Parasitic helminths in Boana pulchella (Duméril & Bibron, 1841) (Anura: Hylidae) and their relation with host diet, body size, and habitat
Palabras clave:
Anurans, Diet, Helminths, Nematoda, Cestoda, Digenea, Acanthocephala, Swamps, BrazilResumen
We analyzed the diet and helminthological fauna of the frog Boana pulchella from the extreme south of Brazil. A total of 100 males were collected from two wetland areas in the state of Rio Grande do Sul: Ilha dos Marinheiros (n = 50) in the Rio Grande municipality, and the UFPel/ Embrapa (n = 50) in the Capão do Leão municipality. Boana pulchella food items and helminths
found in different organs were identified and quantified. We analyzed the relationship between helminth assemblage and host diet, body size, and sampling sites. Boana pulchella presented a generalist diet, composed mainly of terrestrial insects, with diet richness higher at Ilha dos Marinheiros. Helminth fauna was composed of Nematoda, Cestoda, Digenea, and Acanthocephala,
with no difference in helminth richness and abundance between sampling sites. However, the abundance of helminths presented a significant correlation with the volume of items found in the gastrointestinal contents of the anurans from UFPel/Embrapa-CL. Although for some helminth taxa there were significant differences in prevalence and mean intensity of infection among host size classes, the GLM (generalized linear model) between helminth abundance and anuran
SVL (snout-vent length) was not significant. Oxyascaris oxyascaris, Cosmocercinae gen. spp., Ochoterenella sp., Diplostomidae gen. spp., Pseudoacanthocephalus sp., and Centrorhynchus sp. were the main taxa constituting the helminth assemblage associated to B. pulchella males at the sampling sites. The occurrence of helminths at larval and adult stages suggests that B. pulchella may occupy different trophic levels in the biological cycles of those helminths. This helminth parasitic fauna associated with B. pulchella is mainly composed of taxa with heteroxenous cycles involving several intermediate and paratenic hosts, which agrees with the observations of a typical generalist anuran diet in this species.
Citas
Aho, J.M. 1990. Helminth communities of amphibians and reptiles: comparative approaches to understanding patterns and processes, p.157-195. In: Esch GW, Bush 276 AO, Aho JM (eds.) Parasite communities: patterns and processes. Chapman and Hall, London.
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-versusisolationist parasite communities hypothesis. Web Ecology 11: 11–19.
Amato, J.F.R.; Amato, S.B.; Araujo, P.B. & Quadros, A.F. 2003. First report of pigmentation dystrophy in terrestrial isopods, Atlantoscia floridana (van Name) (Isopoda, Oniscidea), induced by larval acanthocephalans. Revista Brasileira de Zoologia 20: 711–716.
Amato, J.F.R. & Amato, S.B. 2010. Técnicas gerais para coleta e preparação de helmintos endoparasitos de aves: 367–393. In: Von Matter S., F. C. Straube, I. Accordi, V. Piacentini, J. F. Cândido-Jr (ed.), Ornitologia e Conservação: Ciência Aplicada, Técnicas de Pesquisa e Levantamento. Technical Books Editora, Rio de Janeiro.
Anderson, R. C. 2000. Nematode parasites of vertebrates: their development and transmission. 2ª Ed. CABI International.
Anderson, R.C. & Bain, O. 2009. Capítulo 3: Rhaditida. In: Key to the Nematode Parasites of Vertebrates. CAB International, Massachusetts.
Antoniazzi, C.E.; López, J.A.; Duré, M. & Falico, D.A. 2013. Alimentación de dos especies de anfibios (Anura: Hylidae) en la estación de bajas temperaturas y su relación con la acumulación de energía en Santa Fe, Argentina. Revista de Biología Tropical 61: 875–886.
Bacher, M.R. & Vaucher, C. 1985. Parasitic helminths from Paraguay VII: systematic position of Oxyascaris Travassos, 1920 (Nematoda: Cosmocercoidea). Revue Suisse de Zoologie 92: 303–310.
Barger, M.A. & Nicko, B.B. 1998. Structure of Leptorhynchoides thecatus and Pomphorhynchus bulbocolli (Acanthocephala) eggs in habitat partitioning and transmission. Journal of Parasitology 84: 534-537.
Blanchet, S.; Rey, O.; Berthier, P.; Lek, S. & Loot, G. 2009. Evidence of parasite-mediated disruptive selection on genetic diversity in a wild fish population. Molecular Ecology 18: 1112–1123.
Borteiro, C., Castro, O., Sabalsagaray, M.J., Kolenc, F.; Debat, C.M. & Ubilla, M. 2015. Spargana in the Neotropical frog Hypsiboas pulchellus (Hylidae) from Uruguay. North- Western Journal of Zoology 11: 171–173.
Brooks, D.R. & Hoberg, E.P. 2000. Triage for the biosphere: the need and rationale for taxonomic inventories and phylogenetic studies of parasites. Comparative Parasitology 67: 1–21.
Bush, A.O.; Aho, J.M. & Kennedy, C.R. 1990. Ecological versus phylogenetic determinants of helminth parasite community richness. Evolutionary Ecology 4: 1–20.
Bush, A.O.; Lafferty, K.D., Lotz, J.M. & Shostar, A.W. 1997. Parasitology meets ecology on its own terms: Margolis et al. Revisited. Journal of Parasitology 83: 575–583.
Campião, K.M.; Dias, O.T.; Silva, R.J.; Ferreira, V.L. & Tavares, L.E.R. 2016. Living apart and having similar trouble: frog helminth parasites determined by the host or by the habitat? Canadian Journal of Zoology 94: 761–765.
Chabaud, A.G. 2009. Capítulo 9: Ascaridida. In: Key to the Nematode Parasites of Vertebrates. CAB International, Massachusetts
Chao, A. & Jost, L. 2012. Coverage‐based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology, 93: 2533-2547.
Costello, M.J. 1990. Predator feeding strategy and prey importance: a new graphical analysis. Journal of Fish Biology 36: 261-263.
Coyner, D.F.; Spalding, M.G. & Forrester, D. J. 2002. Epizootiology of Eustrongylides ignotus in Florida: distribution, density, and natural infections in intermediate hosts. Journal of Wildlife Diseases 38: 483-499.
CRMV. 2012. Conselho Federal de Medicina Veterinária. Available at: http://portal.cfmv.gov.br/ Accessed in: 25 September 2015.
Crofton, H.D. 1971. A quantitative approach to parasitism. Parasitology 62: 179-194.
Draghi, R.; Drago, F.B.; Saibene, P.E. & Agostini, M.G. 2020. Helminth communities from amphibians inhabiting agroecosystems in the Pampean Region (Argentina) Revue suisse de Zoologie 127: 261-274.
Duré, M.I.; Schaefer, E.F; Hamann, M.I. & Kehr, A.I. 2004. Consideraciones ecológicas sobre la dieta, la reprodución y el parasitismo de Psedopaludicola boliviana (Anura, Leptodactylidae) de Corrientes, Argentina. Phylomedusa 3: 121-131.
Freitas, J.F.T. 1958. Estudos sobre “Oxyascarididae” (Travassos, 1920) (Nematoda, Subuluroidea). Memórias do Instituto Oswaldo Cruz 56: 489–515.
Frost, D.R. 2022. Amphibian Species of the World: an Online Reference. Version 6.1 (Accessed June 20, 2022). Electronic Database accessible at https://amphibiansoftheworld.amnh. org/index.php. American Museum of Natural History, New York, USA.
Guerrero, R. & Yánez-Muñoz, M.H. 2018. Acarine biodiversity in Ecuador: two new species of endoparasitic chiggers (Acarina: Trombiculidae) from terrestrial andean anurans. MANTER: Journal of Parasite Biodiversity 9: 18.
Hamann, M.I. & González, C.E. 2009. Larval digenetic trematodes in tadpoles of six amphibian species from northeastern Argentina. Journal of Parasitology 95: 623-628.
Hammer Ø.;, Harper, D.A.T. & Ryan, P.D. 2001 PAST: Paleontological Statistics Software Package for Education and Data Analysis. Paleontological Statistics, PAST, 2.16. Available at: https://palaeo-electronica.org/2001_1/past/ issue1_01.htm Accessed 10 March 2020.
Hocking, D.J. & Babbitt, K.J. 2014. Amphibian contributions to ecosystem services. Herpetological Conservation and Biology 9: 1-17.
Hsieh, T. C., Ma, K. H. & Chao, A. 2016. iNEXT: an R package for rarefaction and extrapolation of species diversity (H ill numbers). Methods in Ecology and Evolution 7: 1451-1456.
Huckembeck, S.; Loebmann, D.; Albertoni, E.F.; Hefler, S.M.; Oliveira, M.C.L.M. & Garcia, A. 2014. Feeding ecology and basal food sources that sustain the Paradoxal frog Pseudis minuta: Multiple approaches combining stomach content, prey availability, and stable isotopes. Hydrobiologia 740: 253-264.
Hudson, P.J.; Dobson, A.P. & Lafferty, K.D. 2006. Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution 21: 38-385.
Jones, A. 2005. Capítulo 25: Diplodiscidae Cohn, 1904. In: Key to the Trematoda. Volume 2. CABI Publishing, Massachusetts.
Kawakami, E. & Vazzoler, C. 1980. Método gráfico e estimative de índice alimentar aplicado no estudo de alimentação de peixes. Boletim do Instituto Oceanográfico 29: 205-207.
Kehr, AI. & Hamann, M.I. 2003. Ecological aspects of parasitism in the tadpole of Pseudis paradoxa from Argentina. Herpetological Review 34: 336-341.
Kelehear, C.; Hudson, C.M.; Mertins, J.W. & Shine, R. 2017. First report of exotic ticks (Amblyomma rotundatum) parasitizing invasive cane toads (Rhinella marina) on the Island of Hawai’i. Ticks and tick-borne diseases 8: 330-333.
Khalil, L.F.; Jones, A. & Bray, R.A. 1994. Order Cyclophyllidea (diagnosis and key to families). In: Keys to the cestode parasites of vertebrates. CAB International, Wallingfors, U.K.
Khokhlova, I.S.; Serobyan, V.; Degen, A.A.; Krasnov, B.R. 2010. Host gender e offspring quality in a flea parasitic on a rodent. The Journal of Experimental Biology 213: 3299-3304.
Kiewiadomska, K. 2002. Família Diplostomidae. In: Gibson, D.I.; Jones, A. & Bray, R.A. Keys to the Trematoda – Volume I. CABI International e The Natural History Museum, Londres, UK.
Klaion, T. 2011. Diet and nematode infection in Proceratoprhys boiei (Anura: Cycloramphidae) from two Atlantic rainforest remnants in Southeastern Brazil. Anais da Academia Brasileira de Ciências 83: 1303-1312.
Klein, S.L. 2004. Hormonal e immunological mechanisms mediating sex differences in parasitic infection. Parasite Immunology 26: 247–264.
Koprivnikar, J.; Marcogliese, D.J.; Rohr, J.R.; Orlofske, S.A.; Raffel, T.R. & Johnson P.T.J. 2012. Macroparasite infections of amphibians: what can they tell us? EcoHealth 9: 342-360.
Lunaschi, L.I. & Drago, F.B. 2010. A new species of Centrorhynchus (Acanthocephala, Centrorhynchidae) endoparasite of Guira guira (Aves, Cuculidae) from Argentina. Helminthologia 41: 38-47.
Machado, D.A.F. 1940. Pesquisas helmintológicas realizadas no estado de Mato Grosso – Acanthocephala. Memórias do Instituto Oswaldo Cruz 35: 593-601.
Mackenzie, J.V. 2007. Human land use and patterns of parasitism in tropical anphibian host. Biological Conservation 137: 102-116.
Maneyro, R. & Rosa, I. 2004. Temporal and spatial changes in the diet of Hyla pulchella (Anura, Hylidae) in southern Uruguay. Phyllomedusa 3: 101-113.
Maneyro, R.; Loebmann, D.; Tozetti, A. & Fonte, L.F.M. 2017. Anfíbios das planícies costeiras do extremo sul do Brasil e Uruguai. Anolis Books Editora, 176 pp.
Marcogliese, D.J. 2004. Parasites: Small Players with Crucial Roles in the Ecological Theater. EcoHealth 1: 151-164.
Marcogliese D.J. 2005. Parasites of the superorganism: are they indicators of ecosystem health? International Journal for Parasitology 35: 705-716.
Moura, M.O.F.L.; Bregue, S.B. & Valente, A.L.S. 2017. Levantamento de helmintos de aves de rapina de Pelotas, Rio Grande do Sul. XXVI Congresso de Iniciação Científica, Pelotas, 4 pp.
Mugnai, R.; Nessimian, J.L & Baptista, D.F. 2010. Manual de identificação de macroinvertebrados aquáticos do estado do Rio de Janeiro. Technical Books Editora, 174 pp.
Needham, J.G. & Needham, P.R. 1978. Guía para el estudio de los seres vivos de las aguas dulces. Editora Reverté, S.A., 131 pp.
Olsen, O.W. 1974. Animal parasites: their life cycles and ecology. Third Edition.
Petrochenko, V.I. 1971. Acanthocephala of domestic and wild animals. Israel Program for Scientific Translations, 465 pp.
Poulin, R. 1996. Sexual inequalities in helminth infections: a cost of being male? The American Naturalist 147: 287-295.
Poulin, R. 1997. Species richness of parasite assemblages: evolution and patterns. Annual Review of Ecology and Systematics 28: 341-358.
Reiczigel, J.; Marozzi, M.; Fábián, I. & Rózsa, L. 2019. Biostatistics for parasitologists – a primer to Quantitative Parasitology. Trends in Parasitology 35: 277-281.
Rosa, A.C.; Maneyro, R. & Camargo, A. 2011. Trophic niche variation and individual specialization in Hypsiboas pulchellus (Duméril and Bibron, 1841) (Anura, Hylidae) from Uruguay. South American Journal of Herpetology 6: 98-106.
Santos, V.G.T.; Amato, S.B. & Borges, M.M. 2013. Community structure of helminth parasites of the “Cururu” toad, Rhinella icterica (Anura: Bufonidae) from southern Brazil. Parasitology Research 112: 1097-1103.
Seeliger, U.; Odebrecht, C. & Castello, J.P. 1998. Fluxo de energia e habitats no estuário da Lagoa dos Patos: 326. In: Seeliger et al. Os ecossistemas costeiro e marinho do extremo sul do Brasil. Rio Grande.
Schmidt, G.D. 1986. Handbook of tapeworm identification. Florida Constitution Revision Commission, 675 pp.
Silveira, E.C.; Mascarenhas, C.S.; Antunes, G.M.; Loebmann, D. 2019. Occurrence of Hannemania sp. (Acariformes: Leeuwenhoekiidae) larvae in males of Boana pulchella (Anura: Hylidae) from southern Brazil. Revista Mexicana de Biodiversidad 90: 1-5.
Solé, M. & Pelz, B. 2007. Do male tree frogs feed during the breeding season? Stomach flushing of five syntopic hylid species in Rio Grande do Sul, Brazil. Journal of Natural History 41: 2757-2763.
Spalding, M.G.; Bancroft, G.T. & Forrester, D.J. 1993. The epizootiology of eustrongylidosis in wading birds (Ciconiiformes) in Florida. Journal of Wildlife Diseases 29: 237-249.
StataCorp, L.P. 2007. Stata data analysis and statistical software. Special Edition Release (10.1 ed.), Stata, College Station. 733pp.
Sures, B. 2004. Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends in Parasitology 20: 170-177.
Tkach, V.V. 2008. Family Haematoloechidae Freitas & Lent, 1939: 361-365. In: Keys to the Trematoda. v. 3. – CABI International, London.
Travassos, L. 1920 Contribuições para o conhecimento da fauna helmintológica brasileira. Memórias do Instituto Oswaldo Cruz 67:1–886. Archivos da Escola Superior de Agronomia e Medicina Veterinária 4: 17-20.
Travassos, L. 1926. Contribuição para o conhecimento da fauna helmintológica brasileira. XX. Revisão dos acantocéfalos brazileiros. Parte II. Fam. Echinorhynchidae. Sf. Centrarchinae Travassos, 1919. Memórias do Instituto Oswaldo Cruz 19: 31-125.
Travassos, L.; Freita, J.F.T. & Kohn, A. 1969. Trematódeos do Brasil. Memórias do Instituto Oswaldo Cruz 67: 1-886.
Van, S.M.; Schittini, G.M.; Marra, R.V.; Azevedo, A.R.M.; Vicente, J.J. & Vrcibradic, D. 2006. Body size, diet and endoparasites of the microhylid frog Chiasmocleis capixaba in an Atlantic Forest areaof southern Bahiastate, Brazil. Brazilian Journal of Biology 66: 167-173.
Vaucher, C. 1987. Polystomes d'Equateur, avec description de deux nouvelles especes. Bulletin de la Societe Neuchfteloise des Sciences Naturelles 110: 45-56.
Von Zuben, C.J. 1997. Implicações da agregação espacial de parasitas para a dinâmica populacional na interação hospedeiro-parasita. Revista de Saúde Pública 31: 523-530.
Wegner, K.M.; Kalbe, M.; Kurtz, J.; Reusch, T.B.H. & Milinski, M. 2003. Parasite selection for immunogenetic optimality. Science 301: 1343.
Wilson, K.; Bjørnstad; O.; Dobson, N.A.P.; Merler, S.; Poglayen, G.; Randolph, S.E.; Read, A.F & Skorping, A. 2002. Heterogeneities in macroparasite infections: patterns e processes, p 6-44. In: Hudson, P. J.; Rizzoli, A.; Grenfell, B. T.; Heesterbeek, H.; Dobson, A. P. (eds) The Ecology of Wildlife Diseases, United Kingdom, Oxford Press.
Descargas
Publicado
Cómo citar
Número
Sección
Licencia
Derechos de autor 2022 Cuadernos de Herpetología
Esta obra está bajo una licencia internacional Creative Commons Atribución-NoComercial 4.0.
Atribución - No Comercial - Sin Obras Derivadas 4.0 Internacional
Usted es libre de:
- Compartir — copiar y redistribuir el material en cualquier medio o formato
- La licenciante no puede revocar estas libertades en tanto usted siga los términos de la licencia
Bajo los siguientes términos:
- Atribución — Usted debe dar crédito de manera adecuada , brindar un enlace a la licencia, e indicar si se han realizado cambios . Puede hacerlo en cualquier forma razonable, pero no de forma tal que sugiera que usted o su uso tienen el apoyo de la licenciante.
- No Comercial — Usted no puede hacer uso del material con propósitos comerciales .
- Sin Derivadas — Si remezcla, transforma o crea a partir del material, no podrá distribuir el material modificado.
- No hay restricciones adicionales — No puede aplicar términos legales ni medidas tecnológicas que restrinjan legalmente a otras a hacer cualquier uso permitido por la licencia.
