Epibionts associated with the juvenile green turtle (Chelonia mydas) from the foraging and developmental area

of Cerro Verde, Uruguay

Luciana Alonso1, Javier Calcagno1 & Fabrizio Scarabino2
1

Laboratorio de Ecologa de Organismos Bentnicos Marinos, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires. Pabelln 2, Ciudad Universitaria C1428EHA Capital Federal, Argentina. E-mail: aloluciana@gmail.com Museo Nacional de Historia Natural y Antropologa C.C. 399, CP 11000, Montevideo, Uruguay.

INTRODUCTION
Sea turtles offer a settlement substrate for an important variety of epibiotic organisms. Despite the fact that studies of epibionts on Chelonia mydas are very scarce, this species appears to support a lower level of species richness and abundance than Caretta caretta and Eretmochelys imbricata1. Barnacles are the epibionts most frequently reported, and their distribution over the body of the turtle appears to follow an aggregated pattern. In addition, due to the hermaphroditic condition of most barnacles, settling in aggregations is indispensable in order to successfully complete their life cycle. The primary objective of this research is to characterize the epibionts associated with the juvenile green turtle (Chelonia mydas) that inhabits the Coastal-Marine Protected Area Cerro Verde and La Coronilla Islands and adjacent waters (3356 S 53 29 W) with particular emphasis on barnacles (Fig. 1). The specific goals are to: I. Identify the barnacles hosted by C. mydas to the lowest possible taxonomic level.

The most frequent barnacle taxa was Platylepas spp. followed by Chelonibia testudinaria, Amphibalanus spp., Lepas anatifera, Conchoderma virgatum and L. anserifera (Fig. 3). It is appropriate to highlight that Amphibalanus spp. were usually associated with stranded turtles that exhibited a poor health condition. a)
Platylepas spp. C. testudinaria

High proportions of opportunistic barnacles (0,98) were found during the beginning of the summer while obligate commensals showed higher proportions in the beginning of the autumn (0,99) (Fig. 6).
1 3

18

0,8

Proportion

0,6

393 700 162 506

#O / #CT #CO / #CT

0,4

0,2

163 14 December January February March

Amphibalanus spp. L. anatifera

L. anserifera

C. virgatum

II. Study the distribution patterns of barnacles on the body. III. Analyse the variations in the composition of obligate and opportunistic commensal barnacles during the study period. b)
Frequency (%)
100 80 60 40 20 0 16,09 14,94 9,20 6,90 80,46

1 cm

Fig. 6. Opportunistic (#O/#CT) and obligate (#CO/#CT) commensal barnacle proportions for each month of the study period. #O and #CO are the number of opportunistic and obligate barnacles respectively, while #CT is the total number of barnacles found. Turtles examined: 3 in December, 44 in January, 13 in February and 27 in March. The numbers on the bars indicate the abundance (N).

Barra del Chuy

DISCUSSION
Although green turtles from Cerro Verde and La Coronilla Islands hosted a greater richness of epibiont taxa than reported in studies from northern Brazil2, the percentage frequency of occurrence of the reported taxa did not exceed what has been found among C. caretta and E. imbricata3,4. The high occurrence of barnacles is in accordance with what has been previously documented for C. mydas and C. caretta from other areas, these being the most characteristic epibionts encountered on the examined sea turtles. To our knowledge, this is the first report on the interaction between Lepas anserifera and C. mydas. The other barnacle taxa encountered are in accordance with those reported for juvenile C. mydas from Rio Grande do Sul5. The clumped pattern observed on the plastron for Platylepas spp. may support the existence of behavioural mechanisms favouring aggregation of the cyprid larvae. However, differential water flow, food accessibility, desiccation, and abrasion6 may have contributed to post-settlement mortality, thus enhancing the clumped pattern observed. The increasing proportions registered for obligate commensal barnacles during the study period supports the hypothesis of seasonal migrations of green turtles along the Southwestern Atlantic Ocean7. If most turtles migrate to Brazil in response to low water temperatures during cold months and return to Cerro Verde when the water temperature increases, the longer period of permanence of the green turtles in the same area, as well as their increasing density, would favour higher obligate commensal recruitment at late summer. The higher proportions of opportunistic barnacles, such as those from the genera Amphibalanus, at the early summer may be related to the proximity to their reproductive activity in the spring and enhanced by the existence of brumation in some of the examined animals, or turtles that, due to their poor health condition, facilitate opportunistic settlement of the organisms.

1,15

vi rg at um

na ria

sp p.

an at ife

ph ib al an us

Pl at yl ep as

te st ud i

C.

L.

Punta Coronilla

Is. de la Coronilla

C.

Cerro Verde

Fig. 3. Barnacles found among captured and stranded juvenile C. mydas. a) Barnacle taxa encountered. b) Percentage frequency of occurrence. Most barnacle taxa were more frequent on the carapace (Fig.4). While Amphibalanus spp. and L. anatifera showed a high occurrence on the carapace, the ocurrence of C. testudinaria and C. virgatum was divided between the carapace and the plastron. L. anserifera was registered on the carapace of only one turtle. Platylepas spp. was the only taxa that presented a higher occurrence on the plastron followed by the skin, limbs, carapace and head. Although Platylepas spp. was more frequent on the skin than on the limbs or carapace, for the analysis of variance we decided to compare plastron, limbs and carapace because the high frequency observed was due to the high abundance (104 barnacles) on the skin of only one turtle. Platylepas spp. was significantly more frequent on the plastron than on the limbs or carapace (Plastron-Limbs P<0,05, Plastron-Carapace P<0,01, N=18), while no significant differences were found between carapace and limbs (CarapaceLimbs P=0,981).
100 80

Punta del Diablo 1 km

Fig. 1. Study area. Capture points are in blue and white points indicate the northernmost and southernmost localities sampled.

METHODS
The samples were obtained from turtles captured or stranded during the field season (December 2006 March 2007) carried out by Karumb. Digital photographs were taken of the turtles and their epibionts, which were then totally removed, their position on the body of the was recorded, and samples were preserved in 70% ethanol. The percentage frequency of occurrence was estimated for the different taxa found, considering presence and absence. Barnacles were identified, counted, and the percentage frequency of occurrence among the different sectors of the turtles body was estimated considering their abundance. Spatial pattern of distribution was analyzed using the Nearest-Neighbour Method for the most frequent taxa (Platylepas spp.). In order to study preferences on Platylepas spp. settlement position, we carried out a two factors analysis of variance (Randomized Blocks Design) followed by pairwise comparisons using Tukeys method. Finally, the proportions of occurrence between the opportunistic and obligate commensal barnacles were calculated for each month of study. Barnacles specimens will be deposited at the Museo Argentino de Ciencias Naturales Bernardino Rivadavia , Buenos Aires, Argentina, and at the Museo Nacional de Historia Natural y Antropologa, Montevideo, Uruguay.

Am

Platylepas spp. Amphibalanus spp. L. anserifera

C. testudinaria L. anatifera C. virgatum

Frequency (%)

60 40 20 0 Carapace Plastron Limbs Skin Head

L.

an se r

ife ra

sp p.

ra

ACKNOWLEDGEMENTS
We wish to thank Alejandro Fallabrino, Carlos Romero, Gustavo Martinez Souza, Melisa Morales, Rachel McDonald, Karumb technicians and the volunteers for their valuable help and co-operation in conducting this study. This research was funded by Karumb N.G.O., Laboratorio de Ecologa de Organismos Bentnicos Marinos (FCEyN, UBA) and Idea Wild. We are also grateful to Project GLOBAL, Disney Animal Kingdom, Western Pacific Regional Fisheries Management Council, US National Marine Fisheries Service, US Fish and Wildlife Service (Marine Turtle Conservation Fund), David and Lucille Packard Foundation, the Sandler Family Foundation, Carlos Peralta Quintero and Robert N. Allen, Jr. for their financial support, which enabled LA to attend the symposium.

Fig. 4. Percentage frequency of occurrence of barnacles on the bodies of stranded and captured turtles. A clumped spatial pattern of distribution on the plastron was detected for Platylepas spp. in 10 of the 13 examined turtles (Fig. 5).
1 2 3 4 5

RESULTS
All of the 87 green turtles examined were juveniles (mean standard Curved Carapace Length, CCL=39,9 5,3 cm, range=31,6-56,0 cm), 71 were captured, while 16 were stranded turtles. Only 10,34% were free of epibonts, while 14 taxa were found among the rest of the turtles. Barnacles were the most frequent (87,36%), followed by algae (24,14%) and leeches (17,24%). The rest of the organisms found were polychaetes (6,90%), hydrozoans (4,60%), amphipods (4,60%), bivalves such as mussels (3,45%) and oysters (2,30%), gastropods (2,30%), crabs (2,30%), isopods (2,30%), bryozoans (2,30%) and polycladids worms (1,15%). Whilst 79,3% of the examined turtles were characterized by hosting barnacles, algae and/or leeches, the other 11 taxa reported were found among only 10,3% of the turtles, most of which exhibited a poor health condition (Fig. 2).

LITERATURE CITED
1. Garca M., Ferreira M.B., Calvario J. & Al-Kiyumi A., 2000. The first report of epizoic algae or nesting green turtles, Chelonia mydas, at Ras Al Hadd Turtle Reserve, Arabian Sea, Oman. In: Seminoff J.A. (compiler). Proceedings of the Twenty-second Annual Symposium on Sea Turtle Biology and Conservation. NOAA Technical Memorandum NMFS-SEFSC-503, p. 210. 2. Pereira S., Lima E., Mathews H. & Ventura A., 2006. Epibionts associated with Chelonia mydas from northern Brazil. Marine Turtle Newsletter, 111: 17-18. 3. Frick, M.G., Mason P.A., Williams K.L., Andrews K. & Gerstung H., 2003. Epibionts of hawksbill turtles in a Caribbean nesting ground: A potentially unique association with snapping shrimp (Crustacea: Alpheidae). Marine Turtle Newsletter, 99: 8-11. 4. Badillo F.J., 2007. Epizotos y parsitos de la tortuga boba (Caretta caretta) en el Mediterrneo Occidental. PhD Thesis. Facultat de Ciencies Biologiques. Univesitat de Valencia, 262 pp. 5. Bugoni L., Krause L., Almeida A.O. & Padua Bueno A.A., 2001. Commensal barnacles of sea turtles in Brazil. Marine Turtle Newsletter, 94: 7-9. 6. Pfaller J.B., Bjorndal K.A., Reich K.J., Williams K.L. & Frick M.G., 2006. Distribution patterns of epibionts on the carapace of loggerhead turtles, Caretta caretta. JMBA2 Biodiversity Records: 1-4. 7. Lpez-Mendilaharsu M., Estrades A., Caraccio M.N., Calvo V., Hernndez M. & Quirici V., 2006. In: Menafra R., Rodrguez-Gallego L., Scarabino F. & Conde D. (editors). Bases para la conservacin y el manejo de la costa uruguaya. Vida Silvestre Uruguay, Montevideo, pp. 247-257.

P < 0,01 N = 12

P < 0,01 N = 17

P < 0,01 N = 23

P = < 0,01 N = 14

P < 0,01 N = 14

10

P < 0,01 N = 32

P < 0,01 N = 23

P < 0,01 N = 15

P < 0,05 N = 38

P < 0,1 N = 23

11

12

13

P = 0,186 N = 10

P = 0,204 N = 17

P = 0,445 N = 11

Fig. 2. Turtle hosting a high taxa richness and exhibiting a poor health condition.

Fig. 5. Spatial pattern of distribution for Platylepas spp. over the plastron and marginal scutes in ventral view of the carapace.