Resumen
Introducción: Los pequeños cetáceos son buenos bioindicadores de la contaminación ambiental; sin embargo, el conocimiento acerca de su estado ecotoxicológico en Centroamérica es escaso. En Panamá, el acceso a muestras para determinar el estado ecotoxicológico de delfines oceánicos es limitado; por lo tanto, los varamientos proveen una alternativa para obtener muestras. En abril de 2016, un raro evento de varamiento masivo ocurrió en la Península de Azuero (Pacífico panameño), en el cual 60 delfines de dientes rugosos (Steno bredanensis) vararon incluyendo diez que murieron en la playa.
Objetivo: Determinar los niveles de mercurio total (THg), e isótopos estables de δ13C y δ15N en los delfines de dientes rugosos por primera vez en la región.
Métodos: Nueve muestras de piel de adultos fueron colectadas, almacenadas en etanol al 70 %, y analizadas posteriormente para determinar THg e isótopos estables.
Resultados: Las concentraciones de THg variaron entre 4 764 y 18 689 ng g-1 de peso seco (dw) (promedio= 12 841; DE= 5 083 ng g-1 dw), los valores de δ13C entre −16.8 y −15.2 ‰ (promedio= −16.2; DE= 0.6 ‰), y los de δ15N entre 14.3 y 15.9 ‰ (promedio= 15.0; DE= 0.5 ‰).
Conclusiones: Los altos niveles de THg reportados para esta especie en la Península de Azuero son consistentes con los reportados en la piel de los delfines de dientes rugosos en otras áreas del mundo, como en el estado de Río de Janeiro en Brasil y La Guajira en el Caribe colombiano. Las altas concentraciones de mercurio (Hg) pueden estar relacionadas con la dieta de los delfines de dientes rugosos, la cual, de acuerdo a los valores de δ15N encontrados aquí, parece estar basada en presas de alto nivel trófico que acumulan más Hg en sus tejidos. Sin embargo, estudios dietarios adicionales son requeridos para confirmar estos resultados. Un monitoreo continuo de la dieta usando análisis tradicionales, así como de los niveles de contaminación en peces y delfines, es necesario para entender la ecotoxicología de los delfines en Panamá.
Citas
Alcala-Orozco, M., Caballero-Gallardo, K., & Olivero-Verbel, J. (2019). Mercury exposure assessment in indigenous communities from Tarapaca village, Cotuhe and Putumayo Rivers, Colombian Amazon. Environmental Science Pollution Research, 26, 36458–36467. https://doi.org/10.1007/s11356-019-06620-x
Aubail, A., Méndez-Fernandez, P., Bustamante, P., Churlaud, C., Ferreira, M., Vingada, J. V., & Caurant, F. (2013). Use of skin and blubber tissues of small cetaceans to assess the trace element content of internal organs. Marine Pollution Bulletin, 76(1–2), 158–169; https://doi.org/10.1016/j.marpolbul.2013.09.008
Avila, I. C., Kaschner, K., & Dormann, C. F. (2018). Current global risks to marine mammals: Taking stock of the threats. Biological Conservation, 221, 44–58. https://doi.org/10.1016/j.biocon.2018.02.021
Baird, R. W. (2016). The Lives of Hawai’i’s Dolphins and Whales. University of Hawai’i Press.
Baptista, G., Kehrig, H. A., Di Beneditto, A. P. M., Hauser-Davis, R. A., Almeida, M. G., Rezende, C. E., Siciliano, S., de Moura, J. F., & Moreira, I. (2016). Mercury, selenium and stable isotopes in four small cetaceans from the Southeastern Brazilian coast: Influence of feeding strategy. Environmental Pollution, 218, 1298–1307. https://doi.org/10.1016/j.envpol.2016.08.088
Barragán-Barrera, D. C., Luna-Acosta, A., May-Collado, L. J., Polo-Silva, C., Riet-Sapriza, F. G., Bustamante, P., Hernández-Ávila, M. P., Vélez, N., Farías-Curtidor, N., & Caballero, S. (2019). Foraging habits and levels of mercury in a resident population of bottlenose dolphins (Tursiops truncatus) in Bocas del Toro Archipelago, Caribbean Sea, Panama. Marine Pollution Bulletin, 145, 343–356. https://doi.org/10.1016/j.marpolbul.2019.04.076
Barragán-Barrera, D. C., Farías-Curtidor, N., Luna-Acosta, A., Bustamante, P., Ayala, R., & Caballero, S. (2019, September 15-18). Evidence of mercury bioaccumulation in skin samples of wild delphinids in La Guajira, Colombian Caribbean [Paper presentation]. SETAC Latin America 13th Biennial Meeting, Cartagena, Colombia.
Barragán-Barrera, D. C., Farías-Curtidor, N., Chávez-Carreño, P. A., Mesa-Gutiérrez, R. A., Duarte, A., Correa-Cárdenas, C. A., Polo-Silva, C. J., Riet-Sapriza, F., Luna-Acosta, A., Bustamante, P., Jiménez-Pinedo, C., Ayala-Mendoza, R., & Caballero, S. (2019, October 22-25). Estado genético y ecotoxicológico de cuatro especies de delfines en La Guajira, Caribe colombiano [Paper presentation]. XVIII Seminario Nacional de Ciencias y Tecnologías del Mar SENALMAR, Barranquilla, Colombia.
Béland, P., DeGuise, S., Girard, C., Lagacé, A., Martineau, D., Michaud, R., Muir, D. C. G., Norstrom, R. J., Pelletier, É., Ray, S., & Shugart, L. R. (1993). Toxic Compounds and Health and Reproductive Effects in St. Lawrence Beluga Whales. Journal of Great Lakes Research, 19(4), 766–775. https://doi.org/10.1016/S0380-1330(93)71264-2
Bosch, A., O’Neill, B., Sigge, G., Kerwath, S., Hoffman, L. (2016). Mercury accumulation in Yellowfin tuna (Thunnus albacares) with regards to muscle type, muscle position and fish size. Food Chemistry, 190, 351–356. https://doi.org/10.1016/j.foodchem.2015.05.109
Bossart, G. D. (2011). Marine mammals as sentinel species for oceans and human health. Veterinary Pathology, 48(3), 676–690. https://doi.org/10.1177/0300985810388525
Cáceres-Saez, I., Goodall, R. N. P., Dellabianca, N. A., Cappozzo, H. L., & Ribeiro Guevara, S. (2015). The skin of Commerson’s dolphins (Cephalorhynchus commersonii) as a biomonitor of mercury and selenium in Subantarctic waters. Chemosphere, 138, 735–743. https://doi.org/10.1016/j.chemosphere.2015.07.026
Correa, L., Rea, L. D., Bentzen, R., & O’Hara, T. M. (2014). Assessment of mercury and selenium tissular concentrations and total mercury body burden in 6 Steller sea lion pups from the Aleutian Islands. Marine Pollution Bulletin, 82(1–2), 175–182. https://doi.org/10.1016/j.marpolbul.2014.02.022
DeNiro, M. J., & Epstein, S. (1978). Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta, 42(5), 495–506. https://doi.org/10.1016/0016-7037(78)90199-0
Desforges, J-P. W., Sonne, C., Levin, M., Siebert, U., De Guise, S., & Dietz, R. (2016). Immunotoxic effects of environmental pollutants in marine mammals. Environmental International, 86, 126–139. https://doi.org/10.1016/j.envint.2015.10.007
Elliott, J. E., Kirk, D. A., Elliott, K. H., Dorzinsky, J., Lee, S., Ruelas Inzunza, E., Cheng, K. M. T., Scheuhammer, T., & Shaw, P. (2015). Mercury in forage fish from Mexico and Central America: implications for fish-eating birds. Archives of Environmental Contamination and Toxicology, 69, 375–389. https://doi.org/10.1007/s00244-015-0188-x
Elorriaga-Verplancken, F. R., Paniagua-Mendoza, A., Blanco-Jarvio, A., Carone, E., Robles-Hernández, R., Ballínez-Ambriz, C., & Rosales-Nanduca, H. (2020). Stable isotope assessment of a mass stranding of short-beaked common dolphins (Delphinus delphis delphis) reveals their provenance: Integrating knowledge of a little-known odontocete in the Gulf of California. Regional Studies in Marine Science, 40, 101503. https://doi.org/10.1016/j.rsma.2020.101503
Espinoza, M., Munroe, S. E. M., Clarke, T. M., Fisk, A. T., & Wehrtmann, I. S. (2015). Feeding ecology of common demersal elasmobranch species in the Pacific coast of Costa Rica inferred from stable isotope and stomach content analyses. Journal of Experimental Marine Biology and Ecology, 470, 12–25. https://doi.org/10.1016/j.jembe.2015.04.021
Farías-Curtidor, N., & Barragán-Barrera, D. C. (2017, October 22-27). Occurrence of odontocetes in La Guajira (Northern portion of the Colombian Caribbean)[Paper presentation]. The 22nd Biennial Conference on The Biology of Marine Mammals, Halifax, Nova Scotia, Canada.
Farías-Curtidor, N., & Barragán-Barrera, D. C. (2019, October 22-25). Ocurrencia de pequeños cetáceos en La Guajira (Caribe colombiano)[Paper presentation]. XVIII Seminario Nacional de Ciencias y Tecnologías del Mar SENALMAR, Barranquilla, Colombia
Fontaine, M., Carravieri, A., Simon-Bouhet, B., Bustamante, P., Gasco, N., Bailleul, F., Guinet, C., & Cherel, Y. (2015). Ecological tracers and at-sea observations document the foraging ecology of southern long-finned pilot whales (Globicephala melas edwardii) in Kerguelen waters. Marine Biology, 162, 207–219. https://doi.org/10.1007/s00227-014-2587-3
Geraci, J., & Lounsbury, V. (1993). Marine Mammals Ashore: A Field Guide for Strandings. Texas A&M University Sea Grant College Program.
Hidalgo-Reza, M., Elorriaga-Verplancken, F. R., Aguíñiga-García, S., & Urbán R, J. (2019). Impact of freezing and ethanol preservation techniques on the stable isotope analysis of humpback whale (Megaptera novaeangliae) skin. Rapid Communication in Mass Spectometry, 33(8), 789–794. https://doi.org/10.1002/rcm.8392
Jefferson, T. A. (2018). Rough-toothed dolphin Steno bredanensis. In B. Würsig, J. G. M. Thewissen & K. Kovacs (Eds.), Encyclopedia of Marine Mammals, (3rd ed., pp. 838–840). Academic Press. https://doi.org/10.1016/B978-0-12-804327-1.00223-5
Kershaw, J. L., & Hall, A. J. (2019). Mercury in cetaceans: Exposure, bioaccumulation and toxicity. Science of The Total Environment, 694, 133683. https://doi.org/10.1016/j.scitotenv.2019.133683
Kiszka, J., Oremus, M., Richard, P., Poole, M., & Ridoux, V. (2010). The use of stable isotope analyses from skin biopsy samples to assess trophic relationships of sympatric delphinids off Moorea (French Polynesia). Ecology, 395(1–2), 48–54. https://doi.org/10.1016/j.jembe.2010.08.010
Kiszka, J., Lesage, V., & Ridoux, V. (2014). Effect of ethanol preservation on stable carbon and nitrogen isotope values in cetacean epidermis: Implication for using archived biopsy samples. Marine Mammal Science, 30(2), 788–795. https://doi.org/10.1111/mms.12058
Kiszka, J., Baird, R., & Braulik, G. (2019). Steno bredanensis (errata version published in 2020)[e.T20738A178929751]. The IUCN Red List of Threatened Species,. https://dx.doi.org/10.2305/IUCN.UK.2019-2.RLTS.T20738A178929751.en
Krey, A., Ostertag, S. K., & Chan, H. M. (2015). Assessment of neurotoxic effects of mercury in beluga whales (Delphinapterus leucas), ringed seals (Pusa hispida), and polar bears (Ursus maritimus) from the Canadian Arctic. Science of The Total Environment, 509–510, 237–247. https://doi.org/10.1016/j.scitotenv.2014.05.134
Kuczaj II, S. A., & Yeater, D. (2007). Observations of rough-toothed dolphins (Steno bredanensis) off the coast of Utila, Honduras. Journal of the Marine Biological Association of the United Kingdom, 87(1), 141–148. https://doi.org/10.1017/S0025315407054999
Kuiken, T., & Hartmann, M. (1991) Proceedings of the first European Cetacean Society workshop on ‘Cetacean pathology: dissection techniques and tissue sampling’. ECS Newsletter, 17, 1–39.
Lemos, L. S., de Moura, J. F., Hauser-Davis, R. A., de Campos, R. C., & Siciliano, S. (2013). Small cetaceans found stranded or accidentally captured in southeastern Brazil: Bioindicators of essential and non-essential trace elements in the environment. Ecotoxicology and Environmental Safety, 97, 166–175. https://doi.org/10.1016/j.ecoenv.2013.07.025
Lesage, V., Hammill, M. O., & Kovacs, K. M. (2001). Marine mammals and the community structure of the estuary and Gulf of St. Lawrence, Canada: Evidence from stable isotope analysis. Marine Ecology Progress Series, 210, 203–221. https://doi.org/10.3354/meps210203
Mackey, E., Oflaz, R., Epstein, M., Buehler, B., Porter, B. J., Rowles, T., Wise, S. A., & Becker, P. R. (2003). Elemental composition of liver and kidney tissues of rough-toothed dolphins (Steno bredanensis). Archives of Environmental Contamination and Toxicology, 44, 0523–0532. https://doi.org/10.1007/s00244-002-2039-9
Martineau, D., De Guise, S., Fournier, M., Shugart, L., Girard, C., Lagacé, A., & Béland, P. (1994). Pathology and toxicology of beluga whales from the St. Lawrence Estuary, Quebec, Canada. Past, present and future. Science of The Total Environment, 154(2-3), 201–215. https://doi.org/10.1016/0048-9697(94)90088-4
May-Collado, L. J., Amador-Caballero, M., Casas, J. J., Gamboa-Poveda, M. P., Garita-Alpízar, F., Gerrodette, T., González-Barrientos, R., Hernández-Mora, G., Palacios, D. M., Palacios-Alfaro, J. D., Pérez, B., Rasmussen, K., Trejos-Lasso. L., & Rodríguez-Fonseca, J. (2017). Ecology and conservation of cetaceans of Costa Rica and Panama. In M. Rossi-Santos & C. Finkl (Eds.), Advances in Marine Vertebrate Research in Latin America (pp. 293–319) Springer Press. https://doi.org/10.1007/978-3-319-56985-7_12
Méndez-Fernandez, P., Taniguchi, S., Santos, M. C. O., Cascão, I., Quérouil, S., Martín, V., Tejedor, M., Carrillo, M., Rinaldi, C., Rinaldi, R., Barragán-Barrera, D. C., Farías-Curtidor, N., Caballero, S., & Montone, R. C. (2020). Population structure of the Atlantic spotted dolphin (Stenella frontalis) inferred through ecological markers. Aquatic Ecology, 54, 21–34. https://doi.org/10.1007/s10452-019-09722-3
Oremus, M., Poole, M. M, Albertson, G. R., & Baker, C. S. (2012). Pelagic or insular? Genetic differentiation of rough-toothed dolphins in the Society Islands, French Polynesia. Journal of Experimental Marine Biology and Ecology, 432–433, 37–46. https://doi.org/10.1016/j.jembe.2012.06.027
Ortega-Ortiz, C. D., Elorriaga-Verplancken, F. R., Arroyo-Salazar, S. A., García-Valencia, R. X., Juárez-Ruiz, A. E., Figueroa-Soltero, N. A., Liñán-Cabello, M. A., & Chávez-Comparán, J. C. (2014). Foraging Behavior of the Rough-Toothed Dolphin (Steno bredanensis) in Coastal Waters of the Mexican Central Pacific. Aquatic Mammals, 40(4), 357–363. https://doi.org/10.1578/AM.40.4.2014.357
Paschoalini, V. U., Troina, G. C., Campos, L. B., & Santos, M. C. O. (2021). Trophic ecology and foraging areas of cetaceans sampled in the coastal waters of south-eastern Brazil assessed through skin δ13C and δ15N. Journal of the Marine Biological Association of the United Kingdom, 101(2), 471–480. https://doi.org/10.1017/S0025315421000217
Pitman, R. L., & Stinchcomb, C. (2002). Rough-toothed dolphins (Steno bredanensis) as predators of mahimahi (Coryphaena hippurus). Pacific Science, 56(4), 447-450. https://doi.org/10.1353/psc.2002.0043
Reeves, R. R., Stewart, B. S., Clapham, P. J., Powell, J. A. (2008). Guide to marine mammals of the world. National Audubon Society Inc.
Reif, J. S., Schaefer, A. M., & Bossart, G. D. (2015). Atlantic bottlenose dolphins (Tursiops truncatus) as a sentinel for exposure to mercury in humans: closing the loop. Veterinary Sciences, 2(4), 407–422. https://doi.org/10.3390/vetsci2040407
Sandoval-Herrera, N. I., Vargas-Soto, J. S., Espinoza, M., Clarke, T. M., Fisk, A. T., & Wehrtmann, I. S. (2015). Mercury levels in muscle tissue of four common elasmobranch species from the Pacific coast of Costa Rica, Central America. Regional Studies in Marine Science, 3, 254–261. http://dx.doi.org/10.1016/j.rsma.2015.11.011
Schwacke, L. H., Voit, E. O., Hansen, L. J., Wells, R. S., Mitchum, G. B., Hohn, A. A., & Fair, P. A. (2002). Probabilistic risk assessment of reproductive effects of polychlorinated biphenyls on bottlenose dolphins (Tursiops truncatus) from the Southeast United States Environmental Toxicology and Chemistry, 21(12), 2752–2764. https://doi.org/10.1002/etc.5620211232
Tieszen, L. L., Boutton, T. W., Tesdahl, K. G., & Slade, N. A. (1983). Fractionation and turnover of stable carbon isotopes in animal tissues: Implications for δ 13C analysis of diet. Oecologia, 57, 32–37. https://doi.org/10.1007/BF00379558
Troina, G. C., Botta, S., Dehairs, F., Di Tullio, J. C., Elskens, M., & Secchi, E. R. (2020). Skin δ13C and δ15N reveal spatial and temporal patterns of habitat and resource use by free ranging odontocetes from the southwestern Atlantic Ocean. Marine Biology, 167(186), 1–19. https://doi.org/10.1007/s00227-020-03805-8
Troina, G. C., Riekenberg, P., van der Meer, M., Botta, S., Dehairs, F., & Secchi, E. R. (2021). Combining isotopic analysis of bulk-skin and individual amino acids to investigate the trophic position and foraging areas of multiple cetacean species in the western South Atlantic. Environmental Research, 201, 111610. https://doi.org/10.1016/j.envres.2021.111610
Vélez, N., Bessudo, S., Barragán-Barrera, D. C., Ladino, F., Bustamante, P., & Luna-Acosta, A. (2021). Mercury concentrations and trophic relations in sharks of the Colombian Pacific. Marine Pollution Bulletin, 173(Part B), 113109. https://doi.org/10.1016/j.marpolbul.2021.113109
West, K. L., Mead, J. G., & White, W. (2011). Steno bredanensis (Cetacea: Delphinidae). Mammalian Species, 43(886), 177–189. https://doi.org/10.1644/886.1
Wiener, J. G., Krabbenhoft, D. P., Heinz, G. H., & Scheuhammer, A. M. (2003). Ecotoxicology of mercury. In J. G. Wiener, D. P. Krabbenhoft, G. H. Heinz & A. M. Scheuhammer (Eds.), Handbook of Ecotoxicology (2nd ed., pp. 409–463). CRC Press.
Wiener, J. G., & Suchanek, T. H. (2008). The basis for ecotoxicological concern in aquatic ecosystems contaminated by historical mercury mining. Ecological Application, 18(8), A3–A11. https://doi.org/10.1890/06-1939.1
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