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Preferential Liver Accumulation of Mercury Explains Low Concentrations in Muscle of Caiman yacare (Alligatoridae) in Upper Amazon

Abstract

Caiman yacare is considered one of the top predators in the Amazon basin, and understanding pollutant distribution within its tissues may help its sustainable management. As a top predator, C. yacare should have the highest mercury concentrations, but has lower Hg concentrations than carnivorous fish (Rivera et al. 2016), which are part of their diet. We compared total Hg among liver, kidney, fat, and muscle of C. yacare, and whether trends in the distribution of Hg among tissues were like other crocodilians, aquatic birds, omnivorous, and carnivorous fish. Fat had the lowest concentrations (0.025 ± 0.03 mg kg−1) followed by muscle (0.15 ± 0.06 mg kg−1), kidney (0.57 ± 0.30 mg kg−1) and liver (1.81 ± 0.80 mg kg−1). Such preferential accumulation makes C. yacare meat a safer alternative for human consumption than carnivorous fish. The relation between Hg accumulation in liver and muscle is highest in crocodilians, which has evolutive and environmental implications.

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References

  1. Anan Y, Kunito T, Watanabe I, Sakai H, Tanabe S (2001) Trace element accumulation in hawksbill turtles (Eretmochelys imbricata) and green turtles (Chelonia mydas) from Yaeyama Islands, Japan. Environ Toxicol Chem 20:2802–2814

    CAS  Article  Google Scholar 

  2. Andreani G, Santoro M, Cottignoli S, Fabbri M, Carpene E, Isani G (2008) Metal distribution and metallothionein in logger head (Caretta caretta) and green (Chelonia mydas) sea turtles. Sci Total Environ 390:287–294

    CAS  Article  Google Scholar 

  3. Asociación Matusha Aidha (2016) Plan de Manejo de Lagarto (Caiman yacare) de la TCO Tacana I 2016–2018. CIPTA, WCS y MMNPT. 77

  4. Azevedo LP, dos Santos Ferraz RH, de Magalhães MRL, Oliveira AP, Cogliati B, Lemos LMS et al (2020) Healing potential of Caiman yacare (Daudin, 1802) visceral fat oil. Wound Medicine, 100195

  5. Barbieri FL, Cournil A, Gardon J (2009) Mercury exposure in a high fish eating Bolivian Amazonian population with intensesmall-scale gold-mining activities. Int J Environ Health 19:267–277

    CAS  Article  Google Scholar 

  6. Branco V, Canário J, Holmgren A, Carvalho C (2011) Inhibition of the thioredoxin system in the brain and liver of zebra-seabreams exposed to waterborne methylmercury. Toxicol Appl Pharm 25:95–103

    Article  CAS  Google Scholar 

  7. Buenfil-Rojas AM, Álvarez-Legorreta T, Cedeño-Vázquez JR (2015) Metals and metallothioneins in Morelet’s crocodile (Crocodylus moreletii) from a transboundary river between Mexico and Belize. Arch Environ Contam Toxicol 68:265–273

    CAS  Article  Google Scholar 

  8. Buenfil-Rojas AM, Alvarez-Legorreta T, Cedeño-Vázquez JR (2018) Mercury and metallothioneins in blood fractions and tissues of captive Morelet’s crocodiles in Quintana Roo, Mexico. Chemosphere 199:630–636

    CAS  Article  Google Scholar 

  9. Burger J, Gochfeld M, Rooney AA, Orlando EF, Woodward AR, Guillette LJ Jr (2000) Metals and metalloids in tissues of American alligators in three Florida lakes. Arch Environ Contam Toxicol 38:501–508

    CAS  Article  Google Scholar 

  10. CIPTA, WCS (2010) Manejo del lagarto por el pueblo Tacana, La Paz, Bolivia. 28

  11. Clarkson TW, Magos L (2006) The toxicology of mercury and its chemical compounds. Crit Rev Toxicol 36:609–662

    CAS  Article  Google Scholar 

  12. Correia J, Cesar R, Marsico E, Diniz GTN, Zorro MC, Castilhos Z (2014) Mercury contamination in alligators (Melanosuchus niger) from Mamirauá Reservoir (Brazilian Amazon) and human health risk assessment. Environ Sci Pollut Res 21:13522–13527

    CAS  Article  Google Scholar 

  13. Cosson RP (1994) Heavy metal intracellular balance and relationship with metallothionein induction in the liver of carp after contamination by silver, cadmium and mercury following or not pretreatment by zinc. Biometals 7:9–19

    CAS  Article  Google Scholar 

  14. Da Silva DS, Lucotte M, Roulet M, Poirier H, Mergler D, Santos EO, Crossa M (2005) Trophic structure and bioaccumulation of mercury in fish of three natural lakes of the Brazilian Amazon. Water Air Soil Pollut 165:77–94

    CAS  Article  Google Scholar 

  15. Duvall SE, Barron MG (2000) A screening level probabilistic risk assessment of mercury in Florida Everglades food webs. Ecotox Environ Safe 47:298–305

    CAS  Article  Google Scholar 

  16. Figueiredo SI, Araújo L, Ferraz RH, Guimarães FR, Cantarini JL, Araújo EG (2015) Bases ósseas e musculares dos cortes comerciais do tronco de jacaré-do-Pantanal (Caimanyacare Daudin, 1802). Pesqui Vet Brasil 35:749–761

    Article  Google Scholar 

  17. Grigg G, Kirshner D (2015) Biology and evolution of crocodylians. CSIRO Publishing, Clayton South (VIC)

    Book  Google Scholar 

  18. Gunderson MP, Pickett MA, Martin JT, Hulse EJ, Smith SS, Smith LA, Campbell RM, Lowers RH, Boggs A, Guillette LJ et al (2016) Variations in hepatic biomarkers in American alligators (Alligator mississippiensis) from three sites in Florida, USA . Chemosphere 155:180–187

    CAS  Article  Google Scholar 

  19. Hamer DH (1986) Metallothionein. Annu Rev Biochem 55:913–951

    CAS  Article  Google Scholar 

  20. Hosseini M, Bagher SM (2013) Bioaccumulation of trace mercury in trophic levels of benthic, benthopelagic, pelagic fish species, and sea birds from Arvand River, Iran. Biological Trace Elements Research 156:175–180

    CAS  Article  Google Scholar 

  21. IBM (2015) IBM SPSS Statistics, version 23.0. https://www.ibm.com/products/spss-statistics

  22. Jagoe CH, Arnold-Hill B, Yanochko GM, Winger PV, Brisbin IL Jr (1998) Mercury in alligators (Alligator mississippiensis) in the southeastern United States. Sci Total Environ 213:255–262

    CAS  Article  Google Scholar 

  23. Kasper D, Forsberg BR, do Amaral Kehrig H et al (2018) Mercury in Black-Waters of the Amazon. In: Myster RW (ed) Igapó (Black-water flooded forests) of the Amazon basin. Springer, Cham, pp 39–56

    Chapter  Google Scholar 

  24. Kaoud HA, El-Dahshan AR (2010) Bioaccumulation and histopathological alterations of the heavy metals in Oreochromis niloticus fish. Nat Sci 8:147–156

    Google Scholar 

  25. Khan B, Tansel B (2000) Mercury bioconcentration factors in American alligators (Alligator mississippiensis) in the Florida everglades. Ecotoxicol Environ Safety 47:54–58

    CAS  Article  Google Scholar 

  26. Lawson AJ, Moore CT, Rainwater TR, Nilsen FM, Wilkinson PM, Lowers RH, Guillete LJ, McFadden KW, Jodice PG (2020) Nonlinear patterns in mercury bioaccumulation in American alligators are a function of predicted age. Sci Total Environ 707:135103

    CAS  Article  Google Scholar 

  27. Lázaro WI, de Oliveira RF, dos Santos-Filho M, da Silva CJ, Malm O, Ignacio AR, Diéz S (2015) Non-lethal sampling for mercury evaluation in crocodilians. Chemosphere 138:25–32

    Article  CAS  Google Scholar 

  28. Lucia M, André JM, Gontier K, Diot N, Veiga J, Davail S (2010) Trace element concentrations (mercury, cadmium, copper, zinc, lead, aluminium, nickel, arsenic, and selenium) in some aquatic birds of the Southwest Atlantic Coast of France. Arch Environ Contam Toxicol 58:844–853

    CAS  Article  Google Scholar 

  29. Magarelli G, Fostier AH (2005) Influence of deforestation on the mercury air/soil exchange in the Negro River Basin, Amazon. Atmos Environ 39:7518–7528

    CAS  Article  Google Scholar 

  30. Magos L, Brown AW, Sparrow S, Bailey E, Snowden RT, Skipp WR (1985) The comparative toxicology of ethyl- and methylmercury. Arch Toxicol 57:260–267

    CAS  Article  Google Scholar 

  31. Maurice-Bourgoin L, Quiroga I, Chincheros J, Courau P (2000) Mercury distribution in water and fishes of the upper Madeira rivers and mercury exposure in riparian Amazonian populations. Sci Total Environ 260:73–86

    CAS  Article  Google Scholar 

  32. Mieiro CL, Bervoets L, Joosen S, Blust R, Duarte AC, Pereira ME, Pacheco M (2011) Metallothioneins failed to reflect mercury external levels of exposure and bioaccumulation in marine fish considerations on tissue and species specific responses. Chemosphere 85:114–121

    CAS  Article  Google Scholar 

  33. MMAyA (2009) Estrategia para la Reconducción del Programa Nacional de Conservación y Aprovechamiento Sostenible del Lagarto. Viceministerio de Medio Ambiente, Biodiversidad y Cambios Climáticos – Dirección General de Biodiversidad y Áreas Protegidas. MMAyA, La Paz

    Google Scholar 

  34. Molina CI, Gibon FM, Duprey JL, Dominguez E, Guimarães JRD, Roulet M (2010) Transfer of mercury and methylmercury along macroinvertebrate food chains in a floodplain lake of the Beni River, Bolivian Amazonia. Sci Total Environ 408:3382–3391

    CAS  Article  Google Scholar 

  35. Nevado JB, Martín-Doimeadios RR, Bernardo FG, Moreno MJ, Herculano AM, Do Nascimento JLM, Crespo-López ME (2010) Mercury in the Tapajós River basin, Brazilian Amazon: a review. Environ Int 36:593–608

    Article  CAS  Google Scholar 

  36. Nordberg M, Nordberg G (2009) Metallothioneins: historical development and overview. Metal ions in life sciences. R Soc Chem Cambridge 5:1–29

    CAS  Google Scholar 

  37. Norris DO (1997) Vertebrate endocrinology. Academic Press, San Diego

    Google Scholar 

  38. Orr SE, Bridges CC (2017) Chronic kidney disease and exposure to nephrotoxic metals. Int J Mol Sci 18:1039

    Article  CAS  Google Scholar 

  39. Piotrowski JK, Trojanowska B, Wiśniewska-Knypl JM, Bolanowska W (1974) Mercury binding in the kidney and liver of rats repeatedly exposed to mercuric chloride: induction of metallothionein by mercury and cadmium. Toxicol Appl Pharmacol 27:11–19

    CAS  Article  Google Scholar 

  40. Pouilly M, Yunoki T, Rosales C, Torres L (2004) Trophic structure of fish assemblages from Mamoré River floodplain lakes (Bolivia). Ecol Freshw Fish 13:245–257

    Article  Google Scholar 

  41. Pouilly M, Rejas D, Pérez T, Duprey JL, Molina CI, Húbas C, Guimarães JRD (2013) Trophic structure and mercury biomagnification in tropical fish assemblages. PLoS ONE 8 – 5, Iténez River

    Google Scholar 

  42. Rivera SJ, Pacheco LF, Achá D, Molina CI, Miranda-Chumacero G (2016) Low total mercury in Caiman yacare (Alligatoridae) as compared to carnivorous, and non-carnivorous fish consumed by Amazonian indigenous communities. Environ Pollut 218:366–371

    CAS  Article  Google Scholar 

  43. Rumbold DG, Fink LE, Laine KA, Niemczyk SL, Chandrasekhar T, Wankel SD, Kendall C (2002) Levels of mercury in alligators (Alligator mississippiensis) collected along a transect through the Florida Everglades. Sci Total Environ 297:239–252

    CAS  Article  Google Scholar 

  44. Sakai H, Saeki K, Ichihashi H, Kamezaki N, Tanabe S, Tatsukawa R (2000) Growth-related changes in heavy metal accumulation in green turtle (Chelonia mydas) from Yaeyama Islands, Okinawa, Japan. Arch Environ Contam Toxicol 39:378–385

    CAS  Article  Google Scholar 

  45. Santos SA, Nogueira MS, Pinheiro MS, Campos Z, Magnusson WE, Mourao GDM (1996) Diets of Caiman crocodilus yacare from different hábitats in the Brazilian Pantanal. J Herpetol 6:111–118

    Google Scholar 

  46. Schneider L, Belgerb L, Burgerc J, Vogta RC (2009) Mercury bioacumulation in four tissues of Podocnemis erythrocephala (Podocnemididae: Testudines) as a function of water parameters. Sci Total Environ 407:1048–1054

    CAS  Article  Google Scholar 

  47. Scheneider L, Pacheco R, Kluczkoviski A Jr, Martinez G, Marioni B, Carl Vogt R, Da Silveira R (2012) Mercury concentration in the spectacled Caiman and Black Caiman (Alligatoridae) of the Amazon: implications for human health. Arch Environ Con Tox 63:270–279

    Article  CAS  Google Scholar 

  48. Schneider L, Eggins S, Maher W, Vogt RC, Krikowa F, Kinsley L, Eggins SM, Da Silveira R (2015) An evaluation of the use of reptile dermal scutes as a non-invasive method to monitor mercury concentrations in the environment. Chemosphere 119:162–170

    Google Scholar 

  49. Sergio F, Schmitz OJ, Krebs CJ, Holts RD, Wirsing MR, Ripple WJ, Ritchie E, Ainley D, Oro D, Jhala Y, Hiraldo F, Korpimäki E (2014) Towards a cohesive, holistic view of top predation: a definition, synthesis and perspective. Oikos 123:1234–1243

    Article  Google Scholar 

  50. Smith PN, Cobb GP, Godard-Codding C, Hoff D, McMurry ST, Rainwater TR (2007) Contaminant exposure in terrestrial vertebrates. Environ Pollut 150:41–64

    CAS  Article  Google Scholar 

  51. Souza-Araujo J, Giarrizo T, Lima MO (2015) Mercury concentration in different tissues of Podocnemis unifilis (Troschel, 1848) (Podocnemididae: Testudines) from the lower Xingu River—Amazonian, Brazil. Braz J Biol 75:106–111

    CAS  Article  Google Scholar 

  52. Thomas P, Baer KN, White RB (1994) Isolation and partial characterization of metallothionein in the liver of the red-eared turtle (Trachemys scripta) following intreperitoneal administration of cadmium. Comp Biochem Physiol C 107:221–226

    Article  Google Scholar 

  53. Trinchella F, Riggio M, Filosa S, Parisi E, Scudiero R (2008) Molecular cloning and sequencing of metallothionein in squamates: new insights into the evolution of the metallothionein genes in vertebrates. Gene 423:48–56

    CAS  Article  Google Scholar 

  54. Vasak M (2005) Advances in metallothionein structure and functions. J Trace Elem Med Biol 19:13–17

    CAS  Article  Google Scholar 

  55. Veiga MM, Hinton JJ (2002) Abandoned artisanal gold mines in the Brazilian Amazon: a legacy of mercury pollution. Nat Resour Forum 26:15–26

    Article  Google Scholar 

  56. Vieira LM, Nunes VDS, Amaral MDA, Oliveira AC, Hauser-Davis RA, Campos RC (2011) Mercury and methylmercury ratios in Caiman (Caiman cocodrilus yacare) from the Pantanal area. Brazil J Environ Monitor 13:280–287

    CAS  Article  Google Scholar 

  57. Vieira M, Bernardi JV, Dórea JG, Rocha BC, Ribeiro R, Zara LF (2018) Distribution and availability of mercury and methylmercury in different waters from the Rio Madeira Basin, Amazon. Environ Pollut 235:771–779

    CAS  Article  Google Scholar 

  58. WHO (World Health Organization) (1991) Inorganic mercury. World Health Organization International Programme on Chemical Safety. WHO, Geneva, p 168

    Google Scholar 

  59. Yanochko GM, Jagoe CH, Brisbin IL Jr. (1997) Tissue mercury concentrations in alligators (Alligator mississippiensis) from the Florida Everglades and the Savannah River Site, South Carolina. Arch Environ Contamin Toxicol 32:323–328

    CAS  Article  Google Scholar 

  60. Zalups RK, Diamond GL (1987) Mercuric chloride-induced nephrotoxicity in the rat following unilateral nephrectomy and compensatory renal growth. Virchows Archiv B 53:336

    CAS  Article  Google Scholar 

  61. Zalups RK (2000) Molecular interactions with mercury in the kidney. Pharmacol Rev 52:113–144

    CAS  Google Scholar 

  62. Zalups RK, Koropatnick J (2000) Temporal changes in metallothionein gene transcription in rat kidney and liver: relationship to content of mercury and metallothionein protein. J Pharmacol Exp Ther 295:74–82

    CAS  Google Scholar 

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Acknowledgements

This work was supported by the Unidad de Calidad Ambiental (P.I.; D. Achá) of the Instituto de Ecología, Universidad Mayor de San Andrés (UMSA) and the Master program in Biology of the same University. This work was performed within the young research associate team “JEAI TITICACA” (P.I.; D. Achá) supported by the French Institute National Research for Sustainable Development (IRD). Field sampling was possible thanks to the funding and continues support of the Wildlife Conservation Society (WCS). We extend our particular thanks to Consejo Indígena del Pueblo Tacana (CIPTA) and Matusha Aidha Association of Caiman managers in Cachichira community. We would also like to thanks Gustavo Álvarez and José Luis Mollericona for their help during sampling.

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Salazar-Pammo, A.C., Achá, D. & Miranda-Chumacero, G. Preferential Liver Accumulation of Mercury Explains Low Concentrations in Muscle of Caiman yacare (Alligatoridae) in Upper Amazon. Bull Environ Contam Toxicol 106, 264–269 (2021). https://doi.org/10.1007/s00128-020-03081-8

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Keywords

  • Crocodilian
  • Mercury decontamination
  • Sustainable management
  • Mercury in kidney