Abstract
The green turtle (Chelonia mydas) is known to present an herbivorous diet as an adult; however, juveniles may have an omnivore habit, and these changes in food preference may affect the uptake and accumulation of pollutants, such as mercury (Hg). In order to better understand the influence of this ontogenetic shift on Hg accumulation, this study evaluates the concentrations of total mercury (THg), methyl mercury (MeHg), and stable isotopes of carbon and nitrogen (δ13C and δ15N) in a group of juveniles of the green turtle. Tissue samples (liver, kidney, muscle, and scutes) were sampled from 47 turtles stranded dead on the coast of Bahia, NE, Brazil, between 2009 and 2013. The turtles analyzed showed a size range of 24.9–62.0 cm and an average of 36.4 ± 7.2 cm of curved carapace length. The scutes showed to be a viable method for Hg monitoring in the green turtles. The concentrations of THg and MeHg decreased with increasing size. The isotope values of δ15N and δ13C did not show a clear relationship with the size, suggesting that the green turtles used in our work would be occupying similar trophic levels, and foraging habitat.
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References
Aguirre AA, Lutz PL (2004) Marine turtles as sentinels of ecosystem health: is fibropapillomatosis an indicator? EcoHealth 1(3):275–283. https://doi.org/10.1007/s10393-004-0097-3
Almeida AP, Moreira LMP, Bruno SC, Thomé 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. https://doi.org/10.3354/esr00357
Arthur KE, Boyle MC, Limpus CJ (2008) Ontogenetic changes in diet and habitat use in green sea turtle (Chelonia mydas) life history. https://doi.org/10.3354/meps07440
Barbieri E (2009) Concentration of heavy metals in tissues of green turtles (Chelonia mydas) sampled in the Cananéia estuary, Brazil. Braz J Oceanogr 57(3):243–248. https://doi.org/10.1590/S1679-87592009000300007
Beckers F, Rinklebe J (2017) Cycling of mercury in the environment: sources, fate, and human health implications: a review. Crit Rev Environ Sci Technol 47:693–794. https://doi.org/10.1080/10643389.2017.1326277
Bezerra MF, Lacerda LD, Costa BGB, Lima EHSM (2012) Mercury in the sea turtle Chelonia mydas (Linnaeus, 1958) from Céara coast, NE Brazil. An Acad Bras Cienc 84:123–128
Bezerra MF, Lacerda LD, Lima EHSM, Melo MTD (2013) Monitoring mercury in green sea turtles using keratinized carapace fragments (scutes). Mar Pollut Bull 77:424–427. https://doi.org/10.1016/j.marpolbul.2013.09.020
Bezerra MF, Lacerda LD, Rezende CE, Franco ML, Almeida MG, Macêdo GR, Pires TT, Rostán G, Lopez GG (2015) Food preferences and Hg distribution in Chelonia mydas assessed by stable isotopes. Environ Pollut 206:236–246. https://doi.org/10.1016/j.envpol.2015.07.011
Bolten A (2003) Variation in sea turtle life history patterns: neritic vs. oceanic developmental stages. Biol. Sea turtles 2:243–257. https://doi.org/10.1201/9781420040807.ch9
Burgett CM, Burkholder DA, Coates KA, Fourqurean VL, Kenworthy WJ, Manuel SA, Outerbridge ME, Fourqurean JW (2018) Ontogenetic diet shifts of green sea turtles (Chelonia mydas) in a mid-ocean developmental habitat. Mar Biol 165:1–12. https://doi.org/10.1007/s00227-018-3290-6
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. https://doi.org/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 BioEcol 393:83–89. https://doi.org/10.1016/j.jembe.2010.07.004
Chételat J, Ackerman JT, Eagles-Smith CA, Hebert CE (2020) Methylmercury exposure in wildlife: a review of the ecological and physiological processes affecting contaminant concentrations and their interpretation. Sci Total Environ 135117. https://doi.org/10.1016/j.scitotenv.2019.135117
De Macedo GR, Tarantino TB, Barbosa IS, Pires TT, Rostan G, Goldberg DW, Pinto LFB, Korn MGA, Franke CR (2015) Trace elements distribution in hawksbill turtle (Eretmochelys imbricata) and green turtle (Chelonia mydas) tissues on the northern coast of Bahia. Brazil Mar Pollut Bull 94:284–289. https://doi.org/10.1016/j.marpolbul.2015.02.033
Di Beneditto APMD, Bittar VT, Rezende CED, Camargo PB, Kehrig HA (2013) Mercury and stable isotopes (δ15N and δ13C) as tracers during the ontogeny of Trichiurus lepturus. Neotropical Ichthyology 11(1):211–216. https://doi.org/10.1590/S1679-62252013000100024
Di Beneditto APM, Siciliano S, Monteiro LR (2017) Herbivory level and niche breadth of juvenile green turtles (Chelonia mydas) in a tropical coastal area: insights from stable isotopes. Mar Biol 164:1–12. https://doi.org/10.1007/s00227-016-3044-2
Driscoll CT, Mason RP, Chan HM, Jacob DJ, Pirrone N (2013) Mercury as a global pollutant: sources, pathways, and effects. Environ Sci Technol 47:4967–4983. https://doi.org/10.1021/es305071v
González 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. Bio. Ecol. 429:64–72. https://doi.org/10.1016/j.jembe.2012.06.007
Gray JS (2002) Biomagnification in marine systems: the perspective of an ecologist. Mar Pollut Bull 45:46–52. https://doi.org/10.1016/S0025-326X(01)00323-X
Hamann M, Godfrey MH, Seminoff JA, Arthur K, Barata PCR, Bjorndal KA, Casale P (2010) Global research priorities for sea turtles: informing management and conservation in the 21st century. Endanger Species Res 11(3):245–269. https://doi.org/10.3354/esr00279
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(1):52–64. https://doi.org/10.1007/s00442-006-0431-2
Haywood J, Fuller W, Godley B, Shutler J, Widdicombe S, Broderick A (2019) Global review and inventory: how stable isotopes are helping us understand ecology and inform conservation of marine turtles. Mar Ecol Prog Ser 613:217–245. https://doi.org/10.3354/meps12889
Jakimska A, Konieczka P, Skóra K, Namieśnik J (2011) Bioaccumulation of metals in tissues of marine animals, part II: metal concentrations in animal tissues. Polish J Environ Stud 20:1127–1146
Jardim A, López-Mendilaharsu M, Barros F (2016) Demography and foraging ecology of Chelonia mydas on tropical shallow reefs in Bahia, Brazil. J Mar Biol Assoc U K 96(6):1295–1304. https://doi.org/10.1017/S0025315415001629
Jensen MP, Bell I, Limpus CJ, Hamann M, Ambar S, Whap T, FitzSimmons NN (2016) Spatial and temporal genetic variation among size classes of green turtles (Chelonia mydas) provides information on oceanic dispersal and population dynamics. Mar Ecol Prog Ser 543:241–256. https://doi.org/10.3354/meps11521
Kampalath R, Gardner SC, Méndez-Rodríguez L, Jay JA (2006) Total and methylmercury in three species of sea turtles of Baja California Sur. Mar Pollut Bull 52(12):1816–1823. https://doi.org/10.1016/j.marpolbul.2006.09.019
Komoroske LM, Lewison RL, Seminoff JA, Deheyn DD, Dutton PH (2011) Pollutants and the health of green sea turtle’s resident to an urbanized estuary in San Diego, CA. Chemosphere 84:544–552. https://doi.org/10.1016/j.chemosphere.2011.04.023
Lam JCW, Tanabe S, Chan SKF, Lam MHW, Martin M, Lam PKS (2006) Levels of trace elements in green turtle eggs collected from Hong Kong: evidence of risks due to selenium and nickel. Environ Pollut 144:790–801. https://doi.org/10.1016/j.envpol.2006.02.016
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 Bio Ecol 405:25–32. https://doi.org/10.1016/j.jembe.2011.05.012
Lescord GL, Johnston TA, Branfireun BA, Gunn JM (2018) Percentage of methylmercury in the muscle tissue of freshwater fish varies with body size and age and among species. Environ Toxicol Chem 37(10):2682–2691. https://doi.org/10.1002/etc.4233
Mackay D, Fraser A (2000) Bioaccumulation of persistent organic chemicals: mechanisms and models 110, 375–391. https://doi.org/10.1016/S0269-7491(00)00162-7
Marins RV, de Paula Filho FJ, Maia SRR, de Lacerda LD, Marques WS (2004) Distribuição de mercúrio total como indicador de poluição urbana e industrial na costa brasileira. Química Nova 27:763–770. https://doi.org/10.1590/S0100-40422004000500016
May K, Stoeppler M, Reisinger K (1987) Studies in the ratio total mercury/methylmercury in the aquatic food chain. Toxicol Environ Chem 13:153–159. https://doi.org/10.1080/02772248709357178
Miguel C, de Deus Santos MR (2019). Ecotoxicological studies of metal pollution in sea turtles of Latin America. In Pollution of water bodies in Latin America (pp. 129–156). Springer, Cham. https://doi.org/10.1007/978-3-030-27296-8_9
Monzón-Argüello C, Cardona L, Calabuig P, Camacho M, Crespo-Picazo JL, García-Párraga D, Mayans S, Luzardo OP, Orós J, Varo-Cruz N (2018) Supplemental feeding and other anthropogenic threats to green turtles (Chelonia mydas) in the Canary Islands. Sci Total Environ 621:1000–1011. https://doi.org/10.1016/j.scitotenv.2017.10.126
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 Conservation and Biology 13(2):260–266. https://doi.org/10.2744/CCB-1058.1
Nagaoka SM, Martins AS, Dos Santos RG, Tognella MMP, de Oliveira Filho EC, Seminoff JA (2012) Diet of juvenile green turtles (Chelonia mydas) associating with artisanal fishing traps in a subtropical estuary in Brazil. Mar Biol 159(3):573–581. https://doi.org/10.1007/s00227-011-1836-y
Ng CKY, Lam JCW, Zhang XH, Gu HX, Li TH, Ye M, Bin Xia ZR, Zhang FY, Duan JX, Wang WX, Lam IKS, Balazs GH, Lam PKS, Murphy MB (2018) Levels of trace elements, methylmercury and polybrominateddiphenyl ethers in foraging green turtles in the South China region and their conservation implications. Environ Pollut 234:735–742. https://doi.org/10.1016/j.envpol.2017.11.100
Nica A, Popescu A, Ibănescu DC (2017) A current problem: mercury pollution. Current Trends in Natural Sciences 6(12):165–169
Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18(1):293–320. https://doi.org/10.1146/annurev.ecolsys.18.1.293
Rodriguez CAB, Bezerra MF, Rezende CE, Bastos WR, Lacerda LD (2019) Mercury and methylmercury in carapace of the marine turtle Caretta caretta, in northeastern Brazil and its potential for environmental monitoring. An Acad Bras Cienc 91(2):e20180672. Epub July 10, 2019. https://doi.org/10.1590/0001-3765201920180672
Sakai H, Saeki K, Ichihashi H, Kamezaki N, Tanabe S, Tatsukawa R (2000a) Growth-related changes in heavy metal accumulation in green turtle (Chelonia mydas) from Yaeyama Islands, Okinawa, Japan. Arch Environ Contam Toxicol 39:378–385. https://doi.org/10.1007/s002440010118
Sakai H, Saeki K, Ichihashi H, Suganuma H, Tanabe S, Tatsukawa R (2000b) Species-specific distribution of heavy metals in tissues and organs of loggerhead turtle (Caretta caretta) and green turtle (Chelonia mydas) from Japanese coastal waters. Mar Pollut Bull 40:701–709. https://doi.org/10.1016/S0025-326X(00)00008-4
Schneider L, Maher W, Green A, Vogt RC (2013) Mercury contamination in reptiles: an emerging problem with consequences for wildlife and human health. Mercury: Sources, Applications and Health Impacts. Nova Science Publishers, Inc., Hauppauge, New York, USA, 173–232
Storelli MM, Ceci E, Marcotrigiano GO (1998) Distribution of heavy metal residues in some tissues of Caretta caretta ({ILinnaeus}) specimen beached along the Adriatic Sea (Italy). Bull Environ Contam Toxicol 60:546–552. https://doi.org/10.1007/s001289900660
Taylor VF, Carter A, Davies C, Jackson BP (2011) Trace-level automated mercury speciation analysis. Anal Methods 3(5):1143–1148. https://doi.org/10.1039/C0AY00528B
Unep (2013) Global mercury assessment 2013: sources, emissions, releases, and environmental transport. Unep 42. https://doi.org/DTI/1636/GE
Van de Merwe JP, Hodge M, Olszowy HA, Whittier JM, Lee SY (2010) Using blood samples to estimate persistent organic pollutants and metals in green sea turtles (Chelonia mydas). Mar Pollut Bull 60:579–588. https://doi.org/10.1016/j.marpolbul.2009.11.006
Vander Zanden HB, Bjorndal KA, Bolten AB (2013) Temporal consistency and individual specialization in resource use by green turtles in successive life stages. Oecologia 173:767–777. https://doi.org/10.1007/s00442-013-2655-2
Vander Zanden HB, Tucker AD, Bolten AB, Reich KJ, Bjorndal KA (2014) Stable isotopic comparison between loggerhead sea turtle tissues. Rapid Commun Mass Spectrom 28:2059e2064. https://doi.org/10.1002/rcm.6995
Vander Zanden MJ, Clayton MK, Moody EK, Solomon CT, Weidel BC (2015) Stable isotope turnover and half-life in animal tissues: a literature synthesis. PLoS One 10(1). https://doi.org/10.1371/journal.pone.0116182
Vélez-Rubio GM, Cardona L, Mendilaharsu LCML, Souza GM, Carranza A, González-Paredes D, Tomás J (2016) Ontogenetic dietary changes of green turtles (Chelonia mydas) in the temperate southwestern Atlantic. Mar Biol 163:1–16. https://doi.org/10.1007/s00227-016-2827-9
Acknowledgments
The author would like to thank the team of the Coastal Biogeochemistry Laboratory for the support in processing and analysis of samples, and to the team of the Marine Turtle Conservation Project (TAMAR Project) for the support in the field work.
Funding
This study was funded by Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP) and Conselho Nacional de Desenvolvimento Científico e Tecnológico CNPq (Proc. No. 405.244/2018-5).
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Rodriguez, C.A.B., de Lacerda, L.D., Bezerra, M.F. et al. Influence of size on total mercury (THg), methyl mercury (MeHg), and stable isotopes of N and C in green turtles (Chelonia mydas) from NE Brazil. Environ Sci Pollut Res 27, 20527–20537 (2020). https://doi.org/10.1007/s11356-020-08623-5
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DOI: https://doi.org/10.1007/s11356-020-08623-5