Acta Limnologica Brasiliensia
https://app.periodikos.com.br/journal/alb/article/doi/10.1590/S2179-975X10120
Acta Limnologica Brasiliensia
Original Article

Investigating the diversity of fish parasites in the floodplain of the upper Paraná River: a long-term ecological monitoring

Investigando a diversidade de parasitas de peixes da planície de inundação do alto rio Paraná: um monitoramento ecológico de longa duração

João Otávio Santos Silva; Atsler Luana Lehun; Aparecida de Fátima Cracco Rodrigues; Lidiany Doreto Cavalcanti; Danilo Nunes Nicola; Wagner Toshio Hasuike; Ricardo Massato Takemoto

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Abstract

Abstract:: Aim: The aim of this study was to present the description of new species of fish parasites in native and non-native hosts and the parasite interaction / host, available in studies for 37 years in the upper Paraná River floodplain.

Methods: The sampling described in this study is part of a scientometric methodology, in which specific query expressions were used, together with the database available in the Nupelia Sector Library, through Theses and Dissertations.

Results: A total of 44 species of parasites belonging to different groups were described for 27 species of fish of different orders. In these 37 years of studies, an increase 68% was observed in the number of parasite species, presenting a richness of 201 species in the floodplain, being: Monogenea, Digenea, Nematoda and Cestoda are the groups that present the largest records of species. More than 80 hosts have their parasite fauna registered and most studies are carried out with species of native hosts in the floodplain, being Prochilodus lineatus the host with the highest number of records.

Conclusions: Parasitological studies are an important scientific tool for understanding the dynamics of ecological interactions in the natural environment, and knowledge of this diversity of organisms is continuous and necessary, and the results of the monitoring carried out in the floodplain during the last 37 years only reinforce this with a constant increase in the description of new species and new records of parasite-host interactions. In times of constant environmental loss and habitat fragmentation, it is of utmost importance to care for and preserve floodplains to maintain biodiversity.

Keywords

ichthyoparasites, parasitism, biodiversity, ecological study

Resumo

Resumo: Objetivo: O objetivo deste estudo, foi apresentar a descrição de novas espécies de parasitos de peixe em hospedeiros nativos e não nativos, a interação parasito/hospedeiro, com dados disponibilizados de 37 anos de estudos na planície de inundação do alto rio Paraná.

Métodos: A amostragem descrita neste estudo faz parte de uma metodologia cienciométrica, na qual foram utilizadas expressões de consultas específicas, junto com o banco de dados disponíveis pela Biblioteca setorial do Nupelia, através de Teses e Dissertações.

Resultados: Ao todo, 44 espécies de parasitas pertencentes a diferentes grupos foram descritas para 27 espécies de peixes de diferentes ordens. Atualmente, registrou-se um aumento de 68% no número de espécies de parasitas, apresentando uma riqueza de 201 espécies na planície de inundação, sendo: Monogenea, Digenea, Nematoda e Cestoda os grupos que apresentam os maiores registros de espécies. Mais de 80 hospedeiros tem sua fauna parasitária registrada e maioria dos estudos são realizados com espécies de hospedeiros nativos da planície, sendo Prochilodus lineatus o hospedeiro com o maior número de registros.

Conclusões: Os estudos parasitológicos são uma ferramenta científica importante para entender a dinâmica das interações ecológicas em ambiente natural, e o conhecimento desta diversidade de organismos é contínuo e necessário, e os resultados do monitoramento realizado na planície durante os últimos 37 anos só reforçam isso com aumento constante de descrição de espécies novas e novos registros de interação parasito hospedeiro. Em tempos de perda constante de ambiente e fragmentação de habitats, é de extrema importância cuidar e preservar as planícies aluviais para manter a biodiversidade.
 

Palavras-chave

ictioparasitas, parasitismo, biodiversidade, estudo ecológico

Referencias

AFFONSO, I.D.P., KARLING, L.C., TAKEMOTO, R.M., GOMES, L.C. and NILSSON, P.A. Light-induced eye-fluke behavior enhances parasite life cycle. Frontiers in Ecology and the Environment, 2017, 15(6), 340-341. http://dx.doi.org/10.1002/fee.1513.

AGAPOW, P.M., BININDA-EMONDS, O.R., CRANDALL, K.A., GITTLEMAN, J.L., MACE, G.M., MARSHALL, J.C. and PURVIS, A. The impact of species concept on biodiversity studies. The Quarterly Review of Biology, 2004, 79(2), 161-179. http://dx.doi.org/10.1086/383542. PMid:15232950.

AGOSTINHO, A.A. and ZALEWSKI, M. A planície alagável do Alto Rio Paraná: importância e preservação. Maringá: EDUEM, 1996.

AGOSTINHO, A.A., GOMES, L.C., SANTOS, N.C., ORTEGA, J.C. and PELICICE, F.M. Fish assemblages in Neotropical reservoirs: Colonization patterns, impacts and management. Fisheries Research, 2016, 173(1), 26-36. http://dx.doi.org/10.1016/j.fishres.2015.04.006.

AGOSTINHO, A.A., GOMES, L.C., THOMAZ, S.M. and HAHN, N.S. The Upper Paraná River and its floodplain: main characteristics and perspectives for management and conservation. In: S.M. THOMAZ, A.A. AGOSTINHO and N.S. HAHN, eds. The Upper Paraná River and its floodplain: physical aspects, ecology and conservation. Leiden: Backhuys Publishers, 2004, pp. 381-393.

AGOSTINHO, A.A., PELICICE, F.M. and GOMES, L.C. Dams and the fish fauna of the Neotropical region: impacts and management related to diversity and fisheries. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2008, 68(4), 1119-1132, Supplement. http://dx.doi.org/10.1590/S1519-69842008000500019. PMid:19197482.

ARIA, M. and CUCCURULLO, C. bibliometrix: an R-tool for comprehensive science mapping analysis. Journal of Informetrics, 2017, 11(4), 959-975. http://dx.doi.org/10.1016/j.joi.2017.08.007.

AUDRY, S., SCHÄFER, J., BLANC, G. and JOUANNEAU, J.M. Fifty-year sedimentary record of heavy metal pollution (Cd, Zn, Cu, Pb) in the Lot River reservoirs (France). Environmental Pollution, 2004, 132(3), 413-426. http://dx.doi.org/10.1016/j.envpol.2004.05.025. PMid:15325457.

BELLAY, S., OLIVEIRA, E.F., ALMEIDA-NETO, M. and TAKEMOTO, R.M. Ectoparasites are more vulnerable to host extinction than co-occurring endoparasites: evidence from metazoan parasites of freshwater and marine fishes. Hydrobiologia, 2020, 847(13), 2873-2882. http://dx.doi.org/10.1007/s10750-020-04279-x.

BELLAY, S., OLIVEIRA, E.F., ALMEIDA-NETO, M., LIMA JUNIOR, D.P., TAKEMOTO, R.M. and LUQUE, J.L. Developmental stage of parasites influences the structure of fish-parasite networks. PLoS One, 2013, 8(10), e75710. http://dx.doi.org/10.1371/journal.pone.0075710. PMid:24124506.

BENEDITO, E., SANTANA, A.R.A. and WERTH, M. Divergence in energy sources for Prochilodus lineatus (Characiformes: Prochilodontidae) in Neotropical floodplains. Neotropical Ichthyology, 2018, 16(4), e160130. http://dx.doi.org/10.1590/1982-0224-20160130.

BREMER, K., BREMER, B., KARIS, P.O. and KÄLLERSJÖ, M. Time for change in taxonomy. Nature, 1990, 343(6255), 202. http://dx.doi.org/10.1038/343202a0. PMid:2300161.

BRITO, M.A., OLIVEIRA, D., MAMEDE, M.A., RANDIG, O. and LACERDA, F.S. Programa de pesquisa ecológica de longa duração – PELD/CNPq – desafios da gestão, avanços e perspectivas. Oecologia Australis, 2020, 24(2), 259-265. http://dx.doi.org/10.4257/oeco.2020.2402.02.

BROWN, S.P., RENAUD, F., GUÉGAN, J.F. and THOMAS, F. Evolution of trophic transmission in parasites: the need to reach a mating place? Journal of Evolutionary Biology, 2001, 14(5), 815-820. http://dx.doi.org/10.1046/j.1420-9101.2001.00318.x.

BUSH, A.O., FERNÁNDEZ, J.C., ESCH, G.W., SEED, J.R. and NDEZ, J.C.F. Parasitism: the diversity and ecology of animal parasites. Cambridge: Cambridge University Press, 2001, 566 p.

CASTRO, R. and VARI, R.P. Detritivores of the South American fish family Prochilodontidae (Teleostei: Ostariophysi: Characiformes): a phylogenetic and revisionary study. Smithsonian Contributions to Zoology, 2004, 74(3), 1-189. http://dx.doi.org/10.5479/si.00810282.622.

DAGA, V.S. and GUBIANI, É.A. Variations in the endemic fish assemblage of a global freshwater ecoregion: associations with introduced species in cascading reservoirs. Acta Oecologica, 2012, 41, 95-105. http://dx.doi.org/10.1016/j.actao.2012.04.005.

DOBSON, A., LAFFERTY, K.D., KURIS, A.M., HECHINGER, R.F. and JETZ, W. Homage to Linnaeus: how many parasites? How many hosts? Proceedings of the National Academy of Sciences of the United States of America, 2008, 105, 11482-11489, Supplement. http://dx.doi.org/10.1073/pnas.0803232105. PMid:18695218.

DUARTE, G.S.C., LEHUN, A.L., LEITE, L.A.R., CONSOLIN-FILHO, N., BELLAY, S. and TAKEMOTO, R.M. Acanthocephalans parasites of two Characiformes fishes as bioindicators of cadmium contamination in two neotropical rivers in Brazil. The Science of the Total Environment, 2020, 738, 140339. http://dx.doi.org/10.1016/j.scitotenv.2020.140339. PMid:32806342.

EIRAS, J.C., REGO, A.A. and PAVANELLI, G.C. Histopathology in Paulicea lutkeni (Pisces: Pimelodidae) resulting from infections with Megathylacus brooksi and Jauela glandicephalus (Cestoda: Proteocephalidae). Journal of Fish Biology, 1986, 28(3), 359-365. http://dx.doi.org/10.1111/j.1095-8649.1986.tb05172.x.

FRANCESCHINI, L., ZAGO, A.C., MÜLLER, M.I., FRANCISCO, C.J., TAKEMOTO, R.M. and SILVA, R.J. Morphology and molecular characterization of Demidospermus spirophallus n. sp., D. prolixus n. sp. (Monogenea: Dactylogyridae) and a redescription of D. anus in siluriform catfish from Brazil. Journal of Helminthology, 2018, 92(2), 228-243. http://dx.doi.org/10.1017/S0022149X17000256. PMid:28382887.

GARCIA, D.A.Z., VIDOTTO-MAGNONI, A.P. and ORSI, M.L. Características reprodutivas de peixes invasores no rio Paranapanema, bacia do alto rio Paraná, sul do Brasil. Neotropical Biology and Conservation, 2019, 14(4), 511-528. http://dx.doi.org/10.3897/neotropical.14.e49079.

GASQUES, L.S., FABRIN, T.M.C., PRIOLI, S.M.A.P. and PRIOLI, A.J. A introdução do gênero Cichla (BLOCK E SCHNEIDER, 1801) na planície de inundação do alto rio Paraná. Arquivos de Ciências Veterinárias e Zoologia da UNIPAR, 2014, 17(4), 261-266. http://dx.doi.org/10.25110/arqvet.v17i4.2014.5027.

GASQUES, L.S., GRAÇA, R.J., PRIOLI, S.M.A.P., TAKEMOTO, R.M. and PRIOLI, A.J. Molecular characterization of Urocleidoides cuiabai and U. malabaricusi (Monogenea: Dactylogyridae) from the trahira fish Hoplias aff. malabaricus in the Paraná River, Brazil. Journal of Helminthology, 2016, 90(6), 693-697. http://dx.doi.org/10.1017/S0022149X15000966. PMid:26603609.

GRAÇA, R.J., FABRIN, T.M., GASQUES, L.S., PRIOLI, S.M., BALBUENA, J.A., PRIOLI, A.J. and TAKEMOTO, R.M. Topological congruence between phylogenies of Anacanthorus spp. (Monogenea: Dactylogyridae) and their Characiformes (Actinopterygii) hosts: A case of host-parasite cospeciation. PLoS One, 2018, 13(3), e0193408. http://dx.doi.org/10.1371/journal.pone.0193408. PMid:29538463.

HAUSDORF, B. Progress toward a general species concept. Evolution; International Journal of Organic Evolution, 2011, 65(4), 923-931. http://dx.doi.org/10.1111/j.1558-5646.2011.01231.x. PMid:21463293.

JÚLIO JÚNIOR, H.F., DEI TÓS, C., AGOSTINHO, A.A. and PAVANELLI, C.S. A massive invasion of fish species after eliminating a natural barrier in the upper rio Paraná basin. Neotropical Ichthyology, 2009, 7(4), 709-718. http://dx.doi.org/10.1590/S1679-62252009000400021.

KADLEC, D., ŠIMKOVÁ, A., JARKOVSKÝ, J. and GELNAR, M. Parasite communities of freshwater fish under flood conditions. Parasitology Research, 2003, 89(4), 272-283. http://dx.doi.org/10.1007/s00436-002-0740-2. PMid:12632164.

KARLING, L.C., ISAAC, A., AFFONSO, I.P., TAKEMOTO, R.M. and PAVANELLI, G.C. The impact of a dam on the helminth fauna and health of a neotropical fish species Salminus brasiliensis (Cuvier 1816) from the upper Paraná River. Journal of Helminthology, 2013, 87(2), 245-251. http://dx.doi.org/10.1017/S0022149X1200034X. PMid:22776324.

KENNEDY, C.R. and BUSH, A.O. The relationship between pattern and scale in parasite communities: a stranger in a strange land. Parasitology, 1994, 109(2), 187-196. http://dx.doi.org/10.1017/S0031182000076290. PMid:8084664.

KENNEDY, C.R. The dynamics of intestinal helminth communities in eels Anguilla anguilla in a small stream: long-term changes in richness and structure. Parasitology, 1993, 107(1), 71-78. http://dx.doi.org/10.1017/S0031182000079427.

KENNEDY, C.R. The ecology of parasites of freshwater fishes: the search for patterns. Parasitology, 2009, 136(12), 1653-1662. http://dx.doi.org/10.1017/S0031182009005794. PMid:19366479.

LACERDA, A.C.F., BELLAY, S., TAKEMOTO, R.M. and PAVANELLI, G.C. Randomness of component communities of parasites of fish in a neotropical floodplain. Pan-American Journal of Aquatic Sciences, 2013, 8(1), 39-50.

LEHUN, A.L., DUARTE, G.S.C. and TAKEMOTO, R.M. Nematodes as indicators of environmental changes in a river with different levels of anthropogenic impact. Anais da Academia Brasileira de Ciências, forthcoming 2021.

LEHUN, A.L., HASUIKE, W.T., SILVA, J.O.S., CICCHETO, J.R.M., MICHELAN, G., RODRIGUES, A.F.C., NICOLA, D.N., LIMA, L.D., CORREIA, A.N. and TAKEMOTO, R.M. Checklist of parasites in fish from the upper Paraná River floodplain: an update. Revista Brasileira de Parasitologia Veterinária, 2020, 29(3), e008720. http://dx.doi.org/10.1590/s1984-29612020066. PMid:32935771.

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

LIZAMA, M.L., TAKEMOTO, R.M. and PAVANELLI, G.C. 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, 2005, 12(4), 299-304. http://dx.doi.org/10.1051/parasite/2005124299. PMid:16402561.

NICOLA, D.N., AFFONSO, I.P. and TAKEMOTO, R.M. Behavioral changes in host foraging: Experiments with Clinostomum (Trematoda, Digenea) parasitizing Loricariichtys platymetopon (Loricariidae). Experimental Parasitology, 2020, 216, 107916. http://dx.doi.org/10.1016/j.exppara.2020.107916. PMid:32590020.

ORSI, M.L. and AGOSTINHO, A.A. Introdução de espécies de peixes por escapes acidentais de tanques de cultivo em rios da Bacia do Rio Paraná, Brasil. Revista Brasileira de Zoologia, 1999, 16(2), 557-560. http://dx.doi.org/10.1590/S0101-81751999000200020.

OTA, R.R., DEPRA, G.C., GRAÇA, W.J. and PAVANELLI, C.S. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes: revised, annotated and updated. Neotropical Ichthyology, 2018, 16(2). http://dx.doi.org/10.1590/1982-0224-20170094.

PADILLA, D.K. and WILLIAMS, S.L. Beyond ballast water: aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Frontiers in Ecology and the Environment, 2004, 2(3), 131-138. http://dx.doi.org/10.1890/1540-9295(2004)002[0131:BBWAAO]2.0.CO;2.

PARISELLE, A., BOEGER, W.A., SNOEKS, J., BILONG BILONG, C.F., MORAND, S. and VANHOVE, M.P. The monogenean parasite fauna of cichlids: a potential tool for host biogeography. International Journal of Evolutionary Biology, 2011, 2011, 471480. http://dx.doi.org/10.4061/2011/471480. PMid:21869935.

PAVANELLI, G.C., MACHADO, M.H. and TAKEMOTO, R.M. Fauna helmíntica de peixes do rio Paraná, região de Porto Rico, Paraná. In: A.E.A.M. VAZZOLER, A.A. AGOSTINHO and N.S. HAHN, eds. A planície de inundação do Alto rio Paraná. Maringá: EDUEM/Nupélia, 1997, pp. 307-329.

PAVANELLI, G.C., TAKEMOTO, R.M. and EIRAS, J.C. Parasitologia de peixes de água doce do Brasil. Maringá: Eduem, 2013.

PELICICE, F.M. and AGOSTINHO, A.A. Fish fauna destruction after the introduction of a non-native predator (Cichla kelberi) in a Neotropical reservoir. Biological Invasions, 2009, 11(8), 1789-1801. http://dx.doi.org/10.1007/s10530-008-9358-3.

PINEDA, A., PAULA, A., IATSKIU, P., MORESCO, G., SOUZA, Y., ORTEGA, L., ZANON, F., ZANCO, B., JATI, S., BORTOLINI, J. and RODRIGUES, L. Uma área de proteção em uma planície subtropical influencia a diversidade taxonômica e funcional do fitoplâncton. Oecologia Australis, 2020, 24(2), 505-523. http://dx.doi.org/10.4257/oeco.2020.2402.19.

POULIN, R. Determinants of host-specificity in parasites of freshwater fishes. International Journal for Parasitology, 1992, 22(6), 753-758. http://dx.doi.org/10.1016/0020-7519(92)90124-4. PMid:1428509.

POULIN, R. Variation in infection parameters among populations within parasite species: intrinsic properties versus local factors. International Journal for Parasitology, 2006, 36(8), 877-885. http://dx.doi.org/10.1016/j.ijpara.2006.02.021. PMid:16620823.

POULIN, R., PRESSWELL, B. and JORGE, F. The state of fish parasite discovery and taxonomy: a critical assessment and a look forward. International Journal for Parasitology, 2020, 50(10-11), 733-742. http://dx.doi.org/10.1016/j.ijpara.2019.12.009. PMid:32151615.

PURVIS, A. and HECTOR, A. Getting the measure of biodiversity. Nature, 2000, 405(6783), 212-219. http://dx.doi.org/10.1038/35012221. PMid:10821281.

QUINATTO, J., ZAMBELLI, N.L.D.N., SOUZA, D.H., RAFAELI NETO, S.L., CARDOSO, J.T. and SKORONSKI, E. Using the pollutant load concept to assess water quality in an urban river: the case of Carahá River (Lages, Brazil). Revista Ambiente & Água, 2018, 14(1), 2-11. http://dx.doi.org/10.4136/ambi-agua.2252.

R CORE TEAM. R: a language and environment for statistical computing [online]. Vienna: R Foundation for Statistical Computing, 2016 [viewed 20 Oct. 2020]. Available from: https://www.R-project.org/

REGO, A.A. and PAVANELLI, G.C. Jauela glandicephalus gen. n., sp.n. e Megathylacus brooksi sp. n., cestóides proteocefalideos patogênicos para o jaú, Paulicea lutkeni, peixe pimelodideo. Revista Brasileira de Biologia, 1985, 45(4), 643-652.

RIBEIRO, V.R., SILVA, P.R.L., GUBIANI, É.A., FARIA, L., DAGA, V.S. and VITULE, J.R.S. Imminent threat of the predator fish invasion Salminus brasiliensis in a Neotropical ecoregion: eco-vandalism masked as an environmental project. Perspectives in Ecology and Conservation, 2017, 15(2), 132-135. http://dx.doi.org/10.1016/j.pecon.2017.03.004.

SCHOLZ, T., TAKEMOTO, R.M. and KUCHTA, R. First freshwater bothriocephalidean (Cestoda) from tropical South America, closely related to African taxa. The Journal of Parasitology, 2017, 103(6), 747-755. http://dx.doi.org/10.1645/17-23. PMid:28727503.

SYMSTAD, A.J., CHAPIN, F.S., WALL, D.H., GROSS, K.L., HUENNEKE, L.F., MITTELBACH, G.G., PETERS, D.P.C. and TILMAN, D. Long-term and large-scale perspectives on the relationship between biodiversity and ecosystem functioning. Bioscience, 2003, 53(1), 89-98. http://dx.doi.org/10.1641/0006-3568(2003)053[0089:LTALSP]2.0.CO;2.

TAKEMOTO, R.M., LIZAMA, M.A.P., GUIDELLI, G.M. and PAVANELLI, G.C. Parasitos de peixes de águas continentais. In: M.J.T. RANZANI-PAIVA, R.M. TAKEMOTO and M.A.P. LIZAMA, eds. Sanidade de organismos aquáticos. São Paulo: Livraria Varela, 2004, pp. 179-198.

TAKEMOTO, R.M., PAVANELLI, G.C., LIZAMA, M.A.P., LACERDA, A.C.F., YAMADA, F.H., MOREIRA, L.H.A., CESCHINI, T.L. and BELLAY, S. Diversity of parasites of fish from the Upper Paraná River floodplain, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2009, 69(2), 691-705, Supplement. http://dx.doi.org/10.1590/S1519-69842009000300023. PMid:19738975.

THOMAZ, S.M., BINI, L.M. and BOZELLI, R.L. Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia, 2007, 579(1), 1-13. http://dx.doi.org/10.1007/s10750-006-0285-y.

THOMAZ, S.M., PAGIORO, T.A., BINI, L.M., ROBERTO, M.C. and ROCHA, R.R.A. Limnological characterization of the aquatic environments and the influence of hydrometric levels. In: S.M. THOMAZ, A.A. AGOSTINHO and N.S. HAHN, eds. The upper Paraná River and its floodplain: physical aspects, ecology and conservation. Leiden: Backhuys Publishers, 2004, pp. 75–102.

VITULE, J.R.S., BORNATOWSKI, H., FREIRE, C.A. and ABILHOA, V. Extralimital introductions of Salminus brasiliensis (Cuvier, 1816) (Teleostei, Characidae) for sport fishing purposes: a growing challenge for the conservation of biodiversity in neotropical aquatic ecosystems. BioInvasions Records, 2014, 3(4), 291-296. http://dx.doi.org/10.3391/bir.2014.3.4.11.

VITULE, J.R.S., FREIRE, C.A. and SIMBERLOFF, D. Introduction of non‐native freshwater fish can certainly be bad. Fish and Fisheries, 2009, 10(1), 98-108. http://dx.doi.org/10.1111/j.1467-2979.2008.00312.x.

VITULE, J.R.S., SKÓRA, F. and ABILHOA, V. Homogenization of freshwater fish faunas after the elimination of a natural barrier by a dam in Neotropics. Diversity & Distributions, 2012, 18(2), 111-120. http://dx.doi.org/10.1111/j.1472-4642.2011.00821.x.

WICKHAM, H. ggplot2: elegant graphics for data analysis [online]. New York: Springer-Verlag, 2016 [viewed 17 Mar. 2015]. Available from: https://ggplot2.tidyverse.org

YAMADA, P.D.O.F., YAMADA, F.H., SILVA, R.J. and ANJOS, L.A. Ecological implications of floods on the parasite communities of two freshwater catfishes in a Neotropical floodplain. Acta Parasitologica, 2017, 62(2), 312-318. http://dx.doi.org/10.1515/ap-2017-0039. PMid:28426419.
 


Submitted date:
20/10/2020

Accepted date:
17/08/2021

Publication date:
16/09/2021

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