Abstract
The present study combines esophageal lavage (n = 74), stomach content (n = 52) and stable isotope analysis (n = 126) to understand the ontogenetic dietary shift of green turtles (Chelonia mydas) inhabiting the temperate waters off Uruguay. Based on esophageal and stomach analysis, green turtles in the region start consuming macroalgae soon after recruiting to neritic habitats; however, gelatinous macrozooplankton is still a major component of the diet of neritic juvenile green turtles measuring of less than 45 cm in curved carapace length (CCL). Conversely, turtles larger than 45 cm CCL were predominantly herbivores, with a gradual increase in the occurrence of macroalgae with size. Stable isotope analysis confirmed the dietary pattern revealed by esophageal lavage and stomach contents analysis, and also revealed that most of the green turtles smaller than 50 cm CCL found in Uruguayan waters had moved from Brazil only a few months ago. This conclusion is based on the large differences in the δ15N values of potential prey from southern Brazil and Uruguay and on a strong signal from Brazilian macrophytes in the skin of most green turtles from Uruguay. Turtles larger than 50 cm CCL, conversely, made a more prolonged use of Uruguayan foraging grounds. Furthermore, according to the stable isotope ratios in their skin, some turtles remained year round in Uruguayan coastal waters. The overall evidence indicates that green turtles inhabiting the coastal waters off Uruguay exhibit a rapid, but not abrupt, dietary shift after recruiting to neritic habitats and are best described as omnivores than as pure herbivores, with a relevant role of gelatinous macrozooplankton in their diets. Furthermore, most of the turtles spend only short periods in the area and their primary foraging grounds are in Brazil.
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References
Acha EM, Mianzan HW, Guerrero RA, Favero M, Bava J (2004) Marine fronts at the continental shelves of austral South America: physical and ecological processes. J Mar Syst 44:83–105
Almeida AP, Moreira LMP, Bruno SC, Thome ́ JCA, Martins AS, Bolten AB, Bjorndal KA (2011) Green turtle nesting on Trindade Island, Brazil: abundance, trends and biometrics. Endanger Species Res 14:193–201
Amorocho DF, Reina RD (2007) Feeding ecology of the East Pacific green sea turtle Chelonia mydas agassizii at Gorgona National Park, Colombia. Endanger Species Res 3:43–51
Arthur KE, Boyle MC, Limpus CJ (2008) Ontogenetic changes in diet and habitat use in green sea turtle (Chelonia mydas) life history. Mar Ecol Prog Ser 362:303–311. doi:10.3354/meps07440
Bellini C, Santos AJB, Grossman A, Marcovaldi MÂ, Barata PCR (2013) Green turtle (Chelonia mydas) nesting on Atol das Rocas, north-eastern Brazil, 1990–2008. J Mar Biol Assoc UK 93:1117–1132
Bethea D, Hale L, Carlon JK, Cortés E, Manire CA, Gelsleichter J (2007) Geographic and ontogenetic variation in the diet and daily ration of the bonnethead shark, Sphyrna tiburo, from the eastern Gulf of Mexico. Mar Biol 152:1009–1020
Bjorndal KA (1980) Nutrition and grazing behaviour of the green turtle Chelonia mydas. Mar Biol 56:147–154
Bjorndal KA (1985) Nutritional ecology of sea turtles. Copeia 3:736–751
Bjorndal KA (1997) Foraging ecology and nutrition of sea turtles. In: Lutz PL, Musick JA (eds) The biology of sea turtles. CRC Press, Boca Ratón, pp 199–231
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917
Bolten AB (2003) Variation in sea turtle life history patterns: neritic vs. oceanic developmental stages. In: Lutz PL, Musick J, Wyneken J (eds) The Biology of Sea Turtles, vol II. CRC Press, Boca Raton, pp 243–257
Borthagaray AI, Carranza A (2007) Mussels as ecosystem engineers: their contribution to species richness in a rocky littoral community. Act Oeco 31:243–250
Burkholder DA, Heithaus MR, Thomson JA, Fourqurean JW (2011) Diversity in trophic interactions of green sea turtles Chelonia mydas on a relatively pristine coastal foraging ground. Mar Ecol Prog Ser 439:277–293. doi:10.3354/meps09313
Campos EJD, Piola AR, Matano RP, Miller JL (2008) PLATA: a synoptic characterization of the southwest Atlantic shelf under influence of the Plata River and Patos Lagoon outflows. Cont Shelf Res 28:1551–1555
Cardona L, Aguilar A, Pazos L (2009) Delayed ontogenic dietary shift and high levels of omnivory in green turtles (Chelonia mydas) from the NW coast of Africa. Mar Biol 156:1487–1495. doi:10.1007/s00227-009-1188-z
Cardona L, Campos P, Levy Y, Demetropoulos A, Margaritoulis D (2010) Asynchrony between dietary and nutritional shifts during the ontogeny of green turtles (Chelonia mydas) in the Mediterranean. J Exp Mar Biol Ecol 393:83–89. doi:10.1016/j.jembe.2010.07.004
Carrión-Cortez JA, Zárate P, Seminoff JA (2010) Feeding ecology of the green sea turtle (Chelonia mydas) in the Galapagos Islands. J Mar Biol Assoc UK 90:1005–1013
Cardona L, Alvarez de Quevedo I, Borrell A, Aguilar A (2012) Massive consumption of gelatinous plankton by Mediterranean apex predators. PLoS ONE 7:e31329. doi:10.1371/journal.pone.0031329
Coelho Claudino M, Abreu PC, Miranda Garcia A (2013) Stable isotopes reveal temporal and between-habitat changes in trophic pathways in a southwestern Atlantic estuary. Mar Ecol Prog Ser 489:29–42. doi:10.3354/meps10400
Coll J, Oliveira EC (1999) The Benthic Marine Algae of Uruguay. Bot Mar 42(1):129–135
Costalago D, Navarro J, Álvarez-Calleja I, Palomera I (2012) Ontogenetic and seasonal changes in the feeding habits and trophic levels of two small pelagic fish species. Mar Ecol Prog Ser 460:169–181
Dalerum F, Angerbjörn A (2005) Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144:647–658. doi:10.1007/s00442-005-0118-0
Defeo O, Horta S, Carranza A, Lercari D, de Álava A, Gómez J, Martínez G, Lozoya JP, Celentano E (2009) Hacia un Manejo Ecosistémico de Pesquerías. Áreas Marinas Protegidas en Uruguay, Facultad de Ciencias-DINARA, Montevideo
DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506
DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351
Drago M, Franco-Trecu V, Zenteno L, Szteren D, Cardona L (2015) Sexual foraging segregation in South American sea lions increases during the pre-breeding period in the Río de la Plata plume. Mar Ecol Prog Ser 525:261–272
Forbes G, Limpus C (1993) A non-lethal method for retrieving stomach contents from sea turtles. Wildlife Res 20:339–343
Garnett ST, Pirce IR, Scott FJ (1985) The diet of the green turtle, Chelonia mydas (L.), in Torres Strait. Aust Wildlife Res 12:103–112
Gonzalez Carman V, Falabella V, Maxwell S, Albareda D, Campagna C, Mianzan H (2012) Revisiting the ontogenetic shift paradigm: the case of juvenile green turtles in the SW Atlantic. J Exp Mar Biol Ecol 429:64–72. doi:10.1016/j.jembe.2012.06.007
Gonzalez Carman V, Botto F, Gaitán E, Albareda D, Campagna C, Mianzan H (2013) A jellyfish diet for the herbivorous green turtle Chelonia mydas in the temperate SW Atlantic. Mar Biol 161(2):339–349. doi:10.1007/s00227-013-2339-9
Hastie TJ, Tibshirani RJ (1990) Generalized additive models. Monog Stat Appl Prob 43, Chapman and Hall, London
Hatase H, Sato K, Yamaguchi M, Takahashi K, Tsukamoto K (2006) Individual variation in feeding habitat use by adult female green sea turtles (Chelonia mydas): are they obligately neritic herbivores? Oecologia 149:52–64
Hernández-García V (1995) The diet of the swordfish Xiphias gladius Linnaeus, 1758, in the central east Atlantic, with emphasis on the role of cephalopod s. Fish Bull 93:403–411
Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326
Horta S, Defeo O (2012) The spatial dynamics of the whitemouth croaker artisanal fishery in Uruguay and interdependencies with the industrial fleet. Fish Res 125–126:121–128
Hyslop EJ (1980) Stomach contents analysis-a review of methods and their application. J Fish Biol 17:41–429
Kelez S (2011) Bycatch and foraging ecology of sea turtles in the eastern Pacific. PhD dissertation, Duke University, Durham, NC
Lazzari L (2012) Isótopos estáveis de carbono e nitrógeno aplicados ao estudio da ecología trófica do peixe-boi marinho (Trichechus manatus). Master Thesis, Programa de Pós-graduaçao em Oceanografia Biológica, Universidad Federal do Rio Grande
Leathwick JR, Elith J, Hastie T (2006) Comparative performance of generalized additive models and multivariate adaptive regression splines for statistical modelling of species distributions. Ecol Mod 199:188–196
Lemons G, Lewison R, Komoroske L, Gaos A, Lai CT, Dutton P, Eguchi T, LeRoux R, Seminoff JA (2011) Trophic ecology of green sea turtles in a highly urbanized bay: insights from stable isotopes and mixing models. J Exp Mar Biol Ecol 405:25–32. doi:10.1016/j.jembe.2011.05.012
Longhurst A (1998) Ecological geography of the sea. Academic Press, San Diego
López-Mendilaharsu M, Gardner SC, Seminoff JA, Riosmena-Rodriguez R (2005) Identifying critical foraging habitats of the green turtle (Chelonia mydas) along the Pacific coast of the Baja California peninsula, Mexico. Aquat Conserv Mar Freshw Ecosyst 15:259–269
López-Mendilaharsu M, Estrades A, Caraccio MN, Calvo V, Hernández M, Quirici V (2006) Biología, ecología y etología de las tortugas marinas en la zona costera uruguaya. In: Menafra R, Rodríguez-Gallego L, Scarabino F, Conde D (eds) Bases para la conservación y el manejo de la costa uruguaya. Vida Silvestre Uruguay, Montevideo, pp 247–257
López-Mendilaharsu M, Gardneri SC, Riosmena-Rodriguez R, Seminoff JA (2008) Diet selection by immature green turtles (Chelonia mydas) at Bahia Magdalena foraging ground in the Pacific Coast of the Baja California Penin- sula, Mexico. J Mar Biol Assoc UK 88:641–647
Makowski C, Seminoff J, Salmon M (2006) Home range and habitat use of juvenile Atlantic green turtles (Chelonia mydas L.) on shallow reef habitats in Palm Beach, Florida, USA. Mar Biol 148:1167–1179
Martinez Souza G (2015) Caracterizaçao populacional de juvenis de tartaruga-verde (Chelonia mydas) em duas áreas do Atlântico Sul Ocidental. PhD Thesis, Programa de Pós-graduaçao em Oceanografia Biológica, Universidad Federal do Rio Grande, Brazil
McCann KS (2012) Food webs. Princeton University Press, Princeton
Morais RA, dos Santos RG, Longo GO, Yoshida ETE, Stahelin GD, Horta PA (2014) Direct evidence for gradual ontogenetic dietary shift in the green turtle chelonia mydas. Chelonian Conserv Biol 13(2):260–266
Nagaoka S, Martins A, Santos R, Tognella M, Oliveira Filho E, Seminoff JA (2012) Diet of juvenile green turtles (Chelonia mydas) associating with artisanal fishing traps in a subtropical estuary in Brazil. Mar Biol 159:573–589. doi:10.1007/s00227-011-1836-y
Oliveira EC (1984) Brazilian mangal vegetation with special emphasis on the seaweeds. In: Por FD, Dor I (eds) Hydrobiology of the Mangal. W. Junkers Publ, The Hague, pp 55–65
Ortega L, Martínez A (2007) Multiannual and seasonal variability of water masses and fronts over the Uruguayan shelf. J Coast Res 23:618–629
Parker D, Dutton PH, Balazs GH (2011) Oceanic diet and distribution of haplotypes for the green turtle, Chelonia mydas, in the central North Pacific. Pac Sci 65(4):419–431
Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source Partitioning Using Stable Isotopes: coping with Too Much Variation. PLoS ONE 5(3):e9672. doi:10.1371/journal.pone.0009672
Payo-Payo A, Ruiz B, Cardona L, Borrell A (2013) Effect of tissue decomposition on stable isotope signatures of striped dolphins Stenella coeruleoalba and loggerhead sea turtles Caretta caretta. Aquat Biol 18:141–147
Pinkas L, Oliphant MS, Iverson ILK (1971) Food habits of albacore, bluefin tuna, and bonito in California waters. Fish Bull 152:1–105
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83:703–718
R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 20 Jan 2014
Reich KJ, Bjorndal KA, Bolten AB (2007) The ‘lost years’ of green turtles: using stable isotopes to study cryptic life stages. Biol Lett 3:712–714. doi:10.1098/rsbl.2007.0394
Reich KJ, Bjorndal KA, Martinez del Rio C (2008) Effects of growth and tissue type on the kinetics of 13C and 15 N incorporation in a rapidly growing ectotherm. Oecologia 155:651–663
Reisser J, Proietti M, Sazima I, Kinas P, Horta P, Secchi E (2013) Feeding ecology of the green turtle (Chelonia mydas) at rocky reefs in western South Atlantic. Mar Biol 160:3169–3179
Russell DJ, Balazs GH (2009) Dietary shifts by green turtles (Chelonia mydas) in the Kane’ohe Bay region of the Hawaiian Islands: a 28-year study. Pac Sci 63:181–192
Russell DJ, Hargrove S, Balazs GH (2011) Marine sponges, other animal food, and nonfood items found in digestive tracts of the herbivorous marine turtle Chelonia mydas in Hawaii. Pac Sci 65:375–381
Santos RG, Silva Martins A, Batista MB, Horta PA (2015) Regional and local factors determining green turtle Chelonia mydas foraging relationships with the environment. Mar Ecol Prog Ser 529:265–277
Seminoff JA, Resendiz A, Nichols WJ (2002) Diet of East Pacific green turtles (Chelonia mydas) in the central Gulf of California, Mexico. J Herpetol 36:447–453
Seminoff JA, Jones TT, Eguchi T, Jones DR, Dutton PH (2006) Stable isotope discrimination (δ13C and δ15N) between soft tissues of the green sea turtle Chelonia mydas and its diet. Mar Ecol Prog Ser 308:271–278
Tomás J, Aznar FJ, Raga JA (2001) Feeding ecology of the loggerhead turtle Caretta caretta in the western Mediterranean. J Zool 255(04):525–532
Vander Zanden HB, Arthur KE, Bolten AB, Popp BN, Lagueux CJ, Harrison E, Campbell CL, Bjorndal KA (2013) Trophic ecology of a green turtle breeding population. Mar Ecol Prog Ser 476:237–249
Vales DG, Saporiti F, Cardona L, De Oliveira LR et al (2014) Intensive fishing has not forced dietary change in the South American fur seal Arctophoca (= Arctocephalus) australis off Río de la Plata and adjoining areas. Aquat Conserv Mar Freshw Ecosyst 24:745–759
Vales DV, Cardona L, García NA, Zenteno L, Crespo EA (2015) Ontogenetic dietary changes in male South American fur seals Arctocephalus australis in Patagonia. Mar Ecol Prog Ser 525:245–260
Vélez-Rubio GM, Estrades A, Fallabrino A, Tomás J (2013) Marine turtle threats in Uruguayan waters: insights from 12 years of stranding data. Mar Biol 160:2797–2811
Vélez-Rubio G, Tomás J, Míguez-Lozano R, Xavier JC, Martinez Souza G, Carranza A (2015) New insights in southwestern Atlantic Ocean Oegopsid squid distribution based on juvenile green turtle (Chelonia mydas) diet analysis. Mar Biodiver 45:701–709. doi:10.1007/s12526-014-0272-x
Wallace BP, DiMatteo AD, Hurley BJ, Finkbeiner EM, Bolten AB et al (2010) Regional Management Units for Marine Turtles: a Novel Framework for Prioritizing Conservation and Research across Multiple Scales. PLoS ONE 5(12):e15465
Weber SB, Weber N, Ellick J, Avery A, Frauenstein R, Godley BJ, Broderick AC (2014) Recovery of the South Atlantic’s largest green turtle nesting population. Biodivers Conserv 23(12):3005–3018
Williams NC, Bjorndal KA, Lamont MM, Carthy RR (2013) Winter Diets of Immature Green Turtles (Chelonia mydas) on a Northern Feeding Ground: integrating Stomach Contents and Stable Isotope Analysis. Estuaries Coasts 37(4):986–994. doi:10.1007/s12237-013-9741-x
Witherington BE, Ehrhart LM (1989) Hypothermic stunning and mortality of marine turtles in the Indian River lagoon system, Florida. Copeia
Wood S (2011) gamm4: Generalized additive mixed models using mgcv and lme4. R package version 0.1–2
Xavier JC, Croxall JP, Cresswell KA (2005) Boluses: a simple, cost- effective diet method to assess the cephalopod prey of albatrosses? Auk 122:1182–1190
Zenteno L, Crespo E, Vales D, Silva L, Saporiti F, Oliveira LR, Secchi ER, Drago M, Aguilar A, Cardona L (2015) Dietary consistency of male South American sea lions (Otaria flavescens) in southern Brazil during three decades inferred from stable isotope analysis. Mar Biol 162:275–289
Acknowledgments
We would like to thank the volunteers and Karumbé members, especially Andrés Estrades, Alejandro Fallabrino, Cecilia Lezama, Natalia Teryda, Virginia Ferrando, Noel Caraccio, Carlos Romero, Alfredo Hargain, Coco Meirana, Luciana Alonso, Virginia Borrat, Juan Manuel Cardozo, Vannessa Massimo, Tatiana Curbelo, Lucía Dominguez and Natalia Viera, for their collaboration in the study and green turtle diet analysis. The authors are really grateful to Elisa Darré who starts with green turtle feeding in her bachelor thesis and realized part of the esophagic lavage samples, Paulo Horta and Alex Garcia for algae collection in Brazil and Fabrizio Scarabino for his collaboration and his help with algae identification. We also thank the support of the Marine Zoology Unit of the Cavanilles Institute of Biodiversity and Evolutionary Biology (University of Valencia), especially to Ohiana Revuelta, Natalia Fraija and Francesc Domenech, and also thank to the Department of Animal Biology of the University of Barcelona in special to Fabiana Sapotitti, Lisette Zenteno, Irene Álvarez de Quevedo and Marcel Clusa. Authors are really grateful to all the persons and institutions that collaborated in the Uruguay marine turtle stranding network: volunteers, local fishermen, government institutions (DINARA and DINAMA), naval prefectures, lifeguard service, rangers, civil organizations (particularly SOCOBIOMA), citizens and tourist. We are really grateful to the two reviewers that help to improve the manuscript. We also acknowledge the financial support from IFAW and Rufford Small Grants to Karumbé members (ML-M and GV-R) and Agencia Nacional de Investigación e Innovación (ANII) to AC. JT is supported by projects CGL2011-30413 of the Spanish Ministry of Economy and Competitiveness and Prometeo II (2015) of the Generalitat Valenciana. This research was conducted under license (No. 200/04, 073/08 and 323/11) from the Fauna Department-Ministry of Cattle, Agriculture and Fishing of Uruguay. CITES permits for export and import of the samples were obtained.
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Vélez-Rubio, G.M., Cardona, L., López-Mendilaharsu, M. et al. Ontogenetic dietary changes of green turtles (Chelonia mydas) in the temperate southwestern Atlantic. Mar Biol 163, 57 (2016). https://doi.org/10.1007/s00227-016-2827-9
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DOI: https://doi.org/10.1007/s00227-016-2827-9