Acanthocephalans are obligate endoparasites characterised by the presence of a proboscis with hooks, which are used to adhere and perforate the intestinal wall of their hosts. Individuals of Echinorhynchus salobrensis Machado Filho, 1948 have been reported parasitising the piranhas Serrasalmus maculatus Kner and Serrasalmus marginatus Valenciennes in the upper Paraná River floodplain. Serrasalmus marginatus is considered non-native at this site, and its establishment occurred after the closure of the Itaipu Hydroelectric, which flooded a natural geographic barrier that separated two ecoregions in the Paraná River. Since they are phylogenetically close and have similar biological and ecological characteristics competition for resources caused the non-native species to become dominant over the native one. Considering the specificity of species of Echinorhynchus Zoega, 1776 in serrasalmids, we evaluated the distribution of E. salobrensis along the gastrointestinal tract of S. maculatus and S. marginatus from the upper Paraná River floodplain. All parasites indices of E. salobrensis were higher in the invasive host S. marginatus when compared to the native S. maculatus. There were no significant interaction effects between host species and sex, and host species and/or sex in the presence of the parasite. When we evaluated the effect of E. salobrensis parasitism on the different gut regions and accessory organs, total abundance was significant in the stomach and caecum organs, and in the first and second regions of the intestine. None of the analytical approaches tested showed an effect of the sex of the host or the sex of the parasite on the presence and abundance of the parasite in the gastrointestinal tract. Studies on acanthocephalan parasitism in fish in Brazil focus on fish farm. The fact that two species of selvage carnivorous fish present high rates of acanthocephalan parasitism, added to the fact that most studies with this group are on farmed fish fed with feed, only emphasise the need for continuity in studies of acanthocephalans in the parasitology of aquatic organisms.

Programa de Pos graduacao em Biologia Comparada Laboratorio de Ictioparasitologia Universidade Estadual de Maringa UEM Maringa Parana Brazil

Programa de Pos graduacao em Ecologia de Ambientes Aquaticos Continentais Laboratorio de Ictioparasitologia Universidade Estadual de Maringa UEM Maringa Parana Brazil

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Agostinho A.A., Pelicice F.M., Gomes L.C., Júlio Jr. H.F. 2010: Reservoir fish stocking: when one plus one may be less than two. Nat. Conserv. 8: 103-111. DOI

Agostinho C.S., Hahn N.S., Marques E.E. 2003: Patterns of food resource use by two congeneric species of piranhas (Serrasalmus) on the upper Paraná River floodplain. Braz. J. Biol. 63: 177-182. DOI

Agostinho C.S., Júlio Jr. H.F. 2002: Observation of an invasion of the piranha Serrasalmus marginatus Valenciennes, 1847 (Osteichthyes, Serrasalmidae) into the Upper Paraná River, Brazil. Acta Sci. Biol. Sci. 24: 391-395.

Agostinho A.A., Julio H.F., Petrere M. 1994: Itaipu reservoir (Brazil): impacts of impoundments on the fish fauna and fisheries. In: I.G. Cowx (Ed.), Rehabilitation of Freshwater Fisheries. Osney Mead, Oxford, pp. 171-184.

Aguiar L.S., de Oliveira M.I.B., de Matos L.V., Gomes A.L.S., da Costa J.I., da Silva G.S. 2018: Distribution of the acanthocephalan Neoechinorhynchus buttnerae and semiquantitative analysis of histopathological damage in the intestine of tambaqui (Colossoma macropomum). Parasitol. Res. 117: 1689-1698. DOI

Alexandre P.C., Luiz E.A., Piana P.A., Gomes L.C., Agostinho A.A. 2004: Relação estoque-recrutamento para as piranhas Serrasalmus marginatus (Valenciennes, 1847) e S. maculatus (Kner, 1860) no rio Baía, alto rio Paraná. Acta Sci. Biol. Sci. 26: 303-307. DOI

Almeida V.L.L., Hahn N.S., Agostinho, C.S. 1998: Stomach content of juvenile and adult piranhas (Serrasalmus marginatus) in the Paraná Floodplains, Brazil. Stud. Neotrop. Fauna Environ. 33: 100-105. DOI

Alves G.H.Z., Figueiredo B.R., Manetta G.I., Sacramento P.A., Tófoli R.M., Benedito E. 2017: Trophic segregation underlies the coexistence of two piranha species after the removal of a geographic barrier. Hydrobiologia 797: 57-68. DOI

Alves J.C., Andreotti G.F., Agostinho A.A., Gomes, L.C. 2021: Effects of the El Niño Southern Oscillation (ENSO) on fish assemblages in a Neotropical floodplain. Hydrobiologia 848: 1811-1823. DOI

Amin O.M. 1987: Key to the families and subfamilies of Acanthocephala, with the erection of a new class (Polyacanthocephala) and a new order (Polyacanthorhynchida). J. Parasitol. 1216-1219. DOI

Bates D., Maechler M., Bolker B., Walker S., Christensen R.H.B., Singmann H., Dai B., Scheipl F., Grothendieck G., Green P. 2009: Package 'lme4'. URL http://lme4. r-forge. r-project. org.

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: 575-583. DOI

Casali G.P., Takemoto R.M. 2016: Endoparasitic fauna of Serrasalmus spp. (Characidae: Serrasalminae) in a neotropical floodplain. Acta Sci. Biol. Sci. 38: 105-112. DOI

Combes C. 2001: Parasitism: the Ecology and Evolution of Intimate Interactions. University of Chicago Press, Chicago, 728 pp.

Duarte G.S.C., Lehun A.L., Leite L.A.R., Consolin-Filho N., Bellay S., Takemoto R.M. 2020: Acanthocephalans parasites of two Characiformes fishes as bioindicators of cadmium contamination in two neotropical rivers in Brazil. Sci. Total Environ. 738: 140339. DOI

Eiras J.C., Takemoto R.M., Pavanelli G.C. 2006: Métodos de Estudo e Técnicas Laboratoriais em Parasitologia de Peixes. Eduem, Maringá, 199 pp.

Fox J., Weisberg S., Adler D., Bates D., Baud-Bovy G., Ellison, S., Heiberger R. 2017: Package 'car'. R Foundation for Statistical Computing.

García-Berthou E., Moreno-Amich R. 1993: Multivariate analysis of covariance in morphometric studies of the reproductive cycle. Can. J. Fish. Aquat. Sci. 50: 1394-1399. DOI

Gouveia E.J., Cavalcanti L.D., Russo M.R. 2020: Echinorhynchus gomesi Machado Filho, 1948 infecting the Patinga hybrid (x2640; Piaractus mesopotamicus×♂ Piaractus brachypomus) in fish farms in Mato Grosso do Sul, Brazil. Aquac. Res. 51: 5118-5124. DOI

Gouveia É.J., Cavalcanti L.D., Takemoto R.M. 2021: Acanthocephalans parasites in farmed fish in Brazil: a review. Aquac. Res. 52: 5990-5999. DOI

Grey A. J., Hayunga E. G. 1980: Evidence for alternative site selection by Glaridacris laruei (Cestoidea: Caryophyllidea) as a result of inter- specific competition. J. Parasitol. 66: 371-372. DOI

Hahn N.S., Fugi R., Andrian I.F. 2004: Trophic ecology of the fish assemblages. In: S.M. Thomaz, A.A. Agostinho and N.S. Hahn (Eds.), The Upper Paraná River and its Floodplain: Physical Aspects, Ecology and Conservation. Backhuys Publishers, Leiden, pp.247-269.

Hothorn T., Bretz F., Westfall P. 2008: Simultaneous inference in general parametric models. Biom. J. 50: 346-363. DOI

Jerônimo G.T., de Pádua S.B., de Andrade Belo M.A., Chagas E.C., Taboga S.R., Maciel P.O., Martins M.L. 2017: Neoechinorhynchus buttnerae (Acanthocephala) infection in farmed Colossoma macropomum: a pathological approach. Aquaculture 469: 124-127. DOI

Kassambara A., Kassambara M.A. 2020: Package 'ggpubr'. R package version 0.1, 6, 0.

Kennedy C.R. 2006: Ecology of the Acanthocephala. Cambrid University Press, Cambridge, 249 pp. DOI

Krogdahl A., Hemre G.I., Mommsen T.P. 2005: Carbohydrates in fish nutrition: digestion and absorption in postlarval stages. Aquac. Nutr. 11: 103-122. DOI

Krogdahl A., Sundby A., Bakke A.M. 2011: Gut secretion and digestion In: A.P. Farrell (Ed.), Encyclopedia of Fish Physiology: From Genome to Environment. Academic Press, Cambridge, pp. 1301-1310. DOI

Lehun A.L., Hasuike W.T., Silva J.O.S., Ciccheto J.R.M., Michelan G., Rodrigues A.F.C., Nicola D.N., Duarte-Lima L., Correia A.N., Takemoto R.M. 2020: Checklist of parasites in fish from the upper Paraná River floodplain: an update. Braz. J. Vet. Parasitol. 29: e008720. DOI

Lehun A.L., Silva J.O.S., Michelan G., Lansac-Tôha F.M., Cavalcanti L.D., Takemoto R.M. 2023: The occurrence of trophically transmitted parasites is influenced by the trophic level and body size of the fish host. Ecol. Freshw. Fish. 32: 648-655. DOI

Lenth R.V. 2016: Least-squares means: the R package lsmeans. J. Stat. Softw. 69: 1-33. DOI

Machado Filho D. A. 1948: "Echinorhynchidae" do Brasil. I. Three new species of "Echinorhynchus" Zoega in Mueller, 1776 and redescription of Echinorhynchus jucundus Travassos, 1923." Rev. Bras. Biol. 8.2: 265-273.

Near T. J. 2002: Acanthocephalan phylogeny and the evolution of parasitism. Integr. Comp. Biol. 42: 668-677. DOI

Nunes B.R.C., de Andrade Lopes Y.V., de Souza R.H.B., Pazdiora R.D., Ushizima T.T., Medeiros S.P., Corrêa L.T., Cardoso I.I., Andrade M.V.V., Maciel-Honda P.O., Chaga E.C., Alexandre Sebastião, F. 2023: Treatments for the control of Neoechinorhynchus buttnerae (Acanthocephala) in tambaqui Colossoma macropomum. Aquac. Int. 31: 1821-1835. DOI

Odum E.P. 2012: Ecologia. Guanabara Koogan, Rio de Janeiro, 468 pp.

Oksanen J., Blanchet F.G., Kindt R., Legendre P., Minchin P.R., O'hara R.B., Simpson G.L., Solymos P., Stevens M.H., Wagner H., Oksanen M.J. 2019: Package 'vegan'.Community ecology package, version 2 (9). The R foundation for statistical computing.

Ota R.R., Deprá G.D.C., Graça W.J.D., Pavanelli C.S. 2018: Peixes da planície de inundação do alto rio Paraná e áreas adjacentes: revised, annotated and updated. Neotrop. Ichthyol. 16: e170094. DOI

Poulin R. 1996: Sexual inequalities in helminth infections: a cost of being a male? Am. Nat. 147: 287-295. DOI

Poulin R. 1997: Population abundance and sex ratio in dioecious helminth parasites. Oecologia 111: 375-380. DOI

R Core Team 2021: R: A language and environment for statistical computing.

Richardson D.J., Martens J.K., Nickol B.B. 1997: Copulation and sexual congress of Leptorhynchoides thecatus (Acanthocephala). J. Parasitol. 83: 542-543. DOI

Ripley B., Venables B., Bates D.M., Hornik K., Gebhardt A., Firth D., Ripley M.B. 2013: Package 'mass'. Cran R. 538: 113-120.

Robinson H.A., Barger M.A. 2007: Microhabitat specificity of Paulisentis missouriensis (Acanthocephala) in creek chub (Semotilus atromaculatus) in southeastern Nebraska, USA. Comp. Parasitol. 74: 355-358. DOI

Rodrigues A.C., de Santana H.S., Baumgartner M.T., Gomes L.C. 2018: Coexistence between native and nonnative species: the invasion process and adjustments in distribution through time for congeneric piranhas in a Neotropical floodplain. Hydrobiologia 817: 279-291. DOI

Rodrigues A.C., Santos N.C.L.D., Baumgartner M.T., Gomes L.C. 2021: Adjustments in population and reproductive dynamics of native and non-native congeneric species during 26 years after invasion. Neotrop. Ichthyol. 19: e200033. DOI

Santos C.P., Gibson D.I., Tavares L.E., Luque, J.L. 2008: Checklist of Acanthocephala associated with the fishes of Brazil. Zootaxa 1938: 1-22. DOI

Santos C.P., Machado P.M., dos Santos E.G.N. 2013: Regulação parasitária e ecossistemas dulcícolas. In: G.C. Pavanelli, R.M. Takemoto and J.C. Eiras (Eds.), Parasitologia de Peixes de água doce do Brasil. Eduem, Maringá, pp. 353-370.

Schmidt H., Mauer K., Hankeln T., Herlyn H. 2022: Host-dependent impairment of parasite development and reproduction in the acanthocephalan model. Cell Biosci. 12: 75. DOI

Starling J.A. 1985: Feeding, nutrition and metabolism. In: D.W.T. Crompton and B.B. Nickol (Eds.), Biology of the Acanthocephala. University Press, Cambridge, pp. 125-212.

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. Braz. J. Biol. 69 (Suppl 2.): 691-705. DOI

Taraschewski H. 2000: Host-parasite interactions in Acanthocephala: a morphological approach. Adv. Parasitol. 46: 1-179. DOI

Wickham H. 2016: Ggplot2. Springer, Cham, 260 pp. DOI

Wickham H., François R., Henry L., Müller K., Wickham M.H. 2020: Package 'dplyr'. A Grammar of Data Manipulation. R package version, 8.

Yamaguti S. 1959: Studies on the helminth fauna of Japan. Part 55. Four new genera of Acanthocephala from fishes. Publ. Seto Mar. Biol. Lab. 7: 319-326. DOI

Zuk M., McKean K.A. 1996: Sex differences in parasite infections: patterns and processes. Int. J. Parasitol. 26: 1009-1024. DOI