Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Acta Parasitologica

4 Issues per year

IMPACT FACTOR 2017: 1.039
5-year IMPACT FACTOR: 1.121

CiteScore 2017: 1.17

SCImago Journal Rank (SJR) 2017: 0.641
Source Normalized Impact per Paper (SNIP) 2017: 0.738

See all formats and pricing
More options …
Volume 62, Issue 2


How does host ecology influence sampling effort in parasite diversity estimates? A case study using Neotropical freshwater fishes

Fábio Hideki Yamada
  • Corresponding author
  • Departamento de Parasitologia, Instituto de Biociências, Universidade Estadual Paulista, 18618-970, Botucatu, SP, Brazil
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Ricardo Massato Takemoto
  • Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringá, Av. Colombo, 5790, 87020-900, Maringá, PR, Brazil
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2017-04-18 | DOI: https://doi.org/10.1515/ap-2017-0042


Accurately estimating biodiversity is fundamental to ecological understanding and prediction. Helminthes are often neglected in biodiversity estimates and when included are often underestimated. Here we examine how sampling effort affects estimates of parasite diversity in an assemblage of freshwater fish from a floodplain in Brazil. We also examine how ecological and behavioral factors influence the sampling effort necessary to accurately estimate the parasite diversity associated with a fish species. We use our dataset to suggest that host species with wide geographic distribution (i.e., long migrations), gregarious behavior (i.e., shoal), larger body size, higher population density, wide diet breadth (i.e., omnivorous), and autochthonous origin, increase the effort necessary to estimate the total diversity of parasites. However, estimating this parasitic fauna has several restrictions and limitations, due to the highly complex of the floodplain ecosystems, with non-linear and non-random responses.

Keywords: Sampling effort; parasite diversity; freshwater fishes; neotropical floodplain


  • Agostinho A.A., Vazzoler A.E.M.A., Thomaz S.M. 1995. The high Paraná river basin: limnological and ichthyological aspects. In: (Eds. J.G. Tundisi, C.E.M. Bicudo and T. Matsumura-Tundisi) Limnology in Brazil. Academia Brasileira de Ciências, Rio de Janeiro, RJ, Brazil, 59–104Google Scholar

  • Agostinho A.A., Thomaz S.M., Gomes L.C. 2005. Conservation of the biodiversity of Brazil’s inland waters. Conservation Biology, 19, 646–652. CrossrefGoogle Scholar

  • Agostinho A.A., Gomes L.C., Pelicice F.M. (Eds). 2007. Ecologia e manejo de recursos pesqueiros em reservatórios do Brasil. Eduem, Maringá, BR, pp. 501. (In Portuguese)Google Scholar

  • Alvarenga F.M.S., Lacerda A.C.F., Takemoto R.M., Pavanelli, G.C. 2009. Absence of metazoan gill parasites on Potamotrygon falkneri (Potamotrygonidae) and its ecological implications in the upper Paraná River floodplain, Brazil. Pan-American Journal of Aquatic Sciences, 4, 589–592Google Scholar

  • Bunge J., Fitzpatrick M. 1993. Estimating the number of species: a review. Journal of the American Statistical Association, 88, 364–373Google Scholar

  • Bush A., Aho J.M., Kennedy C.R. 1990. Ecological versus phylogenetic determinants of helminth parasite community richness. Evolutionary Ecology, 4, 1–20CrossrefGoogle Scholar

  • Ceschini T.L., Takemoto R.M., Yamada F.H., Moreira, L.H.A., Pavanelli G.C. 2010. Metazoan parasite community of Steindachnerina brevipinna (Curimatidae) from Southern Brazil. Helminthologia, 47, 164–169. CrossrefGoogle Scholar

  • Chazdon R.L., Colwell R.K., Denslow J.S., Guariguata M.R. 1998. Statistical methods for estimating species richness for woody regeneration in primary and secondary rain forests of northeastern Costa Rica. In: (Eds F. Dallmeier and J.A. Comiskey) Forest biodiversity research. Monitoring and Modeling. The Parthenon Publishing Group, Washington, 285–309Google Scholar

  • Cochran W.G. (Ed.). 1977. Sampling techniques. 3rd ed. New York, John Wiley & Sons, Inc., New York, pp. 428Google Scholar

  • Coleman B.D., Mares M.A., Willing M.R., Hsieh Y.H. 1982. Randomness, area, and species richness. Ecology, 63, 1121–1133Google Scholar

  • Colwell R.K. 2006. EstimateS: statistical estimation of species richness and shared species from samples. Version 8: http://purl.oclc.org/estimates

  • Colwell R.K., Coddington J.A. 1994. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society Biological Science, 345, 101–118. CrossrefGoogle Scholar

  • Combes, C. (Ed.). 2001. Parasitism: The Ecology and Evolution of Intimate Interactions. The University Chicago Press, Chicago, USA, pp. 522Google Scholar

  • Dove A.D.M. 1999. A new index of interactivity in parasite communities. International Journal for Parasitology, 29, 915–920. CrossrefGoogle Scholar

  • Dove A.D.M., Cribb T.H. 2006. Species accumulation curves and their applications in parasite ecology. Trends in Parasitology, 22, 568–574. CrossrefGoogle Scholar

  • Feliu C., Renaud F., Catzeflis F., Durand P., Hugot J.P., Morand S. 1997. A comparative analysis of parasite species richness of Iberian rodents. Parasitology, 115, 453–466. CrossrefGoogle Scholar

  • Ferrari A.P., Takemoto R.M., Pavanelli G.C. 2007. Digenetic trematodes parasites of Loricariichthys platymetopon (Loricariidae, Siluriformes) of the Upper Paraná River Floodplain, Brazil. Acta Scientiarum Biological Science, 29, 327–329. CrossrefGoogle Scholar

  • Galli P., Stefani F., Benzoni F., Zullini A. 2005. Introduction of alien host–parasite complexes in a natural environment and the symbiota concept. Hydrobiologia, 548, 293–299. CrossrefGoogle Scholar

  • Graça W.J., Pavanelli C.S. (Eds.). 2007. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes. Eduem, Maringá, BR, pp. 241. (In Portuguese)Google Scholar

  • Gregory R.D., Blackburn T.M. 1991. Parasite prevalence and host sample size. Parasitology Today, 7, 316–318CrossrefGoogle Scholar

  • Guidelli G.M., Isaac A., Pavanelli G.C., Takemoto R.M. 2003. Endoparasites infracommunities of Hemisorubim platyrhynchos (Valenciennes, 1840) (Pisces, Pimelodidae) of the Baia river, upper Paraná river floodplain, Brazil: Specific composition and Ecological aspects. Brazilian Journal of Biology, 63, 261–268. CrossrefGoogle Scholar

  • Guidelli G.M., Tavechio W.L., Takemoto R.M., Pavanelli G.C. 2006. Fauna de metazoários parasitas de duas espécies de Leporinus (Characiformes, Anostomidae) da planície de inundação do Alto Rio Paraná, Brasil. Acta Scientiarum Biological Science, 28, 281–290. CrossrefGoogle Scholar

  • Hahn N.S., Fugi R., Andrian I.F. 2004. Trophic ecology of the fish assemblages. In: (Eds. S.M. Thomas, A.A. Agostinho and N.S. Hahn) The upper Paraná river and its floodplain: physical aspects, ecology and conservation. Backhuys Publishers, Leiden, Netherlands, 247–269Google Scholar

  • Hellmann J.J., Fowler G.W. 1999. Bias, precision, and accuracy of four measures of species richness. Ecological Applications, 9, 824–834. CrossrefGoogle Scholar

  • Holmes J.C., Price P.W. 1986. Communities of parasites. In: (Eds: J. Kikkawa and D.J. Anderson) Community Ecology: Pattern and Process. Blackwell Scientific Publications, Oxford, UK, 186–213Google Scholar

  • Junk W.J., Bayley P.B., Sparks R.E. 1989. The flood pulse concept in river-floodplain systems. Canadian Journal of Fishers and Aquatic Sciences, 106, 110–127Google Scholar

  • Kennedy C.R. 2009. The ecology of parasites of freshwater fishes: the search for patterns. Parasitology, 136, 1653–1662. CrossrefGoogle Scholar

  • Kuris A.M., Blaustein A.R., Alió J.J. 1980. Hosts as islands. American Naturalist, 116, 570–586Google Scholar

  • Langeani F., Castro R.M.C.O., Oyakawa T., Shibatta O.A., Pavanelli C.S., Casatti L. 2007. Diversidade da ictiofauna do Alto Rio Paraná: composição atual e perspectives futures. Biota Neotropica, 7, 181–197. (In Portuguese)Google Scholar

  • Lacerda A.C.F., Takemoto R.M., Pavanelli G.C. 2008. Digenea, Nematoda, Cestoda, and Acanthocephala, parasites in Potamotrygonidae (Chondrichthyes) from the upper Paraná River floodplain, states of Paraná and Mato Grosso do Sul, Brazil. Check List, 4, 115–122. CrossrefGoogle Scholar

  • Lizama M.L.A.P., Takemoto R.M., Pavanelli G.C. 2005. Influence of host sex and age on infracommunities of metazoan parasites of Prochilodus lineatus (Valenciennes, 1836) (Prochilodontidae) of the Upper Paraná River floodplain, Brazil. Parasite, 12, 299– 304. CrossrefGoogle Scholar

  • Lizama M.L.A.P., Takemoto R.M., Pavanelli G.C. 2009. Ecological aspects of Metazoan parasites of Astyanax altiparanae Garutti & Britski, 2000 (Characidae) of the Upper Paraná river floodplain, Brazil. Boletim do Instituto de Pesca, 34, 527–533Google Scholar

  • Magurran A.E. (Ed.). 2004. Measuring biological diversity. Oxford: Blackwell Science, pp. 256Google Scholar

  • Moreira L.H.A., Takemoto R.M., Yamada F.H., Ceschini T.L., Pavanelli G.C. 2009. Ecological aspects of metazoan endoparasites of Metynnis lippincottianus (Cope, 1870) (Characidae) from Upper Paraná River floodplain, Brazil. Helminthologia, 46, 214–219. CrossrefGoogle Scholar

  • Orlóci L. 1993. Conjectures and scenarios in recovery study. Coenoses, 8, 141–148Google Scholar

  • Palmer M.W. 1990. The estimation of species richness by extrapolation. Ecology, 71, 1195–1198Google Scholar

  • Palmer M.W. 1991. Estimating species richness: the second-order jackknife reconsidered. Ecology, 72, 1512–1513Google Scholar

  • Palmer M.W. 1995. How should one count species? Natural Area Journal, 15, 124–135Google Scholar

  • Pavanelli G.C., Machado M. H., Takemoto R.M. 1997. Fauna helmíntica de peixes do rio Paraná, região de Porto Rico, Paraná. In: (Eds A.E.A.M. Vazzoler, A.A. Agostinho, N.S. Hahn) A planície de inundação do alto Rio Paraná: aspectos físicos, biológicos e socioeconômicos. Eduem, Maringá, PR, Brazil, 307–329. (In Portuguese)Google Scholar

  • Pillar V.D. 2004. Suficiência amostral. In: (Eds: C.E.M. Bicudo and D.C. Bicudo) Amostragem em Limnologia. Editora Rima, São Carlos, BR, 25–43. (In Portuguese)Google Scholar

  • Post R.J., Millest A.L. 1991. Sample size in parasitological and vector surveys. Parasitology Today, 7, 141CrossrefGoogle Scholar

  • Poulin R. 1995. Phylogeny, ecology, and the richness of parasite community in vertebrates. Ecological Monographs, 65, 283–302. CrossrefGoogle Scholar

  • Poulin R. 1998. Comparison of three estimators of species richness in parasite component communities. Journal of Parasitology, 84, 485–490. CrossrefGoogle Scholar

  • Price P.W. 1980. The evolutionary biology of parasites. Princeton University Press, New Jersey, USA, pp. 256Google Scholar

  • Price P.W., Clancy K.M. 1983. Patterns in number of helminth parasite species in freshwater fishes. Journal of Parasitology, 69, 449–454Google Scholar

  • Ranta E. 1992. Gregariousness vs. solitude – Another look at parasite faunal richness in Canadian freshwater fishes. Oecologia, 89,150–152Google Scholar

  • Salgado-Maldonado G., Novelo-Turcotte M. T., Vazquez G., Caspeta-Mandujano J. M., Quiroz-Martínez, B., Favila M. 2014. The communities of helminth parasites of Heterandria bimaculata (Teleostei: Poeciliidae) from the upper Río La Antigua basin, east-central Mexico show a predictable structure. Parasitology, 141, 970–980. CrossrefGoogle Scholar

  • Suzuki H.I, Vazzoler A.E.A.M., Marques, E.E., Lizama M.A.P. Inada P. 2004. Reproductive ecology of the fish assemblages. In: (Eds: S.M. Thomas, A.A. Agostinho and N.S. Hahn) The upper Paraná river and its floodplain: physical aspects, ecology and conservation. Backhuys Publishers, Leiden, Netherlands, 271–291Google Scholar

  • Takemoto R.M., Pavanelli G.C., Lizama M.A.P., Luque J.L. Poulin R. 2005. Host population density as the major determinant of endoparasite species richness in floodplain fishes of the upper Paraná River, Brazil. Journal of Helminthology, 79, 7584. CrossrefGoogle Scholar

  • Takemoto R.M., Pavanelli G.C., Lizama M.A.P., Lacerda A.C.F., Yamada F.H., Moreira L.H.A., Ceschini T.L., Bellay S. 2009. Diversity of parasites of fish from the Upper Paraná River floodplain, Brazil. Brazilian Journal of Biology, 69, 691–705. CrossrefGoogle Scholar

  • Tavernari F.C., Takemoto R.M., Guidelli G.M., Lizama M.L.A.P., Lacerda A.C.F., Pavanelli G.C. 2009. Parasites of Auchenipterus osteomystax (Osteichthyes, Auchenipteridae) from two different environments, Rosana´s reservoir and upper Paraná river floodplain, Brazil. Acta Scientiarum Biological Science, 31, 49– 54. CrossrefGoogle Scholar

  • Thompson G.G., Withers P.C. 2003. Effect of species richness and relative abundance on the shape of the species accumulation curve. Austral Ecology, 28, 355–360. CrossrefGoogle Scholar

  • Torchin M.E., Lafferty K.D., Dobson A.P., Mackenzie V.J., Kuris A.M. 2003. Introduced species and their missing parasites. Nature, 421, 628–630. CrossrefGoogle Scholar

  • Ward J.V., Tockner K., Schiemer F. 1999. Biodiversity of floodplain river ecosystems: ecotones and connectivity. Regulated Rivers: Research and Management, 15, 125–139. CrossrefGoogle Scholar

  • Walther B.A., Morand S. 1998. Comparative performance of species richness estimation methods. Parasitology, 116, 395–405. CrossrefGoogle Scholar

  • Zelmer D.A., Esch G.W. 1999. Robust estimation of parasite component community richness. Journal of Parasitology, 85, 592–594Google Scholar

About the article

Received: 2016-08-11

Revised: 2016-12-13

Accepted: 2017-01-18

Published Online: 2017-04-18

Published in Print: 2017-06-01

Citation Information: Acta Parasitologica, Volume 62, Issue 2, Pages 348–353, ISSN (Online) 1896-1851, ISSN (Print) 1230-2821, DOI: https://doi.org/10.1515/ap-2017-0042.

Export Citation

© 2017 W. Stefański Institute of Parasitology, PAS.Get Permission

Comments (0)

Please log in or register to comment.
Log in