E L O C H E T A L.

Faye, D., Tito de Morais, L., Raffray, J., Sadio, O., Thiaw, O. T. & Le Loch, F. (2011). Structure
and seasonal variability of fish food webs in an estuarine tropical marine protected area
(Senegal): evidence from stable isotope analysis. Estuarine, Coastal and Shelf Science
92, 607617.
Fry, B. & Scherr, E. B. (1984). 13 C measurements as indicators of carbon flow in marine and
freshwater ecosystems. Contributions in Marine Science 27, 1347.
German, D. P. & Miles, R. D. (2010). Stable carbon and nitrogen incorporation in blood and fin
tissue of the catfish Pterygoplichthys disjunctivus (Siluriformes, Loricariidae). Environmental Biology of Fishes 89, 117133.
Gning, N., Le Loch, F., Thiaw, O. T., Aliaume, C. & Vidy, G. (2010). Estuarine resources use
by juvenile Flagfin mojarra (Eucinostomus melanopterus) in an inverse tropical estuary
(Sine Saloum, Senegal). Estuarine, Coastal and Shelf Science 86, 683691.
Gonzalez-Murcia, S., Marin-Martinez, C. & Ayala-Bocos, A. (2012). Intertidal rockpool ichthyofauna of El Pital, La Libertad, El Salvador. Check List 8, 12161219.
Green, B. C., Smith, D. J., Earley, S. E., Hepburn, L. J. & Underwood, G. J. C. (2009). Seasonal changes in community composition and trophic structure of fish populations of
five salt marshes along the Essex coastline, United Kingdom. Estuarine, Coastal and
Shelf Science 85, 247256.
Hall, S. R. (2004). Stoichiometrically explicit competition between grazers: species replacement, coexistence, and priority effects along resource supply gradients. American Naturalist 164, 157172.
Harrison, I. J. & Howes, G. J. (1991). The pharyngobranchial organ of mugilid fishes: its structure, variability, ontogeny, possible function and taxonomic utility. Bulletin of the British
Museum of Natural History Zoology 57, 111132.
Harrison, I. J. & Senou, H. (1999). Order Mugiliformes. Mugilidae. Mullets. In The Living
Marine Resources of the Western Central Pacific, FAO Species Identification Guide for
Fisheries Purposes (Carpenter, K. E. & Niem, V. H., eds), pp. 20692108. Rome: FAO.
Hesslein, R. H., Hallard, K. A. & Ramlal, P. (1993). Replacement of sulfur, carbon, and nitrogen
in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet
traced by 34 S, 13 C, and 15 N. Canadian Journal of Fisheries and Aquatic Sciences 50,
20712076.
Ibanez-Aguirre, A. L. (1993). Coexistence of Mugil cephalus and M. curema in a coastal lagoon
in the Gulf of Mexico. Journal of Fish Biology 42, 959961.
Laffaille, P., Brosse, S., Feunteun, E., Baisez, A. & Lefeuvre, J. C. (1998). Role of fish communities in particulate organic matter fluxes between salt marshes and coastal marine waters
in the Mont Saint-Michel Bay. Hydrobiologia 374, 121133.
Laffaille, P., Feunteun, E., Lefebvre, C., Radureau, A., Sagan, G. & Lefeuvre, J. C. (2002).
Can thin-lipped mullet directly exploit the primary and detritic production of European
macrotidal salt marshes? Estuarine, Coastal and Shelf Science 54, 729736.
Lasserre, G. (1976). Dynamique des populations ichthyologiques lagunaires. Application
Sparus aurata. PhD Thesis, University of Montpellier, Montpellier 2, France.
Lefeuvre, J.-C., Laffaille, P. & Feunteun, E. (1999). Do fish communities function as biotic vectors of organic matter between salt marshes and marine coastal waters? Aquatic Ecology
33, 293299.
Lujan, N. K., German, D. P. & Winemiller, K. O. (2011). Do wood-grazing fishes partition
their niche?: morphological and isotopic evidence for trophic segregation in Neotropical
Loricariidae. Functional Ecology 25, 13271338.
Luther, G. (1962). The food habits of Liza macrolepis (Smith) and Mugil cephalus L. (Mugilidae). Indian Journal of Fisheries 9, 604626.
Odum, W. E. (1968). The ecological significance of fine particle selection by the striped mullet
Mugil cephalus. Limnology and Oceanography 13, 9298.
Odum, W. E. (1970). Utilization of the direct grazing and plant detritus food chains by the
striped mullet, Mugil cephalus. In Marine Food Chains (Steele, J. H., ed.), pp. 222240.
Edinburgh: Oliver and Boyd.
Okyere, I., Aheto, D. W. & Aggrey-Fynn, J. (2011). Comparative ecological assessment of biodiversity of fish communities in three coastal wetland systems in Ghana. European Journal
of Experimental Biology 1, 178188.

2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, 86, 14441453

I S O T O P I C S I G N AT U R E S O F T W O S Y M PAT R I C M U G I L I D A E

1453

Pags, J. & Citeau, J. (1990). Rainfall and salinity of Sahelian estuary between 1927 and 1987.
Journal of Hydrology 113, 325341.
Peterson, B. J. & Fry, B. (1987). Stable isotopes in ecosystem studies. Annual Review of Ecology
and Systematics 18, 293320.
Pinnegar, J. K. & Polunin, N. V. C. (1999). Differential fractionation of 13 C and 15 N among
fish tissues: implications for the study of trophic interactions. Functional Ecology 13,
225231.
Quan, W. M., Fu, C. Z., Jin, B. S., Luo, Y. Q., Li, B., Chen, J. K. & Wu, J. H. (2007). Tidal
marshes as energy sources for commercially important nektonic organisms: stable isotope
analysis. Marine Ecology Progress Series 352, 8999.
Riera, P., Stal, L. J., Nieuwenhuize, J., Richard, P., Blanchard, G. & Gentil, F. (1999). Determination of food sources for benthic invertebrates in a salt marsh (Aiguillon Bay, France)
by carbon and nitrogen stable isotopes: importance of locally produced sources. Marine
Ecology Progress Series 187, 301307.
Sanchez Rueda, P., Gonzalez Mar, I., Ibanez Aguirre, A. L. & Marquez Garcia, A. (1997).
Sedimento en el contenido estomacal de Mugil cephalus y Mugil curema (Mugiliformes : Mugilidae) en laguna de Tamiahua, Mexico. Revista de Biologa Tropical 45,
11631166.
Shen, K. N., Jamandre, B. W., Hsu, C. C., Tzeng, W. N. & Durand, J.-D. (2011). Plio-Pleistocene
sea level and temperature fluctuations in the northwestern Pacific promoted speciation in
the globally-distributed flathead mullet Mugil cephalus. BMC Evolutionary Biology 11:
83. doi: 10.1186/1471-2148-11-83
Simier, M., Blanc, L., Aliaume, C., Diouf, P. S. & Albaret, J.-J. (2004). Spatial and temporal structure of the fish assemblages in an inverse estuary, the Sine Saloum system
(Senegal). Estuarine, Coastal and Shelf Science 59, 6986.
Sukardjo, S. (2004). Fisheries associated with mangrove ecosystem in Indonesia: a view from a
mangrove ecologist. Biotropia 23, 1339.
Tabutin, D. & Schoumaker, B. (2004). The demography of sub-Saharan Africa from the 1950s
to the 2000s. A survey of changes and a statistical assessment. Population 59, 521621.
Thollot, P., Kulbicki, M. & Harmelin-Vivien, M. (1999). Rseaux trophiques et fonctionnement trophodynamique de lichtyofaune des mangroves de Nouvelle-Caldonie.
Compte-Rendus de lAcadmie des Sciences, Paris 322, 607619.
Whitfield, A. K., Panfili, J. & Durand, J. D. (2012). A global review of the cosmopolitan flathead
mullet Mugil cephalus Linnaeus 1758 (Teleostei: Mugilidae), with emphasis on the biology, ecology, genetics and fisheries aspects of this apparent species complex. Reviews in
Fish Biology and Fisheries 22, 641681.

2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, 86, 14441453