Acta Limnologica Brasiliensia
https://actalb.org/article/doi/10.1590/S2179-975X4123
Acta Limnologica Brasiliensia
Original Article

Fish parasites from a neotropical tidal river within a biodiversity hotspot

Parasitos de peixes de um rio costeiro neotropical dentro de um hotspot de biodiversidade

Luddy Searom Carias de Moraes; Ana Paula Lula Costa; Ricardo Massato Takemoto; Andre Andrian Padial

Downloads: 0
Views: 103

Abstract

Aim: We investigated the ichthyofauna parasite component community across a gradient of anthropogenic pressures of the Guaraguaçu River, south Brazil, a Neotropical river of central importance for biodiversity conservation.

Methods: After fish sampling, all fish were identified, measured, weighed and eviscerated. The viscera and gills were inspected for parasite screening and subsequent identification. Parasite diversity estimators were calculated for the most abundant host species.

Results: A total of 159 host specimens from 12 species were examined, being 140 (88.05%) found to be infected with at least one parasite, including 14 new parasite occurrences. The most widely distributed parasite was the nematode Contracaecum sp., found in 8 host species. The highest mean infection intensity and mean abundance was observed for the monogenean Aphanoblastella mastigatus, infecting the Silver catfish Rhamdia quelen. The Shannon-Wiener, Jost and Simpson indexes were higher for the more abundant fishes, except for the Trahira Hoplias malabaricus. Most host species harbored parasites in poorly aggregated distribution, according to the discrepancy index. The Berger-Parker index showed monogenean dominance in all hosts except for H. malabaricus. We found little evidence for parasite infracommunity changes across the gradient of the river.

Conclusions: We described the infection patterns in an important Neotropical river. The new parasite occurrences highlight the contribution of our study. Fish-parasite interactions changed throughout the river stretches, and we argue that it does not necessarily means changes in diversity and abundance of parasite within species, but the rearrange of interactions. Moreover, it seems that parasites are more abundant in most impacted sites, another reason to continue the monitoring.

Keywords

neotropical tidal river, parasite community, biodiversity conservation, host species, anthropogenic pressures

Resumo

Objetivo: A comunidade componente de parasitas da ictiofauna foi investigada ao longo de um gradiente de pressões antropogênicas no Rio Guaraguaçu, sul do Brasil, um rio Neotropical com grande importância para a conservação da biodiversidade.

Métodos: Após a coleta, todos os peixes foram identificados, medidos, pesados e eviscerados. As vísceras e brânquias foram inspecionadas para coleta e subsequente identificação de parasitas. Estimadores de diversidade de parasitas foram calculados para as espécies de hospedeiros mais abundantes.

Resultados: Um total de 159 espécimes de hospedeiros de 12 espécies foram examinados, sendo 140 (88,05%) infectados com pelo menos um parasita, incluindo 14 novas ocorrências de parasitas. O parasita mais amplamente distribuído foi o nematoide Contracaecum sp., encontrado em 8 espécies de hospedeiros. As maiores intensidades de infecção e abundância foram observadas para o monogenético Aphanoblastella mastigatus, infectando o Jundiá Rhamdia quelen. Os índices de Shannon-Wiener, Jost e Simpson foram maiores para os peixes mais abundantes, exceto para a Traíra Hoplias malabaricus. A maioria das espécies de hospedeiros abrigava parasitas com distribuição pouco agregada, de acordo com o índice de discrepância. O índice de Berger-Parker mostrou a dominância de monogenéticos em todos os hospedeiros, exceto H. malabaricus. Encontramos poucas evidências de mudanças nas infracomunidades de parasitas ao longo do gradiente do rio.

Conclusões: Descrevemos os padrões de infecção em um importante rio Neotropical. As novas ocorrências de parasitas destacam a importância de nosso estudo. Interações entre parasitos e peixes mudaram ao longo dos setores do rio, e isso não necessariamente resulta em mudanças na diversidade e abundância de parasitos dentro de cada espécie, mas um rearranjo das interações. Além disso, parece que os parasitas são mais abundantes na maioria dos locais impactados, o que é mais uma razão para continuar o monitoramento.

Palavras-chave

rio neotropical de maré, comunidade parasitária, conservação de biodiversidade, espécie hospedeira, pressão antropogênica

References

Abelha, M.C.F., & Goulart, E., 2004. Oportunismo trófico de Geophagus brasiliensis (Quoy & Gaimard, 1824) (Osteichthyes, Cichlidae) no reservatório de Capivari, Estrado o Paraná, Brasil. Acta Sci. Biol. Sci. 26(1), 37-45. http://dx.doi.org/10.4025/actascibiolsci.v26i1.1657.

Abell, R., Thieme, M.L., Revenga, C., Bryer, M., Kottelat, M., Bogutskaya, N., Coad, B., Mandrak, N., Contreras Balderas, S., Bussing, W., Stiassny, M.L.J., Skelton, P., Allen, G.R., Unmack, P., Naseka, A., Ng, R., Sindorf, N., Robertson, J., Armijo, E., Higgins, J.V., Heibel, T.J., Wikramanayake, E., Olson, D., López, H.L., Reis, R.E., Lundberg, J.G., Pérez, M.H.S., & Petry, P., 2008. Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. Bioscience 58(5), 403-414. http://dx.doi.org/10.1641/B580507.

Acosta, A.A., Smit, N.J., & Silva, R.J., 2020. Diversity of helminth parasites of eight siluriform fishes from the Aguapeí River, upper Paraná basin, São Paulo state, Brazil. Int. J. Parasitol. Parasites Wildl. 11, 120-128. PMid:32025487. http://dx.doi.org/10.1016/j.ijppaw.2020.01.003.

Amin, O.M., Heckmann, R.A., Inchausty, V., & Vasquez, R., 1996. Immature Polyacanthorhynchus rhopalorhynchus (Acanthocephala: Polyacanthorhynchidae) in Venton, Hoplias malabaricus (Pisces) from Moca Vie River, Bolivia, with notes on its apical organ and histopathology. J. Helminthol. Soc. Wash. 63(1), 115-119.

Anderson, M.J., 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32-46.

Anderson, R.C., 2000. Nemotode parasites of vertebrates, their development and transmission. Wallingford: CAB International, 2 ed. http://dx.doi.org/10.1079/9780851994215.0000.

Araújo, E.S., Vitule, J.R.S., & Padial, A.A., 2021. A checklist of aquatic macrophytes of the Guaraguaçu river basin reveals a target for conservation in the Atlantic rainforest. Acta Sci. Biol. Sci. 43(1), e50542. http://dx.doi.org/10.4025/actascibiolsci.v43i1.50542.

Argolo, L.A., López-Fernández, H., Batalha-Filho, H., & Affonso, P.R.A.M., 2020. Unraveling the systematics and evolution of the ‘Geophagus’ brasiliensis (Cichliformes: Cichlidae) species complex. Mol. Phylogenet. Evol. 150, 106855. PMid:32442518. http://dx.doi.org/10.1016/j.ympev.2020.106855.

Azevedo, R.K., Abdallah, V.D., & Luque, J.L., 2010. Acanthocephala, Annelida, Arthropoda, Myxozoa, Nematoda and Platylminthes parasites of fishes from the Guandu river, Rio de Janeiro, Brazil. Check List 6(4), 659-667. http://dx.doi.org/10.15560/6.4.659.

Berger, W.H., & Parker, F.L., 1970. Diversity of planktonic foraminifera in deep-sea sediments. Science 168(3937), 1345-1347. http://dx.doi.org/10.1126/science.168.3937.1345.

Brasil. Ministério do Meio Ambiente – MMA, 2003. Evaluation of the state of knowledge on biological diversity in Brazil: executive summary. National Biological Diversity Strategy Project. Brasilia: MMA.

Brooks, D.R., & Hoberg, E.P., 2001. Parasite systematics in the 21st century: opportunities and obstacles. Trends Parasitol. 17(6), 273-275. PMid:11378033. http://dx.doi.org/10.1016/S1471-4922(01)01894-3.

Budria, A., 2017. Beyond troubled waters: the influence of eutrophication on host–parasite interactions. Funct. Ecol. 31(7), 1348-1358. http://dx.doi.org/10.1111/1365-2435.12880.

Bush, A.O., Lafferty, K.D., Lotz, J.M., & Shostak, A.W., 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol. 83(4), 575-583. PMid:9267395. http://dx.doi.org/10.2307/3284227.

Casatti, L., 2002. Alimentação dos peixes em um riacho do parque estadual Morro do Diabo, bacia do alto do rio Paraná, sudeste do Brasil. Biota Neotrop. 2(2), 1-14. http://dx.doi.org/10.1590/S1676-06032002000200012.

Castañeda, L., Carvajal, H., & Vélez, I., 2003. Alguns trematodos digenéticos de peces marinos de Charambirá (Chocó, Colombia). Actual. Biol. 25(75), 147-155. http://dx.doi.org/10.17533/udea.acbi.329495.

Costa, A.P.L., Bascompte, J., & Padial, A.A., 2023. Modularity in host-parasite mixed networks: interaction configuration shifts based on human perturbation and parasitism form. Int. J. Parasitol. 53(10), 585-594. PMid:37328044. http://dx.doi.org/10.1016/j.ijpara.2023.04.004.

Crompton, D.W.T., & Nickol, B.B., 1985. Biology of Acanthocephala. New York: Cambridge University Press.

Dias, A.C.M.I., Castelo Branco, C.W., & Lopes, V.G., 2005. Estudo da dieta natural de peixes no reservatório de Ribeirão das Lajes, Rio de Janeiro, Brasil. Acta Sci. Biol. Sci. 27(4), 335-364. http://dx.doi.org/10.4025/actascibiolsci.v27i4.1270.

Dobson, A., Lafferty, K.D., Kuris, A.M., Hechinger, R.F., & Jetz, W., 2008. Homage to Linnaeus: how many parasites? How many hosts? Proc. Natl. Acad. Sci. USA 105(Suppl 1), 11482-11489. PMid:18695218. http://dx.doi.org/10.1073/pnas.0803232105.

Domingues, M.V., & Fehlauer, K.H., 2006. New species of Chauhanellus (Monogenoidea, Platyhelminthes) from the gills of Southern Atlantic marine catfishes (Siluriformes, Ariidae) of the Neotropical region. Zootaxa 1365(1), 61-68. http://dx.doi.org/10.11646/zootaxa.1365.1.5.

Domingues, M.V., Soares, G.B., & Watanabe, A., 2016. Monogenoidea (Polyonchoinea: Dactylogyridae) parasitizing the gills of marine catfish (Siluriformes: Ariidae) inhabiting the Atlantic Amazon Coast of Brazil. Zootaxa 4127(2), 301-326. PMid:27395625. http://dx.doi.org/10.11646/zootaxa.4127.2.4.

Dudgeon, D., 2019. Multiple threats imperil freshwater biodiversity in the Anthropocene. Curr. Biol. 29(19), R960-R967. PMid:31593677. http://dx.doi.org/10.1016/j.cub.2019.08.002.

Eiras, J.C., Takemoto, R.M., & Pavanelli, G.C., 2006. Métodos de estudo e técnicas laboratoriais em parasitologia de peixes. Maringá: EDUEM.

Galvanese, E.F., Costa, A.P.L., Araújo, E.S., Falkievicz, B.C., Melo, G.G.V., Vitule, J.R.S., & Padial, A.A., 2022. Community stability and seasonal biotic homogenization emphasize the effect of the invasive tropical tanner grass on macrphytes from a highly dynamic neotropical tidal river. Aquat. Sci. 84(2), 30. PMid:35400976. http://dx.doi.org/10.1007/s00027-022-00858-3.

Gomiero, L.M., Souza, U.P., & Braga, F.M.S., 2007. Reprodução e alimentação de Rhamdia quelen (Quoy & Gaimard, 1824) em rios do Núcleo Santa Virgínia, Parque Estadual da Serra do Mar, São Paulo, SP. Biota Neotrop. 7(3), 127-133. http://dx.doi.org/10.1590/S1676-06032007000300015.

Gouveia, E.J., Cavalcanti, L.D., Leal, F.C., Mendes, S.G.F., & Russo, M.R., 2021. Trophic relationship between the Patinga hybrid (Piaractus mesopotamicus x Piaractus brachypomus) and Echinorhynchus gomsei Machado Filho, 1948 in fish farms. J. Fish Biol. 98(3), 874-877. PMid:33112421. http://dx.doi.org/10.1111/jfb.14600.

Gower, J.C., 1966. Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53(3-4), 325-338. http://dx.doi.org/10.1093/biomet/53.3-4.325.

Guidelli, G.M., Isaac, A., Takemoto, R.M., & Pavanelli, G.C., 2003. Endoparasite infracommunities of Hemisorubim platyrhynchos (Valenciennes, 1840) (Pisces: Pimelodidae) of the Baia River, upper Parana River floodplain, Brazil: specific composition and ecological aspects. Braz. J. Biol. 63(2), 261-268. PMid:14509848. http://dx.doi.org/10.1590/S1519-69842003000200011.

Instituto Chico Mendes de Conservação da Biodiversidade – ICMBio (Online), 2023. Brasília. Retrieved in 2023, May 2, from https://www.gov.br/icmbio/

Kennedy, C.R. 2006. Ecology of the Acanthocephala. New York: Cambridge University Press. http://dx.doi.org/10.1017/CBO9780511541902

Kohn, A., Cohen, S.C., & Salgado-Maldonado, G., 2006. Checklist of monogenea parasites of freshwater and marine fishes, amphibians and reptiles from Mexico, central America and Caribbean. Zootaxa 1289(1), 1-114. https://doi.org/10.11646/zootaxa.1289.1.1.

Kohn, A., Fernandes, B.M., & Cohen, S.C., 2007. South American trematodes parasites of fishes. São Paulo: CNPq.

Lafferty, K.D., 2012. Biodiversity loss decreases parasite diversity: theory and patterns. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367(1604), 2814-2827. PMid:22966137. http://dx.doi.org/10.1098/rstb.2012.0110.

Lefebvre, F., & Poulin, R., 2005. Life history constraints on the evolution of abbreviated life cycles in parasitic trematodes. J. Helminthol. 79(1), 47-53. PMid:15831113. http://dx.doi.org/10.1079/JOH2004273.

Lima, L.B., Bellay, S., Giacomini, H.C., Isaac, A., & Lima-Junior, D.P., 2016. Influence of host diet and phylogeny on parasite sharing by fish in a diverse tropical floodplain. Parasitology 143(3), 343-349. PMid:26647725. http://dx.doi.org/10.1017/S003118201500164X.

Luque, J.L., & Poulin, R., 2007. Metazoan parasite species richness in neotropical fishes: hotspots and the geography of biodiversity. Parasitology 134(Pt 6), 865-878. PMid:17291392. http://dx.doi.org/10.1017/S0031182007002272.

Luque, J.L., Pereira, F.B., Alves, P.V., Oliva, M.E., & Timi, J.T., 2017. Helminth parasites of South American fishes: current status and characterization as a model for studies of biodiversity. J. Helminthol. Online 91(2), 150. PMid:27855726. http://dx.doi.org/10.1017/S0022149X16000717.

Marcogliese, D.J., & Cone, D.K., 1997. Food webs: a plea for parasites. Trends Ecol. Evol. 12(8), 320-325. PMid:21238094. http://dx.doi.org/10.1016/S0169-5347(97)01080-X.

Marcogliese, D.J., 2003. Food webs and biodiversity: are parasites the missing link. J. Parasitol. 89(6), 106-113.

Marcogliese, D.J., 2005. Parasites of the superorganism: are they indicators of ecosystem health? Int. J. Parasitol. 35(7), 705-716. PMid:15925594. http://dx.doi.org/10.1016/j.ijpara.2005.01.015.

Mello, F.T., Iglesias, C., Borthagaray, A.I., Mazzeo, N., Vilches, J., Larrea, D., & Ballabio, R., 2006. Ontogenetic Allometric Coefficient Changes: implications of diet shift and morphometric traits in Hoplias malabaricus (Bloch) (Characiforme, Erythrinidae). J. Fish Biol. 69(6), 1770-1778. http://dx.doi.org/10.1111/j.1095-8649.2006.01245.x.

Meschiatti, A.J., & Arcifa, M.S., 2002. Early life stages of fish and the relationships with zooplankton in a tropical Brazilian reservoir: Lake Monte Alegre. Braz. J. Biol. 62(1), 41-50. http://dx.doi.org/10.1590/S1519-69842002000100006.

Miller, T.L., & Cribb, T.H., 2008. Family Cryptogonimidae Ward, 1917. In: Bray, R.A., Gibson, D.I., & Jones, A., eds. Keys to the Trematoda. Wallingford: CABI Publishing, 51-112, vol. 3.

Minchella, D., & Scott, M.E., 1991. Parasitism: a cryptic determinant of animal Community structure. Trends Ecol. Evol. 6(8), 250-254. PMid:21232471. http://dx.doi.org/10.1016/0169-5347(91)90071-5.

Morand, S., 2000. Wormy world: comparative tests of theoretical hypotheses on parasite species richness. In: Poulin, R., Morand, S., & Skorping, A., eds. Evolutionary biology of host-parasite relationships: theory meets reality. Amsterdam: Elsevier Science, 63-79.

Moravec, F., 1998. Nematodes of freshwater fishes of the neotropical region. Praha: Academia.

Myers, N., Mittermeier, R.A., Mittermeier, C.G., Fonseca, G.A.B., & Kent, J., 2000. Biodiversity hotspots for conservation priorities. Nature 403(6772), 853-858. PMid:10706275. http://dx.doi.org/10.1038/35002501.

Nadler, S.A., & Pérez-Ponce, L.G., 2011. Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology 138(13), 1688-1709. PMid:21281559. http://dx.doi.org/10.1017/S003118201000168X.

Negrelli, D.C., Iannacone, J., Abdallah, V.D., & Azevedo, R.K., 2021. Qualitative and quantitative study of parasites of Pimelodus maculatus and Rhamdia quelen from the Jacaré-Pepira River, state of São Paulo, Brazil. An. Acad. Bras. Cienc. 93(2), e20190571. http://dx.doi.org/10.1590/0001-3765202120190571.

Novaes, J.L.C., & Carvalho, E.D., 2011. Population structure and stock assessment of Hoplias malabaricus (Characiformes: Erythrinidae) caught by artisanal fishermen in river reservoir transition area in Brazil. Rev. Biol. Trop. 59(1), 71-83. PMid:21513193. http://dx.doi.org/10.15517/rbt.v59i1.3179.

Núñez, M.O., & Pertierra, A.A.G., 1991. The life history of Acanthostomum gnerii Szidat, 1954 (Trematoda: Acanthostomatidae), from the catfish Rhamdia sapo in Argentina. Zool. Anz. 227, 58-71.

Occhi, T.V.T., 2020. Biological invasions and its effect on biodiversity [Tese de doutorado em Ecologia e Conservação]. Curitiba: Universidade Federal do Paraná.

Paraná, 12 set. 2016. Decreto Estadual nº 4.996, de 5 de setembro de 2016. Dispõe sobre o Regulamento que define o documento técnico científico Zoneamento Ecológico-Econômico do Litoral Paranaense - ZEE PR - Litoral. Diário Oficial do Estado do Paraná (Online), Curitiba, PR. Retrieved in 2023, August 16, from https://www.iat.pr.gov.br/Pagina/Zoneamento-Ecologico-Economico-ZEE

Poulin, R., & Morand, S., 2004. Parasite biodiversity. Washington, DC: Smithsonian Books.

Poulin, R., 1992. Determinants of host-specificity in parasites of freshwater fishes. Int. J. Parasitol. 22(6), 753-758. PMid:1428509. http://dx.doi.org/10.1016/0020-7519(92)90124-4.

Poulin, R., 1993. The disparity between observed and uniform distributions: a new look at parasite aggregation. Int. J. Parasitol. 23(7), 937-944. PMid:8106186. http://dx.doi.org/10.1016/0020-7519(93)90060-C.

Poulin, R., 1995. Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecol. Monogr. 65(3), 283-302. http://dx.doi.org/10.2307/2937061.

Poulin, R., 1997. Species richness of parasite assemblages: evolution and patterns. Annu. Rev. Ecol. Syst. 28(1), 341-358. http://dx.doi.org/10.1146/annurev.ecolsys.28.1.341.

Poulin, R., 2011. Uneven distribution of cryptic diversity among higher taxa of parasitic worms. Biol. Lett. 7(2), 241-244. PMid:20861036. http://dx.doi.org/10.1098/rsbl.2010.0640.

Poulin, R., 2014. Parasite biodiversity revisited: frontiers and constraints. Int. J. Parasitol. Online 44(9), 581-589. PMid:24607559. http://dx.doi.org/10.1016/j.ijpara.2014.02.003.

Poulin, R., 2016. Greater diversification of freshwater then marine parasites of fish. Int. J. Parasitol. Online 46(4), 275-279. PMid:26802461. http://dx.doi.org/10.1016/j.ijpara.2015.12.002.

Price, P.W., 1980. Evolutionary biology of parasites. Princeton: Princeton University Press.

Rassier, G.L., Pesenti, T.C., Pereira Júnior, J., Silva, D.S., Wndt, E.W., Monteiro, C.M., & Berne, M.E.A., 2015. Metazoan parasites of Geophagus brasiliensis (Perciformes: Cichlidae) in Patos lagoon extreme South Brazil. Rev. Bras. Parasitol. Vet. 24(4), 447-453. PMid:26648010. http://dx.doi.org/10.1590/S1984-29612015075.

Reiczigel, J., Marozzi, M., Fábián, I., & Rózsa, L., 2019. Biostatistics for parasitologists: a primer to quantitative parasitology. Trends Parasitol. 35(4), 277-281. PMid:30713051. http://dx.doi.org/10.1016/j.pt.2019.01.003.

Reis, R.E., 2013. Conserving the freshwater fishes of South America. Int. Zoo Yearb. 47(1), 65-70. http://dx.doi.org/10.1111/izy.12000.

Rohde, K., 2005. Marine Parasitology. Wallingford, UK: CABI Publishing.

Saad, A.I., Younis, A.E., & Rabei, J.M., 2018. Experimental Life Cylce of Contracaecum quadripapillatum n. sp. in White Pelican (Pelecanus erythrorhynchus) at Lake Nasser, Egypt: morphological and genetic evidences. J. Egypt. Soc. Parasitol. 48(3), 587-598. http://dx.doi.org/10.21608/jesp.2018.76569.

Sato, R.Y., Costa, A.P.L., & Padial, A.A., 2021. The invasive tropical tanner grass decreases diversity of the native aquatic macrophyte community as two scales in a subtropical tidal river. Acta Bot. Bras. 35(1), 140-150. http://dx.doi.org/10.1590/0102-33062020abb0360.

Shamsi, S., 2019. Parasite loss or parasite gain? Story of Contracaecum nematodes in antipodean waters. Parasite Epidemiol. Control 4, e00087. PMid:30766927. http://dx.doi.org/10.1016/j.parepi.2019.e00087.

Simões, S.B.E., Neves, R.F.C., & Santos, C.P., 2008. Life history of Acanthocollaritrema umbilicatum Travassos, Freitas and Bührnheim, 1965 (Digenea: cryptogonimidae). Parasitol. Res. 103(3), 523-528. PMid:18500539. http://dx.doi.org/10.1007/s00436-008-1000-x.

Studer, A., Thieltges, D., & Poulin, R., 2010. Parasites and global warming: net effects of temperature on an intertidal host-parasite system. Mar. Ecol. Prog. Ser. 415, 11-22. http://dx.doi.org/10.3354/meps08742.

Sures, B., Nachev, M., Selbach, C., & Marcogliese, D.J., 2017. Parasite responses to pollution: what we know and where we go in ‘Environmental Parasitology’. Parasit. Vectors 10(1), 65. PMid:28166838. http://dx.doi.org/10.1186/s13071-017-2001-3.

Thatcher, V.E., & Boeger, W.A., 1984a. The parasitic crustaceans from the Brazilian Amazon. 15. Gamispatulus schizodontis gen. et sp. nov. (copepoda: Poecilostomatoida: Vaigamidae) from the nasal fossae of Schizodon fasciatus AGASSIZ. Amazoniana. Limnologia Oecol. Regionalis Systematis Fluminis Amazonas 9(1), 119-126.

Thatcher, V.E., & Boeger, W.A., 1984b. The parasitic crustaceans of fishes from the Brazilian Amazon. 13. Gamidactylus jaraquensis gen. et sp. nov. (copepoda: Poecilostomatoida: Vaigamidae) from the nasal fossae of Semaprochilodus insignis (schomburgk). Amazoniana. Limnologia Oecol. Regionalis Systematis Fluminis Amazonas 8, 421-426.

Thatcher, V.E., & Varella, A.B., 1981. Duas novas espécies de Megacoelium szidat, 1954 (trematoda: Heploporidae), parasitas estomacais de peixes da amazônia brasileira, com uma redefinição do gênero. Acta Amazon. 11(2), 285-289. http://dx.doi.org/10.1590/1809-43921981112285.

Thatcher, V.E., 2006. Amazon fish parasites. Sofia: Pensoft Publishers, vol. 1.

Torres, R., Valdiverso, J., Schaltter, R., Montefusco, A., Revenga, J., Marin, F., Lamilla, J., & Ramalto, G., 2000. Infection by Contracaecum rudolphii (Nematoda: Anisakidae) in the Neotropical Cormorant Phalacrocorax brasilianus, and fishes from the estuary of the Valdinavia river, Chile. Stud. Neotrop. Fauna Environ. 35(2), 101-108. http://dx.doi.org/10.1076/0165-0521(200008)35:2;1-9;FT101.

United Nations Educational, Scientific and Cultural Organization – UNESCO, 1999. WHC nomination documentation (Online). Paris. Retrieved in 2023, August 16, from https://whc.unesco.org/uploads/nominations/893rev.pdf

Universidade Federal do Paraná – UFPR. Laboratório de Análise e Síntese em Biodiversidade, 2023a. Projeto Guaraguacu (Online). Curitiba. Retrieved in 2023, May 2, from https://lasbufprbio.wixsite.com/home/projeto-guaraguacu

Universidade Federal do Paraná – UFPR. Laboratório de Análise e Síntese em Biodiversidade, 2023b. Dados de pesquisa disponíveis (Online). Curitiba. Retrieved in 2023, May 2, from https://lasbufprbio.wixsite.com/home/dados

Vicente, J.J., Pinto, R.M., Noronha, D., & Gonçalves, L., 1995. Nematode parasites of Brazilian Ciconiiformes birds: a general survey with new records for the species. Mem. Inst. Oswaldo Cruz 90(3), 389-393. http://dx.doi.org/10.1590/S0074-02761995000300014.

Winemiller, K.O., 1989. Ontogenetic diet shifts and resource partitioning among piscivorous fishes in the Venezuelan ilanos. Environ. Biol. Fishes 26(3), 177-199. http://dx.doi.org/10.1007/BF00004815.
 


Submitted date:
05/02/2023

Accepted date:
03/04/2024

Publication date:
03/19/2024

65f9cd40a953954ef20d5d72 alb Articles
Links & Downloads

Acta Limnol. Bras. (Online)

Share this page
Page Sections