Helminth diversity of two anurans: Rhinella marina and Incilius valliceps (Anura: Bufonidae) from lagunas de Yalahau, Yucatán, Mexico
DOI:
https://doi.org/10.1016/j.rmb.2017.03.023Keywords:
Parasite, Toads, Communities, RichnessAbstract
Helminth communities in amphibians in Mexico have received little attention. During 2005 and 2006, we collected a total of 52 individuals of the marine toad (Rhinella marina) and 54 of the southern Gulf Coast toad (Incilius valliceps) in the Lagunas de Yalahau (Yucatán, Mexico), in order to study their helminth communities. We produced rarefaction and extrapolation sample-size-based and coverage-based curves to provide asymptotic diversity estimators based on Hill numbers to compare the communities. We calculated the first 3 Hill numbers, which are associated with estimators of species richness and species dominance. In general, all results showed that the sample size was large enough to register most of the species of parasites present in both host toad species. We found more helminth species and a higher diversity in the R. marina community than that in I. valliceps. However, extrapolation analysis showed that when a sample size of 50 individuals is reached, there are no statistical differences between the helminth communities. Our results suggest that amphibian communities in this part of the tropics follow the same pattern as described for Nearctic latitudes, equally the terrestrial habitat of the hosts is an important factor in the structure of its helminth communities.
References
Aho, J. M. (1990). Helminth communities of amphibians and reptiles: comparative approaches to understanding patterns and processes. In G.
W. Esch, A. O. Bush, & J. M. Aho (Eds.), Parasite Communities: Patterns and Processes (pp. 157–195). Dordrecht: Springer Netherlands.
Akani, G. C., Luiselli, L., Amuzie, C. C., & Wokem, G. N. (2011). Helminth community structure and diet of three Afrotropical anuran species: A test of the interactive-versus-isolationist parasite communities hypothesis. Web Ecology, 11, 11–19.
Barton, D. P. (1999). Ecology of helminth communities in tropical Australian amphibians. In International Journal for Parasitology (Vol. 29, pp. 921–926).
Bolek, M. G., & Coggins, J. R. (2003). Helminth community structure of sympatric eastern American toad, Bufo americanus americanus, northern leopard frog, Rana pipiens, and blue-spotted salamander, Ambystoma laterale, from southeastern Wisconsin. The Journal of Parasitology, 89(4), 673–680.
Bush, A. O., Lafferty, K. D., Lotz, J. M., & Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology, 83(4), 575-583.
Cabrera-Guzmán, E., León-Règagnon, V., & García-Prieto, L. (2007). Helminth Parasites of the Leopard Frog Rana cf. forreri (Amphibia: Ranidae) in Acapulco, Guerrero, Mexico. Comparative Parasitology, 74(1), 96–107.
Campbell, J. A. (1998). Amphibians and reptiles of northern Guatemala, the Yucatan and Belize. Oklahoma: University of Oklahoma Press.
Chao, A., Gotelli, N. J., Hsieh, T. C., Sander, E. L., Ma, K. H., Colwell, R. K., & Ellison, A. M. (2014). Rarefaction and extrapolation with Hill numbers: A framework for sampling and estimation in species diversity studies. Ecological Monographs, 84(1), 45–67.
Chao, A., & Jost, L. (2012). Coverage-based rarefaction and extrapolation: Standardizing samples by completeness rather than size. Ecology, 93(12), 2533–2547.
Dobson, A. P. (1990). Models for multi-species parasite-host communities. In G. W. Esch, A. O. Bush, & J. M. Aho (Eds.), Parasite Communities: Patterns and Processes (pp. 261–288). Dordrecht: Springer Netherlands.
Espínola-Novelo, J. F., & Guillén-Hernández, S. (2008). Helminth Parasites in Chaunus marinus and Cranopis valliceps (Anura: Bufonidae) from Lagunas Yalahau, Yucatan, Mexico. Journal of Parasitology, 94(3), 672–674.
Galicia-Guerrero, S., Bursey, C., Goldberg, S. & Salgado-Maldonado, G. (2000). Helminths of two sympatric toad species. Bufo marinus (Linnaeus) and Bufo marmoreus Wiegmann, 1833 (Anura: Bufonidae) from Chamela, Jalisco, México. Comparative Parasitology, 67, 29-133.
Gelover-Alfaro A, Altamirano-Alvarez T, S.-S. M. (2001). Hábitos alimenticios de Bufo valliceps bajo distintas condiciones; con aportación al conocimiento de la ecología alimenticia de Bufo marinus y Bufo marmoreus. Revista de Zoología, 12, 28–32.
Goldberg S R, Bursey C R., Salgado-Maldonado G, Báez R, C. C. (2002). Helminth Parasites of Six Species of Anurans from Los Tuxtlas and Catemaco Lake, Veracruz, Mexico. The Southwestern Naturalist, 47(2), 293–299.
Goldberg, S. R., & Bursey, C. R. (1992). Helminths of the marine toad, Bufo marinus, (Anura, Bufonidae), from American Samoa. J Helminthol Soc Washington, 59, 131–133.
Goodman, J. D. (1989). Langeronia brenesi n. sp. (Trematoda: Lecithodendriidae) in the Mountain Yellow-Legged Frog Rana muscosa from Southern California. Transactions of the American Microscopical Society, 108, 387–393.
Guillén-Hernández, S. (1992). Comunidades de helmintos de algunos anuros de “Los Tuxtlas”, Veracruz. Universidad Nacional Autónoma de México.
Hamann, M. I., González, C. E., & Kehr, A. I. (2006). Helminth community structure of the oven frog Leptodactylus latinasus (Anura, Leptodactylidae) from Corrientes, Argentina. Acta Parasitologica, 51(4), 294–299.
Hill, M. (1973). Diversity and evenness: a unifying notation and its consequences. Ecology, 54(2), 427–432.
Horwitz, P., & Wilcox, B. A. (2005) Parasites, ecosystems and sustainability: an ecological and complex systems perspective. International Journal for Parasitology, 35, 725–732.
Hsieh, T.C., Ma, K.H, Chao, A. 2014. iNEXT: iNterpolation and EXTrapolation for species diversity. R package version 2.0. Available at http://chao.stat.nthu.edu.tw/blog/ softwaredownload
Kennedy, M. J., Killick, L. M., & Beverley-Burton, M. (1987). Life cycle studies on two Digenea, Paradistomum geckonum (Dicrocoeliidae) and Mesocoelium sociale (Mesocoelidae), in geckonid lizards from Indonesia. Canadian Journal of Zoology, 65(10), 2491–2497.
Krebs, C. J. (1989). Ecological Methodology. Harper and Row, 654.
Kuris, Armand M. Blaustein, A. R. and A. J. J. (1980). Kuris etal 80.pdf. The American Naturalist, 116,(4), 570–586.
Lee, C. J. (1996). The amphibians and reptiles of the Yucatán Peninsula. (C. U. Press, Ed.).
León-Règagnon, V., Martínez-Salazar, E. A., Lazcano-Villareal, D., & Rosas-Valdez, R. (2005). Helminth Parasites of Four Species of Anurans From Nuevo Leon, Mexico. The Southwestern Naturalist, 50(2), 251–258.
Linzey, D. W., Bursey, C. R., & Linzey, J. B. (1998). Seasonal occurrence of helminths of the giant toad, Bufo marinus (Amphibia: Bufonidae), in Bermuda. Journal of the Helminthological Society of Washington, 65(2English Article, zoo, pet), 251–258.
Luque, J. L., Martins, a. N., & Tavares, L. E. R. (2005). Community structure of metazoan parasites of the yellow Cururu toad, Bufo ictericus (Anura, Bufonidae) from Rio de Janeiro, Brazil. Acta Parasitologica, 50(3), 215–220.
MacArthur, R. H., Wilson, E. O., & MacArthur, W. (1967). The theory of island biogeography. Princeton University Press Princeton USA Major RE Kendal CE, 1(203), 203.
Magurran, a. E. (1988). Diversity Indices and Species Abundance Models. Ecological Diversity & Its Measurement, 7–32. http://doi.org/10.1007/978-94-015-7358-0_2
Mata-López, R., García-Prieto, L., & León-Règagnon, V. (2002). Infracomunidades de helmintos parásitos de Ambystoma lermaensis (Caudata: Ambystomatidae) en Lerma, México. Revista de Biologia Tropical, 50(1), 303–307.
Mcallister, C. T. Upton, S. J. Conn, D. B. (1989). A comparative study of endoparasites in three species of sympatric Bufo (Anura: Bufonidae), from Texas. Proceedings of the Helminthological Society of Washington, 56(2), 162–167.
Morrone, J. J. (2005). Hacia una síntesis biogeográfica de México. Revista Mexicana de Biodiversidad, 76(2), 207–252.
Muzzall, P. M. (1991). Helminth Infracommunities of the Frogs Rana catesbeiana and Rana clamitans from Turkey Marsh, Michigan. The Journal of Parasitology, 77(3), 366–371.
Paredes-Calderón, L., León-Règagnon, V., & García-Prieto, L. (2004). Helminth infracommunities of Rana vaillanti brocchi (Anura: Ranidae) in Los Tuxtlas, Veracruz, Mexico. Journal of Parasitology, 90(4), 692–696.
Parra-Olea, G., Flores-Villela, O., & Mendoza-Almeralla, C. (2014). Biodiversidad de anfibios en México. Revista Mexicana de Biodiversidad, 85(SUPPL.).
Pearse, A. S. (1936). Parasites from Yucatán. Carnegie Institute ofWashington Publication.
Pérez-Ponce de León, G., García-Prieto, L., & Razo-Mendivil, U. (2002). Species richness of helminth parasites in mexican amphibians and reptiles. Diversity and Distributions, 8(4), 211–218.
Poulin, R. (1997). Species richness of parasite assemblages: Evolution and Patterns. Annual Review of Ecology and Systematics, 28(1), 341–358.
Poulin, R. (2004) Macroecological patterns of species richness in parasite assemblages. Basic and Applied Ecology, 5, 423–434.
Poulin, R. (2014). Parasite biodiversity revisited: forntiers and constrains. International Journal for Parasitology, 581–589.
Poulin, R. and S. Morand. (2004). Parasite Biodiversity. Smithsonian Institution Press. Whasington, USA.
Ragoo, R. M., & Oman-Maharaj, I. R. (2003). Helminths of the cane toads Bufo marinus from Trinidad, West Indies. Caribbean Journal of Sciences, 39, 242–245.
SEMARNAT. (2003). Programa de manejo área natural protegida Parque Estatal Lagunas De Yalahau. México.
Sokal, R. R., & Rohlf, F. J. (1995). Biometry: the principles and practice of statistics in biological research. New York (Vol. 3).
Terán-Juárez, S. A. (2011). Helmintos parásitos en cinco especies de anuros en el sur de Quintana Roo, México. Instituto Tecnológico de Chetumal.
Yáñez-Arenas, C. a, & Guillén-Hernández, S. (2010). Helminth fauna of Lithobates brownorum (Anura: Ranidae) at three localities in the state of Yucatán, Mexico. Revista Mexicana de Biodiversidad, 81(1), 191–195.
Zelmer, D. A., Paredes-Calderón, L., León-Règagnon, V., & García-Prieto, L. (2004). Nestedness in colonization-dominated systems: helminth infracommunities of Rana vaillanti Brocchi (Anura: Ranidae) in Los Tuxtlas, Veracruz, Mexico. Journal of Parasitology, 90(4), 705–710.