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The influence of host ecology and biogeography on the helminth species richness of freshwater fishes in Mexico

Published online by Cambridge University Press:  19 July 2012

L. GARRIDO-OLVERA
Affiliation:
Posgrado en Ciencias Biológicas, Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad Universitaria, Apartado Postal 70-275, C. P. 04510, Distrito Federal, México
H. T. ARITA
Affiliation:
Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Antigua Carretera a Pátzcuaro 8701, Ex-Hacienda de San José de La Huerta, C. P. 58190, Morelia, Michoacán, México
G. PÉREZ-PONCE DE LEÓN*
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad Universitaria, Apartado Postal 70-153, C. P. 04510, Distrito Federal, México
*
*Corresponding author: Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad Universitaria, Apartado Postal 70-153, C. P. 04510, Distrito Federal, México. Tel: +56229131. Fax: +55500164. E-mail: [email protected]

Summary

Freshwater fish helminths, the most well known Mexican vertebrate parasites, include approximately 260 species (platyhelminthes, acanthocephalans, nematodes, and hirudineans). The distribution patterns of adult helminth diversity (throughout parasite and host groups and hydrological regions) are described and the effects of host traits and environmental and geographical factors on diversity are evaluated. Adult helminths include 160 species, parasitizing 149 fish species of 23 families distributed in 21 regions. Nematoda was the most species-rich (>50 species). Cichlidae harboured rich helminth assemblages, with widespread parasites. By contrast, Atherinopsidae and Goodeidae showed relatively poor helminth assemblages, including specific parasites with narrow distribution. Helminth richness in southeastern Mexico was higher than northern or central regions. Non-parametric richness estimators were used to avoid confusion in comparisons with unequal sampling efforts. Bootstrap values, the method with the best performance, indicated that estimated richness shows the same distribution pattern that observed richness. Non-phylogenetic and phylogenetic analyses were used to determine the role of different factors in the parasite diversification. The distribution range was the most important richness predictor (widespread fishes harbour richer parasite assemblages), although interactions between this variable and others such as trophic level, latitude, habitat temperature and precipitation are also important. Likewise, biogeographical factors can also affect parasite diversity.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Aguilar-Aguilar, R., Rosas-Valdez, R. and Pérez-Ponce de León, G. (2010). Rhabdochona ictaluri sp. nov. (Nematoda, Rhabdochonidae) from ictalurid catfishes in Mexico. Acta Parasitologica 55, 276280.CrossRefGoogle Scholar
Aguirre-Macedo, M. L. and Scholz, T. (2005). Culuwiya cichlidorum n. sp. (Digenea: Haploporidae) from the black-belt cichlid Vieja maculicauda (Pisces: Cichlidae) from Nicaragua. Journal of Parasitology 91, 13791384.CrossRefGoogle Scholar
Bell, G. and Burt, A. (1991). The comparative biology of parasite species diversity: intestinal helminths of freshwater fishes. Journal of Animal Ecology 60, 10461063.CrossRefGoogle Scholar
Bloom, D. D., Piller, K. R., Lyons, J., Mercado-Silva, N. and Medina-Nava, M. (2009). Systematics and Biogeography of the Silverside Tribe Menidiini (Teleostomi: Atherinopsidae) Based on the Mitochondrial ND2 Gene. Copeia 2, 408417. doi:10.1643/CI-07-151.CrossRefGoogle Scholar
Bloom, D. D., Unmack, P. J., Gosztonyi, A. E., Piller, K. R. and Lovejoy, N. R. (2012). It's a family matter: Molecular phylogenetics of Atheriniformes and the polyphyly of the surf silversides (Family: Notocheiridae). Molecular Phylogenetics and Evolution 62, 10251030. doi:10.1016/j.ympev.2011.12.006.CrossRefGoogle ScholarPubMed
Breden, F., Ptacek, M. B., Rashed, M., Taphorn, D. and Figueiredo, C. A. (1999). Molecular Phylogeny of the Live-Bearing Fish Genus Poecilia (Cyprinodontiformes: Poeciliidae). Molecular Phylogenetics and Evolution 12, 95104.CrossRefGoogle ScholarPubMed
Caspeta-Mandujano, J. M. (2005) Nematode Parasites of Freshwater Fish in Mexico: Key to Species, Descriptions and Distribution. Universidad Autónoma del Estado de Morelos, Cuernavaca, Morelos, México.Google Scholar
Chakrabarty, P. (2007). A Morphological Phylogenetic Analysis of Middle American Cichlids with Special Emphasis on the Section ‘Nandopsis’ sensu Regan. Miscellaneous Publications Museum of Zoology, University of Michigan 198, 131.Google Scholar
Choudhury, A. and Dick, T. A. (2000). Richness and diversity of helminth communities in tropical freshwater fishes: empirical evidence. Journal of Biogeography 27, 935956. doi:10.1046/j.1365-2699.2000.00450.x.CrossRefGoogle Scholar
Colwell, R. K. (2006). EstimateS: Statistical Estimation of Species Richness and Shared Species from Samples. Version 8. Persisten URL <purl.oclc.org/estimates>Google Scholar
Colwell, R. K., Mao, C. X. and Chang, J. (2004). Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85, 27172727.CrossRefGoogle Scholar
Comisión Nacional del Agua (2008). Estadísticas del Agua en México. Secretaría del Medio Ambiente y Recursos Naturales, México, D. F.Google Scholar
Concheiro Pérez, G. A., Rícan, O., Ortí, G., Bermingham, E., Doadrio, I. and Zardoya, R. (2007). Phylogeny and biogeography of 91 species of heroine cichlids (Teleostei: Cichlidae) based on sequences of the cytochrome b gene. Molecular Phylogenetics and Evolution 43, 91110. doi:10.1016/j.ympev.2006.08.012.CrossRefGoogle Scholar
Crawley, M. J. (2007). The R Book. John Wiley & Sons, Ltd, Imperial College London at Silwood Park, UK.CrossRefGoogle Scholar
Cunha, C., Mesquita, N., Dowling, T. E., Gilles, A. and Coelho, M. M. (2002). Phylogenetic relationships of Eurasian and American cyprinids using cytochrome b sequences. Journal of Fish Biology 61, 929944. doi:10.1006/jfbi.2002.2105.CrossRefGoogle Scholar
Doadrio, I. and Domínguez, O. (2004). Phylogenetic relationships within the fish family Goodeidae based on cytochrome b sequence data. Molecular Phylogenetics and Evolution 31, 416430. doi:10.1016/j.ympev.2003.08.022.CrossRefGoogle ScholarPubMed
Dobson, A. P. and Roberts, M. (1994). The population dynamics of parasitic helminth communities. Parasitology 109 (Suppl.) S97S108.CrossRefGoogle ScholarPubMed
Domínguez-Domínguez, O., Doadrio, I. and Pérez-Ponce de León, G. (2006). Historical biogeography of some river basins in central Mexico evidenced by their goodeine freshwater fishes: a preliminary hypothesis using secondary Brooks parsimony analysis. Journal of Biogeography 33, 14371447. doi:10.1111/j.1365-2699.2006. 01526.CrossRefGoogle Scholar
Espinosa-Huerta, E., García-Prieto, L. and Pérez-Ponce de León, G. (1996). Helminth community structure of Chirostoma attenuata (Osteichthyes: Atherinidae) in two Mexican lakes. Southwestern Naturalist 41, 288292.Google Scholar
ESRI. (1999). Arc View GIS, Version 3.2. Environmental Systems Research Institute, Redlands, CA, USA.Google Scholar
Felsenstein, J. (1985). Phylogenies and the comparative method. American Naturalist 125, 115.CrossRefGoogle Scholar
Fernandez-Eguiarte, A., Zavala-Hidalgo, J. and Romero-Centeno, R. (2010). Atlas Climático Digital de México. Centro de Ciencias de la Atmósfera, UNAM. http://uniatmos.atmosfera.unam.mx/Google Scholar
Froese, R. and Pauly, D. (2011). FishBase. World Wide Web electronic publication. www.fishbase.org, version (11/2011).Google Scholar
García-Prieto, L., Garcia-Varela, M., Mendoza-Garfias, B. and Pérez-Ponce de León, G. (2010). Checklist of the Acanthocephala in wildlife vertebrates of Mexico. Zootaxa 2419, 150.CrossRefGoogle Scholar
Garland, T. Jr., Harvey, P. H. and Ives, A. R. (1992). Procedures for the analysis of comparative data using phylogenetically independt contrasts. Systematic Biology 41, 1832.CrossRefGoogle Scholar
Garrido-Olvera, L., García-Prieto, L. and Pérez-Ponce de León, G. (2006). Checklist of the adult nematode parasites of fishes in freshwater localities from Mexico. Zootaxa 1201, 145.CrossRefGoogle Scholar
Guégan, J.-F. and Kennedy, C. R. (1993). Maximum local helminth parasite community richness in British freshwater fish: a test of the colonization time hypothesis. Parasitology 106, 61100.CrossRefGoogle Scholar
Hardman, M. and Hardman, L. M. (2008). The relative importance of body size and paleoclimatic change as explanatory variables influencing lineage diversification rate: an evolutionary analysis of bullhead catfishes (Siluriformes: Ictaluridae). Systematic Biology 57, 16130. doi:10.1080/10635150801902193.CrossRefGoogle ScholarPubMed
Harris, P. M. and Mayden, R. L. (2001). Phylogenetic relationships of major clades of Catostomidae (Teleostei: Cypriniformes) as inferred from mitochondrial SSU and LSU rDNA sequences. Molecular Phylogenetics and Evolution 20, 225237. doi:10.1006/mpev.2001.0980.CrossRefGoogle ScholarPubMed
Hertwig, S. T. (2008). Phylogeny of the Cyprinodontiformes (Teleostei, Atherinomorpha): the contribution of cranial soft tissue characters. Zoologica Scripta 37, 141174. doi:10.1111/j.1463-6409.2007.00314.x.CrossRefGoogle Scholar
Hrbek, T., Seckinger, J. and Meyer, A. (2007). A phylogenetic and biogeographic perspective on the evolution of poeciliid fishes. Molecular Phylogenetics and Evolution 43, 986998. doi:10.1016/j.ympev.2006.06.009.CrossRefGoogle ScholarPubMed
Huidobro, L., Morrone, J. J. and Alvarez, J. L. (2006). Distributional patterns of freshwater taxa (fishes, crustaceans and plants) from the Mexican transition zone. Journal of Biogeography 33, 731741. doi:10.1111/j.1365-2699.2005.01400.x.CrossRefGoogle Scholar
Hulsey, C. D., García de León, F. J. and Rodiles-Hernández, R. (2006). Micro- and macroevolutionary decoupling of cichlid jaws: a test of liem's key innovation hypothesis. Evolution 60, 20962109.Google ScholarPubMed
Kohn, A., Cohen, S. C. and Salgado-Maldonado, G. (2006). Checklist of Monogenea parasites of freshwater and marine fishes, amphibians and reptiles from Mexico, Central America and Caribbean. Zootaxa 1289, 1114.Google Scholar
Kuris, A. M., Blaustein, A. R. and Alió, J. J. (1980). Hosts as islands. American Naturalist 116, 570586.CrossRefGoogle Scholar
Lavoué, S., Miya, M., Kawaguchi, A., Yoshino, T. and Nishida, M. (2008). The phylogenetic position of an undescribed paedomorphic clupeiform taxon: mitogenomic evidence. Ichthyological Research 55, 328334. doi:10.1007/s10228-008-0044-3.CrossRefGoogle Scholar
Luque, J. L., Mouillot, D. and Poulin, R. (2004). Parasite biodiversity and its determinants in coastal marine teleost fishes of Brazil. Parasitology 128, 671682.CrossRefGoogle ScholarPubMed
Luque, J. L. and Poulin, R. (2004). Use of fish as intermediate hosts by helminth parasites: a comparative analysis. Acta Parasitologica 49, 353361.Google Scholar
Luque, J. L. and Poulin, R. (2008). Linking ecology with parasite diversity in Neotropical fishes. Journal of Fish Biology 72, 189204. doi:10.1111/j.1095-8649.2007.01695.x.CrossRefGoogle Scholar
MacArthur, R. H. and Wilson, E. O. (1967). The Theory of Island Biogeography. Princeton University Press, Princeton, NJ, USA.Google Scholar
Maddison, W. P. and Maddison, D. R. (2011). Mesquite: A Modular System for Evolutionary Analysis. Version 2.75. http://mesquiteproject.orgGoogle Scholar
Marcogliese, D. J. (2002). Food webs and the transmission of parasites to marine fish. Parasitology 124, S83S99.CrossRefGoogle ScholarPubMed
McMahan, C. D., Geheber, A. D. and Piller, K. R. (2010). Molecular systematics of the enigmatic Middle American genus Vieja (Teleostei: Cichlidae). Molecular Phylogenetics and Evolution 57, 12931300. doi:10.1016/j.ympev.2010.09.005.CrossRefGoogle ScholarPubMed
Mejía-Madrid, H., Vázquez-Domínguez, E. and Pérez-Ponce de León, G. (2007). Phylogeography and freshwater basins in Central Mexico: recent history as revealed by the fish parasite Rhabdochona lichtenfelsi (Nematoda). Journal of Biogeography 34, 787801.CrossRefGoogle Scholar
Midford, P. E., Garland, T. Jr. and Maddison, W. P. (2011). PDAP Package of Mesquite. Version 1.16. http://mesquiteproject.org/pdap-mesquite/index.htmlGoogle Scholar
Miller, R. R., Minckley, W. L. and Norris, S. M. (2005). Freshwater Fishes of México, 1st Edn.The University of Chicago Press, Chicago, IL, USA.Google Scholar
Mirande, J. M. (2009). Weighted parsimony phylogeny of the family Characidae (Teleostei: Characiformes). Cladistics 25, 574613. doi:10.1111/j.1096-0031.2009.00262.x.CrossRefGoogle Scholar
Miya, M., Takeshima, H., Endo, H., Ishiguro, N. B., Inoue, J. G., Mukai, T., Satoh, T. P., Yamaguchi, M., Kawaguchi, A., Mabuchi, K., Shirai, S. M. and Nishida, M. (2003). Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 26, 121138.CrossRefGoogle ScholarPubMed
Morand, S., Cribb, T. H., Kulbicki, M., Rigby, M. C., Chauvet, C., Dufour, V., Faliex, E., Galzin, R., Lo, C. M., Lo-Zat, A., Pichelin, S. and Sasal, P. (2000). Endoparasite species richness of New Caledonian butterfly fishes: host density and diet matter. Parasitology 121, 6572.CrossRefGoogle ScholarPubMed
Moravec, F. (1998). Nematodes of Freshwater Fishes of the Neotropical Region. Academia, Praha, Czech Republic.Google Scholar
Nadler, S. and Pérez-Ponce de León, G. (2011). Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology 138, 16881709. doi:10.1017/S003118201000168X.CrossRefGoogle ScholarPubMed
Near, T. J., Bolnick, D. I. and Wainwright, P. C. (2005). Fossil calibrations and molecular divergence time estimates in centrarchid fishes (Teleostei: Centrarchidae). Evolution 59, 17681782.Google ScholarPubMed
Nelson, J. S. (2006). Fishes of the World, 4th Edn.John Wiley & Sons, Inc. Hoboken, New Jersey, USA.Google Scholar
Oceguera-Figueroa, A., Sidall, M. E. and García-Prieto, L. (2010). Sanguijuelas. Biodiversitas 90, 15.Google Scholar
Page, R. D. M. (2003). Tangled Trees: Phylogeny, Cospeciation, and Coevolution. University of Chicago Press, Chicago, IL, USA.Google Scholar
Paterson, A. M. and Gray, R. D. (1997). Host–parasite cospeciation, host switching, and missing the boat. In Host–Parasite Evolution: General Principles and Avian Models (ed. Clayton, D. H. and Moore, J.), pp. 236250. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Pérez-Ponce de León, G. and Choudhury, A. (2005). Biogeography of helminth parasites of freshwater fish in Mexico: The search for patterns and processes. Journal of Biogeography 32, 645659.CrossRefGoogle Scholar
Pérez-Ponce de León, G. and Choudhury, A. (2010). Parasite inventories and DNA-based taxonomy: Lessons from helminths of freshwater fishes in a megadiverse country. Journal of Parasitology 96, 236244.CrossRefGoogle Scholar
Pérez-Ponce de León, G., García-Prieto, L., León-Régagnon, V. and Choudhury, A. (2000). Helminth communities of native and introduced fishes in Lake Pátzcuaro, Michoacán, México. Journal of Fish Biology 57, 303325.CrossRefGoogle Scholar
Pérez-Ponce de León, G., García-Prieto, L. and Mendoza-Garfias, B. (2007). Trematode parasites (Platyhelminthes) of wildlife vertebrates in Mexico. Zootaxa 1534, 1247.CrossRefGoogle Scholar
Pérez-Ponce de León, G., García-Prieto, L. and Mendoza-Garfias, B. (2011). Describing Parasite Biodiversity: The Case of the Helminth Fauna of Wildlife Vertebrates in Mexico. In Changing Diversity in Changing Environment (ed. Grill, O. and Gianfranco, V.), pp. 3354. INTECH open. Croatia. Available from: http://www.intechopen.com/articles/show/title/describing-parasite-biodiversity-the-case-of-the-helminth-fauna-of-wildlife-vertebrates-in-mexico.Google Scholar
Pérez-Ponce de León, G., García-Prieto, L., Osorio-Sarabia, D. and León-Règagnon, V. (1996). Listados Faunísticos de México VI. Helmintos Parásitos de Peces de Aguas Continentales de México, 1st Edn.Instituto de Biología, Universidad Nacional Autónoma de México, México.Google Scholar
Pérez-Rodríguez, R., Domínguez-Domínguez, O., Pérez-Ponce de León, G. and Doadrio, I. (2009). Phylogenetic relationships and biogeography of the genus Algansea Girard (Cypriniformes: Cyprinidae) of central Mexico inferred from molecular data. BMC Evolutionary Biology 9, 223. doi:10.1186/1471-2148-9-223.CrossRefGoogle ScholarPubMed
Ponlet, N., Chaisiri, K., Claude, J. and Morand, S. (2011). Incorporating parasite systematics in comparative analyses of variation in spleen mass and testes sizes of rodents. Parasitology 138, 18041814. doi:10.1017/S003118201100028X.CrossRefGoogle ScholarPubMed
Poulin, R. (1995). Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecological Monographs 65, 283302.CrossRefGoogle Scholar
Poulin, R. (1998a). Evolutionary ecology of parasites. Chapman and Hall, New York.Google Scholar
Poulin, R. (1998b). Comparison of three estimators of species richness in parasite component communities. Journal of Parasitology 84, 485490.CrossRefGoogle ScholarPubMed
Poulin, R. (2001). Another look at the richness of helminth communities in tropical freshwater fish. Journal of Biogeography 28, 737743. doi:10.1046/j.1365-2699. 2001.00570.x.CrossRefGoogle Scholar
Poulin, R. (2011). Uneven distribution of cryptic diversity among higher taxa of parasitic worms. Biology Letters 7, 241244. doi:10.1098/rsbl.2010.0640.CrossRefGoogle ScholarPubMed
Poulin, R. and Morand, S. (2004). Parasite Biodiversity. Washington, DC: Smithsonian Books.Google Scholar
Poulin, R. and Rohde, K. (1997). Comparing the richness of metazoan communities of marine fishes: controlling for host phylogeny. Oecologia 110, 278283.CrossRefGoogle ScholarPubMed
Ptacek, M. B. and Breden, F. (1998). Phylogenetic relationships among the mollies (Poeciliidae: Poecilia: Mollienesia group) based on mitochondrial DNA sequences. Journal of Fish Biology 53 (Suppl. A), 6481.CrossRefGoogle Scholar
R Development Core Team. (2010). R: Language and Environment for Statistical Computing. R Foundation for Statistical Computing. http://www.r-project.org/Google Scholar
Reznick, D. N., Mateos, M. and Springer, M. S. (2002). Independent Origins and Rapid Evolution of the Placenta in the Fish Genus Poeciliopsis. Science 298, 10181020. doi:10.1126/science.1076018.CrossRefGoogle ScholarPubMed
Rícan, O., Zardoya, R. and Doadrio, I. (2008). Phylogenetic relationships of Middle American cichlids (Cichlidae, Heroini) based on combined evidence from nuclear genes, mtDNA, and morphology. Molecular Phylogenetics and Evolution 49, 941957. doi:10.1016/j.ympev.2008.07.022.CrossRefGoogle ScholarPubMed
Roberts, M. G., Dobson, A. P., Arneberg, P., De Leo, G. A., Krecek, R. C., Manfredi, M. T., Lanfranchi, P. and Zaffaroni, E. (2002). Parasite community ecology and biodiversity. In The Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 6382. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Rohde, K. (1992). Latitudinal gradients in species diversity: the search for the primary cause. Oikos 65, 514527.CrossRefGoogle Scholar
Rohde, K., Hayward, C. and Heap, M. (1995). Aspects of the ecology of metazoan ectoparasites of marine fishes. International Journal for Parasitology 25, 945970.CrossRefGoogle ScholarPubMed
Rohde, K. and Heap, M. (1998). Latitudinal differences in species and community richness and in community structure of metazoan endo- and ectoparasites of marine teleost fish. International Journal for Parasitology 28, 461474.CrossRefGoogle ScholarPubMed
Rojas, E., Pérez-Ponce de León, G. and García-Prieto, L. (1997). Helminth community structure of some freshwater fishes from Pátzcuaro, Michoacán, Mexico. Tropical Ecology 38, 121131.Google Scholar
Salgado-Maldonado, G. (2006). Checklist of helminth parasites of freshwater fishes from Mexico. Zootaxa 1324, 1357.CrossRefGoogle Scholar
Salgado-Maldonado, G., Aguilar-Aguilar, R., Cabañas-Carranza, G., Soto-Galera, E. Y. and Mendoza-Palmero, C. (2005). Helminth parasites in freshwater fish from the Papaloapan river basin, Mexico. Parasitology Research 96, 6989.CrossRefGoogle ScholarPubMed
Salgado-Maldonado, G. and Kennedy, C. R. (1997) Richness and similarity of helminth communities in the tropical cichlid fish Cichlasoma urophthalmus from the Yucatánatan Peninsula, Mexico. Parasitology 114, 581590.Google Scholar
Sánchez-Nava, P., Salgado-Maldonado, G., Soto-Galera, E. and Jaimes-Cruz, B. (2004). Helminth parasites of Girardinichthys multiradiatus (Pisces: Goodeidae) in the upper Lerma River sub-basin, Mexico. Parasitology Research 93, 396402.CrossRefGoogle ScholarPubMed
Sasal, P., Morand, S. and Guégan, J.-F. (1997). Parasite species richness for fish of the Mediterranean Sea. Marine Ecology Progress Series 149, 6171.CrossRefGoogle Scholar
Scholz, T., Aguirre-Macedo, M. L. and Salgado-Maldonado, G. (2001). Trematodes of the family Heterophyidae (Digenea) in Mexico: a review of species and new host and geographical records. Journal of Natural History 35, 17331772.CrossRefGoogle Scholar
Scholz, T., Vargas-Vázquez, J., Aguirre-Macedo, L. and Vidal-Martínez, V. M. (1997). Species of Ascocotyle Looss, 1899 (Digenea: Heterophyidae) of the Yucatan Peninsula, Mexico, and notes on their life-cycles. Systematic Parasitology 36, 161181.CrossRefGoogle Scholar
Schönhuth, S. and Doadrio, I. (2003). Phylogenetic relationships of Mexican minnows of the genus Notropis (Actinopterygii, Cyprinidae). Biological Journal of the Linnean Society 80, 323337.CrossRefGoogle Scholar
Schönhuth, S. and Mayden, R. L. (2010). Phylogenetic relationships in the genus Cyprinella (Actinopterygii: Cyprinidae) based on mitochondrial and nuclear gene sequences. Molecular Phylogenetics and Evolution 55, 7798. doi:10.1016/j.ympev.2009.10.030.CrossRefGoogle ScholarPubMed
Simková, A., Morand, S., Matejusová, I., Jurajda, P. and Gelnar, M. (2001). Local and regional influences on patterns of parasite species richness of central European fishes. Biodiversity and Conservation 10, 511525.CrossRefGoogle Scholar
Simons, A. M., Berendzen, P. B. and Mayden, R. L. (2003). Molecular systematics of North American phoxinin genera (Actinopterygii: Cyprinidae) inferred from mitochondrial 12S and 16S ribosomal RNA sequences. Zoological Journal of the Linnean Society 139, 6380.CrossRefGoogle Scholar
Takemoto, R. M., Pavanelli, G. C., Lizama, M. A. P., Luque, J. L. and 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
Vidal-Martínez, V. M. (1995). Processes structuring the helminth communities of native cichlid fishes from Southern Mexico. Ph.D. thesis, University of Exeter, Exeter, UK.Google Scholar
Vidal-Martínez, V. M., Aguirre-Macedo, M. L., Scholz, T., González-Solís, D. and Mendoza-Franco, E. F. (2001). Atlas of the Helminth Parasites of Cichlid Fish of Mexico. Academia, Praha, Czech Republic.Google Scholar
Walther, B. A. and Moore, J. L. (2005). The concepts of bias, precision and accuracy, and their use in the performance of species richness estimators, with a literature review of estimator performance. Ecography 28, 815829.CrossRefGoogle Scholar
Walther, B. A. and Morand, S. (1998). Comparative performance of species richness estimation methods. Parasitology 116, 395405.CrossRefGoogle ScholarPubMed
Wilcox, T. P., García de León, F. J., Hendrickson, D. A. and Hillis, D. M. (2004). Convergence among cave catfishes: long-branch attraction and a Bayesian relative rates test. Molecular Phylogenetics and Evolution 31, 11011113. doi:10.1016/j.ympev.2003.11.006.CrossRefGoogle Scholar