Parasites and diet of Serrasalmus maculatus in a hydroelectric reservoir in Brazil

Parasitos e dieta de Serrasalmus maculatus em um reservatório no Brasil

Bianca da Silva Miguel Lidiane Franceschini Letícia de Oliveira Manoel Bruna Caroline Kotz Kliemann Rosilene Luciana Delariva Igor Paiva Ramos About the authors

Abstract

Serrasalmus maculatus is a species of piranha which, despite being abundant in a reservoir environment, has few studies related to its parasitological and diet aspects. Thus, we aimed to document the parasitic fauna and diet of the S. maculatus in a hydroelectric reservoir in Brazil. In addition, we perform two literature reviews for the Neotropical region, recording the parasitic fauna already associated with S. maculatus and the occurrence of parasite genera identified in this study parasitizing Characiformes from other aquatic systems. Thirty-one hosts were collected with gillnets, from August 2014 to September 2016. Serrasalmus maculatus had a piscivorous feeding habit and a low richness parasitic component community, including two taxa of monogeneans, Anacanthorus lepyrophallus and Mymarothecium sp.; no endohelminths were observed. Data from the literature review, together with the findings of the study, showed that S. maculatus in the Neotropical region harbors 25 helminth taxa, with the monogenean being the most prevalent parasitic group and Brazil is the country with the most reports of the parasitic genera. These findings provide information on the relationships between diet, social behavior, and parasitic fauna of S. maculatus and on the patterns of distribution and infection of the observed parasite rates.

Keywords:
Ectoparasites; Anacanthorus; Mymarothecium; freshwater fish; piranha

Resumo

Serrasalmus maculatus é uma espécie de piranha que, a despeito de ser abundante em ambiente de reservatório, possui poucas informações sobre seus aspectos parasitológicos e dieta. Assim, o presente estudo objetivou documentar a fauna parasitária e a dieta de S. maculatus em um reservatório brasileiro. Além disso, foram realizadas duas revisões literárias para a região Neotropical, registrando a fauna parasitária, já associada a S. maculatus e a ocorrência dos gêneros parasitários identificados neste estudo, registrados em outros peixes Characiformes em outros sistemas aquáticos. Foram coletados 31 hospedeiros com redes de espera entre agosto de 2014 e setembro de 2016. Serrasalmus maculatus apresentou hábito alimentar piscívoro e comunidade componente parasitária com baixa riqueza, incluindo dois táxons de monogenéticos, Anacanthorus lepyrophallus e Mymarothecium sp.; não foram observados endohelmintos. Dados da revisão da literatura, juntamente com os achados deste estudo, mostraram que S. maculatus, na região Neotropical, abriga 25 táxons de helmintos, sendo monogenéticos o grupo de parasitos mais prevalente, e o Brasil o país com mais relatos de parasitos. Estes resultados fornecem informações sobre as relações entre dieta, o comportamento social e a fauna parasitária de S. maculatus e sobre os padrões de distribuição e infecção das taxas de parasitos observadas.

Palavras-chave:
Ectoparasitos; Anacanthorus; Mymarothecium; peixe de água doce; piranha

Introduction

Parasites can influence local communities by affecting host physiology, morphology, reproduction, and behaviour, thereby affecting population, community, and ecosystem structures, and host behaviours (e.g., feeding habits and predator-prey relationships) in turn, can affect the structures of parasite communities (Timi & Poulin, 2020Timi JT, Poulin R. Why ignoring parasites in fish ecology is a mistake. Int J Parasitol 2020; 50(10-11): 755-761. http://dx.doi.org/10.1016/j.ijpara.2020.04.007. PMid:32592807.
http://dx.doi.org/10.1016/j.ijpara.2020....
). However, even though the ecological relevance of parasitism is widely recognised, many studies have neglected the effects of these organisms on their hosts (Timi & Poulin, 2020Timi JT, Poulin R. Why ignoring parasites in fish ecology is a mistake. Int J Parasitol 2020; 50(10-11): 755-761. http://dx.doi.org/10.1016/j.ijpara.2020.04.007. PMid:32592807.
http://dx.doi.org/10.1016/j.ijpara.2020....
). For example, even though Brazil harbours a megadiverse freshwater ichthyofauna (~3500 species) (Froese & Pauly, 2020aFroese R, Pauly D. List of Freshwater Fishes reported from Brazil [online]. FishBase; 2020a [cited 2020 Aug 26]. Available from: https://www.fishbase.de/Country/CountryChecklist.php?c_code=076&vhabitat=fresh⫏_code=&cpresence=present
https://www.fishbase.de/Country/CountryC...
), the parasitology of only 13% of the region’s species has been evaluated, of which the majority are economically important species. Nevertheles little is known about the parasitology of fish species with low commercial importance (Eiras et al., 2010Eiras JC, Takemoto RM, Pavanelli GC. Diversidade de peixes de água doce do Brasil. Maringa: Eduem; 2010., 2011Eiras JC, Takemoto RM, Pavanelli GC, Adriano EA. About the biodiversity of parasites of freshwater fish from Brazil. Bull Eur Assoc Fish Pathol 2011; 31(4): 161-168.).

The piranha, or pirambeba, Serrasalmus maculatus (Kner, 1858) is a medium-sized freshwater fish belonging to Characiformes, that is widely distributed in South America, throughout both the Amazon and Paraguay-Paraná River basins (Froese & Pauly, 2020bFroese R, Pauly D. Serrasalmus maculatus Kner, 1858. [online]. FishBase; 2020b [cited 2020 Aug 26]. Available from: https://www.fishbase.de/summary/serrasalmus-maculatus.html
https://www.fishbase.de/summary/serrasal...
). The species is piscivorous, preferentially consuming fish musculature, fins, and scales. Eventually, invertebrates are the speciesmost common prey (Agostinho & Marques, 2001Agostinho CS, Marques EE. Selection of netted prey by piranhas, Serrasalmus spilopleura and S. marginatus (Pisces, Serrasalmidae). Acta Sci Biol Sci 2001; 23(2): 461-464.; Agostinho et al., 2003Agostinho CS, Hahn NS, Marques EE. Patterns of food resource use by two congeneric species of piranhas (Serrasalmus) on the Upper Paraná River floodplain. Braz J Biol 2003; 63(2): 177-182. http://dx.doi.org/10.1590/S1519-69842003000200002. PMid:14509839.
http://dx.doi.org/10.1590/S1519-69842003...
; Villares et al., 2008Villares GA, Gomiero LM, Goitein R. Feeding of Serrasalmus maculatus (Kner, 1858) (Characiformes; Serrasalmidae) in the Sorocaba river, São Paulo State, Brazil. Acta Sci Biol Sci 2008; 30(3): 267-273. http://dx.doi.org/10.4025/actascibiolsci.v30i3.5011.
http://dx.doi.org/10.4025/actascibiolsci...
). It is also generally gregarious and, although has low economic importance, is one of the most abundant species in hydroelectric reservoirs, because readily adapts to artificial lentic environments (Sazima & Machado, 1990Sazima I, Machado FA. Underwater observations of piranhas in western Brazil. Environ Biol Fishes 1990; 28(1-4): 17-31. http://dx.doi.org/10.1007/BF00751026.
http://dx.doi.org/10.1007/BF00751026...
; Hoffmann et al., 2005Hoffmann AC, Orsi ML, Shibatta AO. Diversidade de peixes do reservatório da UHE Escola Engenharia Mackenzie (Capivara), Rio Paranapanema, bacia do alto rio Paraná, Brasil, e a importância dos grandes tributários na sua manutenção. Iheringia Ser Zool 2005; 95(3): 319-325. http://dx.doi.org/10.1590/S0073-47212005000300012.
http://dx.doi.org/10.1590/S0073-47212005...
; Behr & Signor, 2008Behr ER, Signor CA. Distribuição e alimentação de duas espécies simpátricas de piranhas Serrasalmus maculatus e Pygocentrus nattereri (Characidae, Serrasalminae) do rio Ibicuí, Rio Grande do Sul, Brasil. Iheringia Ser Zool 2008; 98(4): 501-507. http://dx.doi.org/10.1590/S0073-47212008000400014.
http://dx.doi.org/10.1590/S0073-47212008...
). Despite the abundance of S. maculatus in hydroelectric reservoirs, there are few studies on its parasitological aspects.

Most studies of the parasitology of S. maculatus have focused on populations in the Upper Paraná River floodplain region (Pavanelli et al., 1997Pavanelli GC, Machado MH, Takemoto RM. Fauna helmíntica de peixes do rio Paraná, região de Porto Rico, Paraná. In: Vazzoler AEAM, Agostinho AA, Hahn NS, editors. A Planície de inundação do Alto rio Paraná: aspectos físicos, biológicos e socioeconômicos. Maringá: Eduem; 1997. p. 307-329., 2004Pavanelli GC, Machado MH, Takemoto RM, Guidelli GM, Lizama MAP. Helminth fauna of fishes: diversity and ecological aspects. In: Thomaz SM, Agostinho AA, Hahn NS, editors. The Upper Paraná river and its Floodplain: physical aspects, ecology and conservation. Leiden: Backhuys Publishers; 2004. p. 309-329.; Takemoto et al., 2009Takemoto RM, Pavanelli GC, Lizama MAP, Lacerda ACF, Yamada FH, Moreira LHA, et al. Diversity of parasites of fish from the Upper Paraná River floodplain, Brazil. Braz J Biol 2009;69(2 Suppl 2): 691-705. http://dx.doi.org/10.1590/S1519-69842009000300023. PMid:19738975.
http://dx.doi.org/10.1590/S1519-69842009...
; Casali & Takemoto, 2016Casali GP, Takemoto RM. Endoparasitic fauna of Serrasalmus spp. (Characidae: Serrasalminae) in a neotropical floodplain. Acta Sci Biol Sci 2016; 38(1): 105-112. http://dx.doi.org/10.4025/actascibiolsci.v38i1.28592.
http://dx.doi.org/10.4025/actascibiolsci...
; Moreira et al., 2019Moreira J, da Silva Carneiro J, Ruz EJH, Luque JL. New Species and Records of Anacanthorus (Monogenea: Dactylogyridae) Parasitizing serrasalmid fish (Characiformes) from Brazil, including molecular data. Acta Parasitol 2019; 64(3): 449-455. http://dx.doi.org/10.2478/s11686-019-00055-7. PMid:31020494.
http://dx.doi.org/10.2478/s11686-019-000...
), and few studies have examined this species ecology or parasitology in artificial environments. In addition, considering the diet is an important factor in host-parasite interactions and hosts with more diverse diets tend to be more susceptible to endoparasite infections (Lima et al., 2016Lima LB, Bellay S, Giacomini HC, Isaac A, Lima-Junior DP. 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.
http://dx.doi.org/10.1017/S0031182015001...
), we aimed (i) document the parasitic fauna and (ii) characterize the diet of S. maculatus in a hydroelectric reservoir in Brazil. We targeted also (iii) to verify the parasite fauna already associated with S. maculatus in the Neotropical region; and (iv) the occurrence of parasite genera - identified in the present study - in characiform fishes from other aquatic systems (natural or artificial) in the Neotropical region.

Material and Methods

Study area

The Ilha Solteira hydroelectric reservoir is an accumulation basin that was formed in 1978 and is situated along the Upper Paraná River, between the states of São Paulo, Minas Gerais, and Mato Grosso do Sul, Brazil (Figure 1). With a mean depth of 17.6 m, maximum volume of21.06 × 109 m3, hydrographic basin area of 1195 km2, and residence time of 46.7 days, it is one of the largest artificial reservoirs in the neotropics (Garcia et al., 2014Garcia F, Kimpara JM, Valenti WC, Ambrosio LA. Emergy assessment of tilapia cage farming in a hydroelectric reservoir. Ecol Eng 2014; 68: 72-79. http://dx.doi.org/10.1016/j.ecoleng.2014.03.076.
http://dx.doi.org/10.1016/j.ecoleng.2014...
). For the present study, host sampling was conducted in the Can-Can arm in municipality of Santa Clara D’Oeste, São Paulo state, Brazil (50° 55ʹ 59.65″ W and 20° 02ʹ 30.54″ S).

Figure 1
Study area on Ilha Solteira hydroelectric reservoir, Upper Paraná River basin, São Paulo state, Brazil (Campos et al., 2020Campos DWJ, Manoel LO, Franceschini L, Veríssimo-Silveira R, Delariva RL, Ribeiro CS, et al. Occurrence of metacercariae of Austrodiplostomum compactum (Lutz, 1928) (Trematoda, Diplostomidae) in Pimelodus platicirris in the Ilha Solteira Reservoir, São Paulo, Brazil. An Acad Bras Cienc 2020;92(Suppl 2):e20180649. http://dx.doi.org/10.1590/0001-3765202020180649.
http://dx.doi.org/10.1590/0001-376520202...
).

Host sampling

Serrasalmus maculatus specimens were collected using gill nets (3, 4, 5, 6, 7, 8, 10, 12 and 14 cm between non-adjacent nodes) between August 2014 to September 2016 (authorization SISBio nº 42229-1). The collected specimens were euthanized (Authorization CEUA/FEIS nº 001/2014 and Certified SisGen A9038DB) and identified as described by Ota et al. (2018)Ota RR, Deprá GC, Graça WJ, Pavanelli CS. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes: revised, annotated and updated. Neotrop Ichthyol 2018; 16(2): e170094. http://dx.doi.org/10.1590/1982-0224-20170094.
http://dx.doi.org/10.1590/1982-0224-2017...
. The total weight (g, with viscera) and standard length (cm, from snout to last vertebra) of each specimen were recorded, and the fish were subsequently individually stored in plastic bags, frozen and sent to the laboratory for additional analyses. All measurements are expressed as the mean ± standard deviation followed by the range.

Parasitological procedures

The organs (skin, fins, nasal cavities, gills, eyes, heart, liver, gonads, intestines, swim bladder, spleen, gallbladder, and mesentery) were analysed for parasitological procedures, using a stereomicroscope, and parasites preserved in 70% ethanol or mounted on semipermanent slides using Gray and Wess medium. The parasite specimens were then subject to morphological analysis, using a computerised image analysis system with differential interference contrast (DIC) - LAS V3 (Leica Application Suite V3; Leica Microsystems, Wetzlar, Germany) and identified according to Kritsky et al. (1992)Kritsky DC, Boeger WA, Van Every LR. Neotropical Monogenoidea. 17. Anacanthorus Mizelle and Price, 1965 (Dactylogyridae, Anacanthorinae) from Characoid Fishes of the Central Amazon. J Helminthol Soc Wash 1992; 59(1): 25-51. and Kritsky et al. (1996)Kritsky DC, Boeger WA, Jégu M. Neotropical Monogenoidea. 28. Ancyrocephalinae (Dactylogyridae) of piranha and their relatives (Teleostei, Serrasalmidae) from Brazil and French Guiana: Species of Notozothecium Boeger and Kritsky, 1988, and Mymarothecium gen. n. J Helminthol Soc Wash 1996; 63(1): 153-175.. Parasite prevalence (P, in percentage), mean intensity of infestation (MII), and mean abundance (MA) were then calculated according to Bush et al. (1997)Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. http://dx.doi.org/10.2307/3284227. PMid:9267395.
http://dx.doi.org/10.2307/3284227...
. Mean intensity of infestation and mean abundance are expressed as the mean ± standard error followed by the range.

The host and parasite voucher specimens were deposited in the Fish Collection of São Paulo State University (UNESP), Campus of São José do Rio Preto, São Paulo state, Brazil (DZSJRP 21374), and the Helminthological Collection of the Institute of Bioscience, Section of Parasitology, UNESP, Campus of Botucatu, São Paulo state, Brazil, (Mymarothecium sp. - CHIBB 652 L‒655 L; Anacanthorus lepyrophallus - CHIBB 656 L‒663 L), respectively.

Literature review

Two literature reviews were conducted to verify the parasite fauna already associated with S. maculatus in the Neotropical region; and to verify the occurrence of parasite genera - identified in the present study - in characiform fishes from other aquatic systems (natural or artificial) in the Neotropical region. In the first review, we collected data on the helminth fauna previously reported for S. maculatus and its synonymy (= Serrasalmus spilopleura Kner, 1860) from the Neotropical region, from the first report in 1997 to 2021. In the second review, we collected data regarding the occurrence of monogenean species belonging to Anacanthorus and Mymarothecium genera in S. maculatus, as well as in other characiforms from the Neotropical region, from the first report of each genus (1965 to 2021 for Anacanthorus, and 1996 to 2021 for Mymarothecium).

The literature reviews were performed by searching relevant databases (SciELO, ISI, Scopus, Google Scholar, and WoRMS) for relevant terms: Serrasalmus, piranha, pirambeba, fish parasite, helminth, Monogenea, Dactylogyridae, Gyrodactylidae, Nematoda, Cestoda, Acanthocephala, Trematoda, Digenea, digenetic, digenean, monogenetic, monogenean, cestode, acanthocephalan, Anacanthorus, and Mymarothecium. All common names were searched using both singular and plural forms in English, Portuguese, and Spanish.

Diet analysis

The stomachs of the host specimens were removed, fixed in 4% formaldehyde, and preserved in 70% alcohol, and stomach contents were analysed using an optical stereomicroscope. Recovered food items were quantified using the volumetric method (displacement of each measured food item from stomach contents using a gridded Petri dish) (Hyslop, 1980Hyslop EJ. Stomach contents analysis – a review of methods and their application. J Fish Biol 1980; 17(4): 411-429. http://dx.doi.org/10.1111/j.1095-8649.1980.tb02775.x.
http://dx.doi.org/10.1111/j.1095-8649.19...
). Glass slides were used to compress food items to 1.0 mm in height, and the number of quadrants occupied by each food item was multiplied by 0.001 to calculate the volume in ml (Hellawell & Abel, 1971Hellawell JM, Abel R. A rapid volumetric method for the analysis of the food fishes. J Fish Biol 1971; 3(1): 20-37. http://dx.doi.org/10.1111/j.1095-8649.1971.tb05903.x.
http://dx.doi.org/10.1111/j.1095-8649.19...
). All food items were identified to lowest possible taxonomic (Bicudo & Bicudo, 1970Bicudo CEM, Bicudo RMT. Algas de águas continentais brasileiras chave ilustrada para identificação de gêneros. São Paulo: Fundação Brasileira para o Desenvolvimento do Ensino de Ciências; 1970.; Mugnai et al., 2010Mugnai R, Nessemian JL, Baptista DF. Manual de identificação de macroinvertebrados aquáticos do Estado do Rio de Janeiro. Rio de Janeiro: Technical Books Editora; 2010.; Ota et al., 2018Ota RR, Deprá GC, Graça WJ, Pavanelli CS. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes: revised, annotated and updated. Neotrop Ichthyol 2018; 16(2): e170094. http://dx.doi.org/10.1590/1982-0224-20170094.
http://dx.doi.org/10.1590/1982-0224-2017...
).

Results

The weight and standard length of the 31 S. maculatus specimens ranged from 32.24 to 650.40 g (139.95 ± 24.42 g) and from 9.5 to 24.0 cm (14.44 ± 0.53), respectively.

The richness of the S. maculatus component parasite community was low and included two monogenean ectoparasites from gills, belonging to Dactylogyridae: Anacanthorus lepyrophallus (P = 84.2%, MII = 7.51 ± 1.50 [1–35], MA = 6.54 ± 1.38 [0–35]) and Mymarothecium sp. (P = 10.5%, MII = 2.33 ± 1.33 [1–7], MA = 0.22 ± 0.92 [0–7]). A total of 210 specimens were collected, and the overall P, MII, and MA of the parasites were 87.09%, 7.78 ± 1.48 (1–35), and 6.77 ± 1.37 (0–35), respectively. No endohelminths were recorded.

Data from the literature review jointly with data from the specimens evaluated here demonstrated that S. maculatus in the Neotropical region harbour 25 helminth taxa (Table 1). Of these 25 taxa, 10 are monogeneans, nine nematodes, three digeneans, two acanthocephalans, and one cestode (Figure 2). Monogeneans most commonly infect host gills, followed by the nasal cavities and body surface (mucus), whereas the endohelminth groups with higher richness, nematodes and acanthocephalans, most commonly infect host intestines (Table 1 and Figure 3). Furthermore, the majority (16/25) of parasite taxa were reported from the Upper Paraná River floodplain in Brazil.

Table 1
Helminth parasites reported from the piranha Serrasalmus maculatus* in Neotropical region.
Figure 2
Taxonomic distribution of parasitic fauna reported from the piranha Serrasalmus maculatus in Neotropical region.
Figure 3
Species richness of parasites reported in Serrasalmus maculatus from Neotropical region, according with their site of infection.

Monogenean species belonging to Anacanthorus and Mymarothecium in Neotropical hosts comprise 101 species (Table 2 and Figure 4). The genus Anacanthorus includes ~92 valid species (Table 2 and Figure 4), which are gill parasites of characiform fishes of the Serrasalmidae (41 species), Triportheidae (20 species), Bryconidae (19 species), Erythrinidae (eight species), and Characidae (four species). Brazil harbours the greatest number of Anacanthorus taxa (84 species). Meanwhile, the genus Mymarothecium includes nine species, which are also parasites of characiform fishes of the family Serrasalmidae, specifically of the genera Serrasalmus (four species), and Piaractus (two species), from Brazil, Peru, and Bolivia (Table 2 and Figure 4)

Table 2
Checklist of valid species of monogeneans belonging to Anacanthorus and Mymarothecium (Dactylogyridae) reported in characiform fishes from Neotropical region.
Figure 4
Monogeneans belonging to Anacanthorus and Mymarothecium (Dactylogyridae) reported from Neotropical characiform fishes.

Stomach content analysis resulted in the identification of ten food items, which mostly included fish fragments (81.7%) but also included terrestrial plants and decapods (Macrobrachium sp.) (Table 3). Serrasalmus maculatus showed piscivorous food habits, due to the predominant consumption of fish fragments (81.7%).

Table 3
Dietary components of piranha Serrasalmus maculatus specimens collected from the Ilha Solteira hydroelectric reservoir, Upper Paraná River basin, São Paulo state, Brazil.

Discussion

This is the first study to report the parasitic fauna of S. maculatus from the northwest region of the Upper Paraná River basin, São Paulo, Brazil. In addition, represents the first report of monogeneans belonging to Mymarothecium in this host species and first report of Anacanthorus lepyrophallus in the Ilha Solteira Reservoir. For monogeneans that parasitise fish gills, the phylogenetic relationships and evolutionary history between host orders are important factors for host-parasite interaction and distribution (Braga et al., 2014Braga MP, Araújo SBL, Boeger WA. Patterns of interaction between Neotropical freshwater fishes and their gill Monogenoidea (Platyhelminthes). Parasitol Res 2014; 113(2): 481-490. http://dx.doi.org/10.1007/s00436-013-3677-8. PMid:24221891.
http://dx.doi.org/10.1007/s00436-013-367...
).

Previous studies have demonstrated that most monogeneans prefer to parasitise specific host lineages (Graça et al., 2018Graça RJ, Fabrin TMC, Gasques LS, Prioli SMAP, Balbuena JA, Prioli AJ, et al. 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.
http://dx.doi.org/10.1371/journal.pone.0...
; Moreira et al., 2019Moreira J, da Silva Carneiro J, Ruz EJH, Luque JL. New Species and Records of Anacanthorus (Monogenea: Dactylogyridae) Parasitizing serrasalmid fish (Characiformes) from Brazil, including molecular data. Acta Parasitol 2019; 64(3): 449-455. http://dx.doi.org/10.2478/s11686-019-00055-7. PMid:31020494.
http://dx.doi.org/10.2478/s11686-019-000...
) (e.g., Mymarothecium taxa parasitise members of the Serrasalmidae) (Braga et al., 2015Braga MP, Razzolini E, Boeger WA. Drivers of parasite sharing among Neotropical freshwater fishes. J Anim Ecol 2015; 84(2): 487-497. http://dx.doi.org/10.1111/1365-2656.12298. PMid:25283218.
http://dx.doi.org/10.1111/1365-2656.1229...
). However, in some cases, members of other monogenean families have been reported to colonize phylogenetically distant hosts. In both cases, host-parasite relationships result from a combination of factors, including cospeciation, host-switching, and ecological fitting (Janzen, 1985Janzen DH. On ecological fitting. Oikos 1985; 45(3): 308-310. http://dx.doi.org/10.2307/3565565.
http://dx.doi.org/10.2307/3565565...
; Brooks et al., 2006Brooks DR, León-Règagnon V, McLennan DA, Zelmer D. Ecological fitting as a determinant of the community structure of platyhelminth parasites of anurans. Ecology 2006;87(7 Suppl): S76-S85. http://dx.doi.org/10.1890/0012-9658(2006)87[76:EFAADO]2.0.CO;2. PMid:16922304.
http://dx.doi.org/10.1890/0012-9658(2006...
; Braga et al., 2014Braga MP, Araújo SBL, Boeger WA. Patterns of interaction between Neotropical freshwater fishes and their gill Monogenoidea (Platyhelminthes). Parasitol Res 2014; 113(2): 481-490. http://dx.doi.org/10.1007/s00436-013-3677-8. PMid:24221891.
http://dx.doi.org/10.1007/s00436-013-367...
, 2015Braga MP, Razzolini E, Boeger WA. Drivers of parasite sharing among Neotropical freshwater fishes. J Anim Ecol 2015; 84(2): 487-497. http://dx.doi.org/10.1111/1365-2656.12298. PMid:25283218.
http://dx.doi.org/10.1111/1365-2656.1229...
). Considering the monophyly of the Characiformes and the diversification of the group only in the continental neotropics, the phylogenetic contiguity between the order’s families may indicate the sharing of a range of intrinsic resources (Braga et al., 2015Braga MP, Razzolini E, Boeger WA. Drivers of parasite sharing among Neotropical freshwater fishes. J Anim Ecol 2015; 84(2): 487-497. http://dx.doi.org/10.1111/1365-2656.12298. PMid:25283218.
http://dx.doi.org/10.1111/1365-2656.1229...
). Anacanthorus spp. are widely distributed in hosts of the five families of the order Characiformes (Figure 4). The sharing of resources (e.g., phylogenetic conservatism and phenotypic flexibility) may have favoured its occurrence within individuals of the same order and family (see Braga et al., 2014Braga MP, Araújo SBL, Boeger WA. Patterns of interaction between Neotropical freshwater fishes and their gill Monogenoidea (Platyhelminthes). Parasitol Res 2014; 113(2): 481-490. http://dx.doi.org/10.1007/s00436-013-3677-8. PMid:24221891.
http://dx.doi.org/10.1007/s00436-013-367...
, 2015Braga MP, Razzolini E, Boeger WA. Drivers of parasite sharing among Neotropical freshwater fishes. J Anim Ecol 2015; 84(2): 487-497. http://dx.doi.org/10.1111/1365-2656.12298. PMid:25283218.
http://dx.doi.org/10.1111/1365-2656.1229...
and cited references).

The predominance of monogeneans in S. maculatus in Neotropical region could be associated with both the parasites’ monoxenous biology and host species’ gregarious habit (Sazima & Machado, 1990Sazima I, Machado FA. Underwater observations of piranhas in western Brazil. Environ Biol Fishes 1990; 28(1-4): 17-31. http://dx.doi.org/10.1007/BF00751026.
http://dx.doi.org/10.1007/BF00751026...
; Strona, 2015Strona G. The underrated importance of predation in transmission ecology of direct lifecycle parasites. Oikos 2015; 124(6): 685-690. http://dx.doi.org/10.1111/oik.01850.
http://dx.doi.org/10.1111/oik.01850...
). Indeed, the proximity of fish in shoals can facilitate monogenean transmission, which occurs through simple contact between hosts (Thatcher, 2006Thatcher VE. Amazon fish parasites. 2nd ed. Sofia: Pensoft Publishers; 2006.). Furthermore, gregarious behaviour also allows free-native larval forms (oncomiracidia) to locate hosts more easily (Thatcher, 2006Thatcher VE. Amazon fish parasites. 2nd ed. Sofia: Pensoft Publishers; 2006.), which would justify the results observed in the present study.

The low parasite richness and absence of endoparasites observed in the present study may be related to host behaviour and/or foraging. Several studies have reported that heteroxenous parasites are transmitted via food web interactions and that intermediate hosts are nearly always dietary components of the parasites’ definitive hosts (Luque & Poulin, 2008Luque JL, Poulin R. Linking ecology with parasite diversity in Neotropical fishes. J Fish Biol 2008; 72(1): 189-204. http://dx.doi.org/10.1111/j.1095-8649.2007.01695.x.
http://dx.doi.org/10.1111/j.1095-8649.20...
; Lima et al., 2016Lima LB, Bellay S, Giacomini HC, Isaac A, Lima-Junior DP. 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.
http://dx.doi.org/10.1017/S0031182015001...
). Therefore, host diet is considered an important factor in host-parasite interactions, and hosts with more diverse diets tend to be more susceptible to endoparasite infections and, thus, usually harbour greater parasite richness (Lima et al., 2016Lima LB, Bellay S, Giacomini HC, Isaac A, Lima-Junior DP. 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.
http://dx.doi.org/10.1017/S0031182015001...
).

The dietary components of S. maculatus identified in the present study were like the findings of previous studies in the Upper Paraná floodplain, including the Ibicuí River, Rio Grande do Sul state, and a lower stretch of the Sorocaba River basin, São Paulo state, Brazil (Agostinho & Marques, 2001Agostinho CS, Marques EE. Selection of netted prey by piranhas, Serrasalmus spilopleura and S. marginatus (Pisces, Serrasalmidae). Acta Sci Biol Sci 2001; 23(2): 461-464.; Agostinho et al., 2003Agostinho CS, Hahn NS, Marques EE. Patterns of food resource use by two congeneric species of piranhas (Serrasalmus) on the Upper Paraná River floodplain. Braz J Biol 2003; 63(2): 177-182. http://dx.doi.org/10.1590/S1519-69842003000200002. PMid:14509839.
http://dx.doi.org/10.1590/S1519-69842003...
; Behr & Signor, 2008Behr ER, Signor CA. Distribuição e alimentação de duas espécies simpátricas de piranhas Serrasalmus maculatus e Pygocentrus nattereri (Characidae, Serrasalminae) do rio Ibicuí, Rio Grande do Sul, Brasil. Iheringia Ser Zool 2008; 98(4): 501-507. http://dx.doi.org/10.1590/S0073-47212008000400014.
http://dx.doi.org/10.1590/S0073-47212008...
; Villares et al., 2008Villares GA, Gomiero LM, Goitein R. Feeding of Serrasalmus maculatus (Kner, 1858) (Characiformes; Serrasalmidae) in the Sorocaba river, São Paulo State, Brazil. Acta Sci Biol Sci 2008; 30(3): 267-273. http://dx.doi.org/10.4025/actascibiolsci.v30i3.5011.
http://dx.doi.org/10.4025/actascibiolsci...
). Serrasalmus maculatus is piscivorous, preferentially ingesting fish fragments (instead of ingesting the host's entire body), and its feeding behaviour includes the mutilation of prey scales, fins, and muscle tissue, which we infer can hinder the ingestion of endoparasites (Sazima & Pombal-Jr, 1988Sazima I, Pombal-Jr JP. Mutilação de nadadeiras em acarás, Geophagus brasiliensis, por piranhas, Serrasalmus spilopleura. Rev Bras Biol 1988; 48(3): 477-483.; Sazima & Machado, 1990Sazima I, Machado FA. Underwater observations of piranhas in western Brazil. Environ Biol Fishes 1990; 28(1-4): 17-31. http://dx.doi.org/10.1007/BF00751026.
http://dx.doi.org/10.1007/BF00751026...
; Casali & Takemoto, 2016Casali GP, Takemoto RM. Endoparasitic fauna of Serrasalmus spp. (Characidae: Serrasalminae) in a neotropical floodplain. Acta Sci Biol Sci 2016; 38(1): 105-112. http://dx.doi.org/10.4025/actascibiolsci.v38i1.28592.
http://dx.doi.org/10.4025/actascibiolsci...
). In the present study, the dietary components of S. maculatus were fish fragments, terrestrial plants, and decapods (Macrobrachium sp.). However, even though Macrobrachium sp. is one of the most common of S. maculatus’ prey items, this genus of shrimp is native from Amazon basin (Collart & Moreira, 1993Collart OO, Moreira LC. Potencial pesqueiro de Macrobrachium amazonicum na Amazônia Central (Ilha do Careiro): variação da abundância e do comprimento. Amazoniana 1993; 12(3/4): 399-413.), and was introduced in Paraná River basin (Bialetzki et al., 1997Bialetzki A, Nakatani K, Baumgartner G, Bond-Buckup G. Occurrence of Macrobrachium amazonicum (Heller) (Decapoda, Palaemonidae) in Leopoldo’s inlet (Ressaco do Leopoldo), upper Paraná River, Porto Rico, Paraná. Rev Bras Zool 1997; 14(2): 379-390. http://dx.doi.org/10.1590/S0101-81751997000200011.
http://dx.doi.org/10.1590/S0101-81751997...
). When a species is introduced to a new area, it may lose part of its natural parasite fauna (i.e., Enemy Release Hypothesis - Keane & Crawley, 2002Keane RM, Crawley MJ. Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 2002; 17(4): 164-170. http://dx.doi.org/10.1016/S0169-5347(02)02499-0.
http://dx.doi.org/10.1016/S0169-5347(02)...
; Tourchin et al., 2002Tourchin ME, Lafferty KD, Kuris AM. Parasites and marine invasions. Parasitology 2002;124(7 Suppl): 137-151. http://dx.doi.org/10.1017/S0031182002001506. PMid:12396221.
http://dx.doi.org/10.1017/S0031182002001...
; Mitchell & Power, 2003Mitchell CE, Power AG. Release of invasive plants from fungal and viral pathogens. Nature 2003; 421(6923): 625-627. http://dx.doi.org/10.1038/nature01317. PMid:12571594.
http://dx.doi.org/10.1038/nature01317...
; Torchin et al., 2003Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM. Introduced species and their missing parasites. Nature 2003; 421(6923): 628-630. http://dx.doi.org/10.1038/nature01346. PMid:12571595.
http://dx.doi.org/10.1038/nature01346...
) and, thereby, break the natural network of complex interactions between intermediate and definitive hosts, which alters the infection dynamics and enables the loss of parasite taxa (Madi & Ueta, 2009Madi RR, Ueta MT. O papel de Ancyrocephalinae (Monogenea: Dactylogyridae), parasito de Geophagus brasiliensis (Pisces: Cichlidae), como indicador ambiental. Rev Bras Parasitol Vet 2009; 18(2): 38-41. http://dx.doi.org/10.4322/rbpv.01802008. PMid:19602315.
http://dx.doi.org/10.4322/rbpv.01802008...
).

Several authors have reported rich endoparasite fauna for S. maculatus in the Upper Paraná River floodplain, whereas endoparasites were completely absent in the present study, and the richness of ectoparasites was low (Pavanelli et al., 1997Pavanelli GC, Machado MH, Takemoto RM. Fauna helmíntica de peixes do rio Paraná, região de Porto Rico, Paraná. In: Vazzoler AEAM, Agostinho AA, Hahn NS, editors. A Planície de inundação do Alto rio Paraná: aspectos físicos, biológicos e socioeconômicos. Maringá: Eduem; 1997. p. 307-329.; Pavanelli et al., 2004Pavanelli GC, Machado MH, Takemoto RM, Guidelli GM, Lizama MAP. Helminth fauna of fishes: diversity and ecological aspects. In: Thomaz SM, Agostinho AA, Hahn NS, editors. The Upper Paraná river and its Floodplain: physical aspects, ecology and conservation. Leiden: Backhuys Publishers; 2004. p. 309-329.; Takemoto et al., 2009Takemoto RM, Pavanelli GC, Lizama MAP, Lacerda ACF, Yamada FH, Moreira LHA, et al. Diversity of parasites of fish from the Upper Paraná River floodplain, Brazil. Braz J Biol 2009;69(2 Suppl 2): 691-705. http://dx.doi.org/10.1590/S1519-69842009000300023. PMid:19738975.
http://dx.doi.org/10.1590/S1519-69842009...
; Casali & Takemoto, 2016Casali GP, Takemoto RM. Endoparasitic fauna of Serrasalmus spp. (Characidae: Serrasalminae) in a neotropical floodplain. Acta Sci Biol Sci 2016; 38(1): 105-112. http://dx.doi.org/10.4025/actascibiolsci.v38i1.28592.
http://dx.doi.org/10.4025/actascibiolsci...
‒ see Table 1). It is possible that the dynamics of parasitic infections are negatively affected by abiotic and biotic homogenisation in artificial habitats (Agostinho et al., 2007Agostinho AA, Pelicice FM, Petry AC, Gomes LC, Júlio HF Jr. Fish diversity in the upper Paraná River basin: habitats, fisheries, management and conservation. Aquat Ecosyst Health Manage 2007; 10(2): 174-186. http://dx.doi.org/10.1080/14634980701341719.
http://dx.doi.org/10.1080/14634980701341...
), such as hydroelectric reservoirs, especially for endoparasites with heteroxenous life cycles.

Floodplains are highly dynamic and complex systems because they include a wide variety of aquatic habitats (e.g., rivers, lakes, and canals) (Junk, 1980Junk WJ. Áreas inundáveis: um desafio para limnologia. Acta Amaz 1980; 10(4): 775-795. http://dx.doi.org/10.1590/1809-43921980104775.
http://dx.doi.org/10.1590/1809-439219801...
; Power et al., 1995Power ME, Sun A, Parker G, Dietrich WE, Wootton JT. Hydraulic Food-chain Models: an approach to the study of food -web dynamics in large rivers. Bioscience 1995; 45(3): 159-167. http://dx.doi.org/10.2307/1312555.
http://dx.doi.org/10.2307/1312555...
), when compared to artificial reservoirs, since the hydrodynamics and biotic communities of such last environments are altered during the damming process. The conversion of lotic to lentic environments involves a series of negative biotic and abiotic impacts, including changes in flow and channel granulometry, increases in fish mortality, increased predation rates, simplification of trophic chains, interruption of fish migration, eutrophication, deterioration of water quality, reduction of benthic community stability, colonisation by macrophytes, invasion by non-native species, and simplification of habitats (Agostinho et al., 1992Agostinho AA, Júlio Júnior HF, Borghetti JR. Considerações sobre os impactos dos represamentos na ictiofauna e medidas para sua atenuação. Um estudo de caso: reservatório de Itaipu. Rev Unimar 1992; 14(Suppl): 89-107.; 2008Agostinho AA, Pelicice FM, Gomes LC. Dams and the fish fauna of the Neotropical region: impacts and management related to diversity and fisheries. Braz J Biol 2008;68(4 Suppl): 1119-1132. http://dx.doi.org/10.1590/S1519-69842008000500019. PMid:19197482.
http://dx.doi.org/10.1590/S1519-69842008...
). Furthermore, these changes can ultimately reduce the abundance and richness of local biota, disrupt the dynamics of host-parasite relationships, and, consequently, alter the structure of parasitic communities (Morley, 2007Morley NJ. Anthropogenic effects of reservoir construction on the parasite fauna of aquatic wildlife. EcoHealth 2007; 4(4): 374-383. http://dx.doi.org/10.1007/s10393-007-0130-4.
http://dx.doi.org/10.1007/s10393-007-013...
), and these seem to be the drivers involved here regarding the low parasite richness observed for S. maculatus.

In summary, the richness of the component parasite community of S. maculatus in the Ilha Solteira hydroelectric reservoir in Brazil was low, in contrast to what has been previously reported in other water environments (Pavanelli et al., 1997Pavanelli GC, Machado MH, Takemoto RM. Fauna helmíntica de peixes do rio Paraná, região de Porto Rico, Paraná. In: Vazzoler AEAM, Agostinho AA, Hahn NS, editors. A Planície de inundação do Alto rio Paraná: aspectos físicos, biológicos e socioeconômicos. Maringá: Eduem; 1997. p. 307-329., 2004Pavanelli GC, Machado MH, Takemoto RM, Guidelli GM, Lizama MAP. Helminth fauna of fishes: diversity and ecological aspects. In: Thomaz SM, Agostinho AA, Hahn NS, editors. The Upper Paraná river and its Floodplain: physical aspects, ecology and conservation. Leiden: Backhuys Publishers; 2004. p. 309-329.; Takemoto et al., 2009Takemoto RM, Pavanelli GC, Lizama MAP, Lacerda ACF, Yamada FH, Moreira LHA, et al. Diversity of parasites of fish from the Upper Paraná River floodplain, Brazil. Braz J Biol 2009;69(2 Suppl 2): 691-705. http://dx.doi.org/10.1590/S1519-69842009000300023. PMid:19738975.
http://dx.doi.org/10.1590/S1519-69842009...
; Casali & Takemoto, 2016Casali GP, Takemoto RM. Endoparasitic fauna of Serrasalmus spp. (Characidae: Serrasalminae) in a neotropical floodplain. Acta Sci Biol Sci 2016; 38(1): 105-112. http://dx.doi.org/10.4025/actascibiolsci.v38i1.28592.
http://dx.doi.org/10.4025/actascibiolsci...
). These findings provide insight into the relationships between S. maculatus diet, social behaviour, and parasite fauna and the distribution and infection patterns of the observed parasite taxa. The present study also illustrates the possible effects of habitat homogenisation on parasite infection dynamics in artificial reservoirs. However, additional multidisciplinary research is needed to elucidate the effects of biotic and abiotic factors on the structure and dynamics of component communities of fish parasites in natural and artificial habitats in the neotropics.

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Publication Dates

  • Publication in this collection
    23 Mar 2022
  • Date of issue
    2022

History

  • Received
    27 Oct 2021
  • Accepted
    10 Feb 2022
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