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Assortative epibiosis of leatherback, olive ridley and green sea turtles in the Eastern Tropical Pacific

Published online by Cambridge University Press:  19 May 2016

Nathan J. Robinson ,
Eric A. Lazo-Wasem ,
Frank V. Paladino ,
John D. Zardus  and
Theodora Pinou
Nathan J. Robinson*
Affiliation:
The Leatherback Trust, Goldring-Gund Marine Biology Station, Playa Grande, Guanacaste, Costa Rica Department of Biology, Indiana University-Purdue University Fort Wayne, Fort Wayne, Indiana, USA
Eric A. Lazo-Wasem
Affiliation:
Division of Invertebrate Zoology, Peabody Museum of Natural History, Yale University, New Haven, Connecticut, USA
Frank V. Paladino
Affiliation:
The Leatherback Trust, Goldring-Gund Marine Biology Station, Playa Grande, Guanacaste, Costa Rica Department of Biology, Indiana University-Purdue University Fort Wayne, Fort Wayne, Indiana, USA
John D. Zardus
Affiliation:
Department of Biology, The Citadel, Charleston, South Carolina, USA
Theodora Pinou
Affiliation:
Department of Biological and Environmental Sciences, Western Connecticut State University, Danbury, Connecticut, USA
*
Correspondence should be addressed to:N. J. Robinson, The Leatherback Trust, Goldring-Gund Marine Biology Station, Playa Grande, Guanacaste, Costa Rica and Department of Biology, Indiana University-Purdue University Fort Wayne, Fort Wayne, Indiana, USA email: nathan@leatherback.org
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Abstract

Sea turtles host a diverse array of epibionts, yet it is not well understood what factors influence epibiont community composition. To test whether epibiont communities of sea turtles are influenced by the hosts’ nesting or foraging habitats, we characterized the epibiota of leatherback, olive ridley and green turtles nesting at a single location on the Pacific coast of Costa Rica. We also compared the epibiota of these turtles to conspecific populations nesting elsewhere in the East Pacific. If epibiont communities are influenced by nesting habitats, we predicted that sympatrically nesting turtles would have comparable epibiont taxa. Alternatively, if epibiont communities are influenced by foraging habitats, we predicted the diversity of epibiont taxa should reflect the type and diversity of the hosts’ foraging habitats. We identified 18 epibiont taxa from 18 leatherback, 19 olive ridley and six green turtles. Epibiont diversity was low on leatherbacks (four taxa), but higher for olive ridley and green turtles (12 and nine epibiont taxa respectively). The epibiont communities of olive ridley and green turtles were not statistically different, but both were different from leatherbacks. In addition, conspecific sea turtles from other nesting locations hosted more similar epibiont communities than sympatrically nesting, non-conspecifics. We conclude that epibiont diversity of nesting sea turtles is partially linked to the diversity of their foraging habitats. We also conclude that the surface properties of the skin and carapace of these turtles may contribute to the uniqueness of leatherback turtle epibiont communities and the similarities between olive ridley and green turtle epibiont communities.

Keywords

community structureChelonia mydasDermochelys coriaceaEastern Tropical PacificepibiotaepibiontLepidochelys olivaceamarine turtlesParque Nacional Marino Las Baulassea turtles
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 97 , Issue 6 , September 2017 , pp. 1233 - 1240
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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References

REFERENCES

Amorocho, D.F. and Reina, R.D. (2007) Feeding ecology of the East Pacific green sea turtle Chelonia mydas agassizii at Gorgona National Park, Colombia. Endangered Species Research 3, 43–51.Google Scholar
Angulo-Lozano, L., Nava-Duran, P.R. and Frick, M.G. (2007) Epibionts of olive ridley turtles nesting at Playa Ceuta, Sinaloa, Mexico. Marine Turtle Newsletter 118, 13–14.Google Scholar
Bailey, H., Benson, S.R., Shillinger, G.L., Bograd, S.J., Dutton, P.H., Eckert, S.A., Morreale, S.J., Paladino, F.V., Eguchi, T., Foley, D.G., Block, B.A., Piedra, R., Hitipeuw, C., Tapilatu, R.F. and Spotila, J.R. (2012) Identification of distinct movement patterns in Pacific leatherback turtle populations influenced by ocean conditions. Ecological Applications 22, 735–747.Google Scholar
Behera, S., Tripathy, B., Sivakumar, K. and Choudhury, B.C. (2015) Stomach contents of olive ridley turtles (Lepidochelys olivacea) occurring in Gahirmatha, Odisha coast of India. Proceedings of the Zoological Society 68, 91–95.Google Scholar
Blanco, G.S., Morreale, S.J., Bailey, H., Seminoff, J.A., Paladino, F.V. and Spotila, J.R. (2012) Post-nesting movements and feeding grounds of a resident East Pacific green turtle Chelonia mydas population from Costa Rica. Endangered Species Research 18, 233–245.Google Scholar
Blanco, G.S., Morreale, S.J., Seminoff, J.A., Paladino, F.V., Piedra, R. and Spotila, J.R. (2013) Movement and diving behavior of internesting green turtles along Pacific Costa Rica. Integrative Zoology 8, 293–306.CrossRefGoogle ScholarPubMed
Caine, E.A. (1986) Carapace epibionts of nesting loggerhead sea turtles: Atlantic coast of U.S.A. Journal of Experimental Biology and Ecology 95, 15–26.CrossRefGoogle Scholar
Carriol, R.P. and Vader, W. (2002) Occurrence of Stomatolepas elegans (Cirripedia: Balanomorpha) on a leatherback turtle from Finmark, northern Norway. Journal of the Marine Biological Association of the United Kingdom 82, 1033–1034.CrossRefGoogle Scholar
Colman, L.P., Sampaio, C.L.S., Weber, M.I. and Comin De Castilhos, J. (2014) Diet of olive ridley sea turtles, Lepidochelus olivacea, in the waters of Sergipe, Brazil. Chelonian Conservation and Biology 13, 266–271.Google Scholar
Colwell, R.K., Chao, A., Gotelli, N.J., Lin, S.-Y., Mao, C.X., Chazdon, R.L. and Longino, J.T. (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation, and comparison of assemblages. Journal of Plant Ecology 5, 3–21.Google Scholar
Delgado Trejo, C. and Diaz, J.A. (2012) Current conservation status of the black sea turtle in Michoacan, Mexico. In Seminoff, J.A. and Wallace, B.P. (eds) Sea turtles of the Eastern Pacific: advances in research and conservation. Tucson, AZ: University of Arizona Press, pp. 263–278.Google Scholar
Domènech, F., Badillo, F.J., Tomás, J., Raga, J.A. and Aznar, F.J. (2015) Epibiont communities of loggerhead marine turtles (Caretta caretta) in the western Mediterranean: influence of geographic and ecological factors. Journal of the Marine Biological Association of the United Kingdom 95, 851–861.Google Scholar
Fonseca, L., Murillo, G.A., Guadamúz, L., Spínola, R.M. and Valverde, R.A. (2009) Downward but stable trend in the abundance of Arribada olive ridley sea turtles (Lepidochelys olivacea) at Nancite Beach, Costa Rica (1971–2007). Chelonian Conservation and Biology 8, 19–27.Google Scholar
Frick, M., Williams, K. and Robinson, M. (1998) Epibionts associated with nesting loggerhead sea turtles (Caretta caretta) in Georgia. Herpetological Review 29, 211–214.Google Scholar
Frick, M.G. and Pfaller, J.B. (2013) Sea turtle epibiosis. In Wyneken, J., Lohmann, K.J. and Musick, J.A. (eds) The biology of sea turtles, Volume 3. Boca Raton, FL: CRC Press, pp. 399–426.Google Scholar
Frick, M.G. and Zardus, J.D. (2010) First authentic report of the turtle barnacle Cylinolepas darwiniana since its description in 1916. Journal of Crustacean Biology 30, 292–295.Google Scholar
Frick, M.G., Zardus, J.D. and Lazo-Wasem, E.A. (2010) A new Stomatolepas barnacle species (Cirripedia: Balanomorpha: Coronuloidea) from leatherback sea turtles. Bulletin of the Peabody Museum of Natural History 51, 123–126.CrossRefGoogle Scholar
Fuller, W.J., Broderick, A.C., Enever, R., Thorne, P. and Godley, B.J. (2010) Motile homes: a comparison of the spatial distribution of epibiont communities on Mediterranean sea turtles. Journal of Natural History 44, 1743–1753.Google Scholar
Gámez Vivaldo, S., Ororio Sarabia, D., Peñaflores Salazar, C., García Hernández, A. and Ramírez Lezema, J. (2006) Identificación de parásitos y epibiontes de la tortuga golfina (Lepidochelys olivacea) que arribó a playas de Michoacán y Oaxaca, México. Veterinaria México 37, 431–440.Google Scholar
Greenblatt, R.J., Work, T.M., Balazs, G.H., Sutton, C.A., Casey, R.N. and Casey, J.W. (2004) The Ozobranchus leech is a candidate mechanical vector for the fibropapilloma-associated turtle herpesvirus found latently infecting skin tumors on Hawaiian green turtles (Chelonia mydas). Virology 1, 101–110.CrossRefGoogle Scholar
Hart, C.E., Blanco, G.S., Coyne, M.S., Delgado-Trejo, C., Godley, B.J., Jones, T.T., Resendiz, A., Seminoff, J.A., Witt, M.J. and Nichols, W.J. (2015) Multinational tagging efforts illustrate regional scale of distribution and threats for East Pacific green turtles (Chelonia mydas agassizii). PLoS ONE 10, e0116225.Google Scholar
Hayashi, R. (2009) New host records of the turtle barnacle, Cylindrolepas sinica: a case study of sea turtles’ behaviour and their epibionts. Marine Biodiversity Records 2, e165.Google Scholar
Hayashi, R. and Tsuji, K. (2008) Spatial distribution of turtle barnacles on the green sea turtle, Chelonia mydas . Ecological Research 23, 121–125.Google Scholar
Hays, G.C., Åkesson, S., Broderick, A.C., Glen, F., Godley, B.J., Luschi, P., Martin, C., Metcalfe, J.D. and Papi, F. (2001) The diving behaviour of green turtles undertaking oceanic migration to and from Ascension Island: dive durations, dive profiles and depth distribution. Journal of Experimental Biology 204, 4093–4098.Google Scholar
Hernández-Vásquez, S. and Valadez-González, C. (1998) Observaciones de los epizoarios encontrados sobre la tortuga golfina Lepidochelys olivacea en La Gloria, Jalisco, México. Ciencias Marinas 24, 119–125.Google Scholar
Houghton, J.D.R., Doyle, T.K., Davenport, J., Wilson, R.P. and Hays, G.C. (2008) The role of infrequent and extraordinary deep dives in leatherback turtles (Dermochelys coriacea). Journal of Experimental Biology 211, 2566–2575.Google Scholar
IUCN (2014) IUCN red list of threatened species. Version 2014.2. <www.iucnredlist.org>. Downloaded on 6 November 2014..+Downloaded+on+6+November+2014.>Google Scholar
Lazo-Wasem, E.A., Pinou, T., Peña de Niz, A. and Feuerstein, A. (2011) Epibionts associated with the nesting marine turtle Lepidochelys olivacea and Chelonia mydas in Jalisco, Mexico: a review and field guide. Bulletin of the Peabody Museum of Natural History 52, 221–240.Google Scholar
Lazo-Wasem, E.A., Pinou, T., Peña de Niz, A., Salgado, M.A. and Schenker, E. (2007) New records of the marine turtle epibiont Balaenophilus umigamecolus (Copepoda: Harpacticoida: Balaenophilidae): new host records and possible implications for marine turtle health. Bulletin of the Peabody Museum of Natural History 48, 153–156.Google Scholar
Majewska, R., Santoro, M., Bolaños, F., Chaves, G. and De Stafano, M. (2015) Diatoms and other epibionts associated with olive ridley (Lepidochelys olivacea) sea turtles from the Pacific coast of Costa Rica. PLoS ONE, e0130351.Google Scholar
Mestre, N.C., Thatje, S. and Tyler, P.A. (2009) The ocean is not deep enough: pressure tolerances during early ontogeny of the blue mussel Mytilus edulis . Proceedings of the Royal Society B Biological Sciences 276, 717–726.Google Scholar
Oliphant, A., Thatje, S., Brown, A., Morini, M., Ravaux, J. and Shillito, B. (2011) Pressure tolerance of the shallow-water caridean shrimp Palaemonetes varians across its thermal tolerance window. Journal of Experimental Biology 214, 1109–1117.CrossRefGoogle ScholarPubMed
Pfaller, J.B., Alfaro-Shigueto, J., Balazs, G., Ishihara, T., Kopitsky, K., Mangel, J.C., Peckham, S.H., Bolten, A.B. and Bjorndal, K.A. (2014) Hitchhikers reveal cryptic host behavior: new insights from the association between Planes major and sea turtles in the Pacific Ocean. Marine Biology 161, 2167–2178.Google Scholar
Pfaller, J.B., Frick, M.G., Reich, K.J., Williams, K.L. and Bjorndal, K.A. (2008) Carapace epibionts of loggerhead turtles (Caretta caretta) nesting at Canaveral National Seashore, Florida. Journal of Nature History 42, 13–14.Google Scholar
Pinou, T., Lazo-Wasem, E.A., Dion, K. and Zardus, J.D. (2013) Six degrees of separation in barnacles? Assessing genetic variability in the sea-turtle epibiont Stomatolepas elegans (Costa) among turtles, beaches and oceans. Journal of Natural History 47, 2193–2212.Google Scholar
Plotkin, P.T. (2010) Nomadic behaviour of the highly migratory olive ridley sea turtle Lepidochelys olivacea in the eastern tropical Pacific Ocean. Endangered Species Research 13, 33–40.CrossRefGoogle Scholar
Plotkin, P.T., Byles, R.A., Rostal, D.C. and Owens, D.W. (1995) Independent versus socially facilitated oceanic migrations of the olive ridley, Lepidochelys olivacea . Marine Biology 122, 137–143.Google Scholar
Polovina, J.J., Howell, E., Parker, D.M. and Balazs, G.H. (2002) Dive-depth distribution of loggerhead (Carretta carretta) and olive ridley (Lepidochelys olivacea) sea turtles in the central North Pacific: might deep longline sets catch fewer turtles? Fisheries Bulletin 101, 189–193.Google Scholar
Robinson, N.J., Thatje, S. and Osseforth, C. (2009) Heartbeat sensors under pressure: a new method for assessing hyperbaric physiology. High Pressure Research 29, 422–430.Google Scholar
Santidrián Tomillo, P., Vélez, E., Reina, R.D., Piedra, R., Paladino, F.V. and Spotila, J.R. (2008) Reassessment of the leatherback turtle (Dermochelys coriacea) nesting population at Parque Nacional Marino Las Baulas, Costa Rica: effects of conservation efforts. Chelonian Conservation and Biology 6, 54–62.Google Scholar
Seminoff, J.A., Resendiz, A. and Nichols, W.J. (2002) Diet of East Pacific green turtles (Chelonia mydas) in the central Gulf of California, México. Journal of Herpetology 36, 447–453.Google Scholar
Shillinger, G.L., Palacios, D.M., Bailey, H., Bograd, S.J., Swithenbank, A.M., Gaspar, P., Wallace, B.P., Spotila, J.R., Paladino, F.V., Piedra, R., Eckert, S.A. and Block, B.A. (2008) Persistent leatherback turtle migrations present opportunities for conservation. PLoS Biology 6, e171.Google Scholar
Shillinger, G.L., Swithenbank, A.M., Bograd, S.J., Bailey, H., Castelton, M.R., Wallace, B.P., Spotila, J.R., Paladino, F.V., Piedra, R. and Block, B. (2010) Identification of high-use internesting habitats for eastern Pacific leatherback turtles: role of the environment and implications for conservation. Endangered Species Research 10, 215–232.Google Scholar
Spotila, J.R., Reina, R.D., Steyermark, A.C., Plotkin, P.T. and Paladino, F.V. (2000) Pacific leatherback turtles face extinction. Nature 405, 529–530.Google Scholar
Wallace, B.P., Zolkewitz, M. and James, M.C. (2015) Fine-scale foraging ecology of leatherback turtles. Frontiers in Ecology and Evolution 3, 15.Google Scholar
Ward, J.H. Jr (1963) Hierarchical grouping to optimize an objective function. Journal of the American Statistical Association 58, 236–244.Google Scholar