Int. J. Aquat. Biol. (2022) 10(5): 370-377 ISSN: 2322-5270; P-ISSN: 2383-0956 Journal homepage: www.ij-aquaticbiology.com © 2022 Iranian Society of Ichthyology Short Communication Effect of parasitism on the relative condition factor of Astyanax bimaculatus (Characiformes: Characidae) a freshwater fish from the Caatinga domain, Brazil Dhenes Ferreira Antunes, Bruno Anderson Fernandes da Silva, Fabio Hideki Yamada Laboratory of Parasitic Ecology, Department of Biological Science, Regional University of Cariri, Crato, Ceará state, Brazil. s Article history: Received 3 April 2022 Accepted 7 August 2022 Available online 2 5 October 2022 Keywords: Freshwater fish Neotropical region Metazoan parasite Upper Jaguaribe River Welfare Abstract: The present study aimed to evaluate the effect of parasitism on the condition factor of Astyanax bimaculatus (Linnaeus 1758) (Characiformes, Characidae), in Batateiras river, Salgado River basin, northeastern Brazil. A total of 242 host specimens were collected between August 2018 and February 2020. The host presented a community of metazoan parasites of 14 taxa, totaling 1,750 specimens collected, with a mean total abundance of 7.23 specimens per fish, being the class Monogenea, the most predominant taxonomic group. The relative condition factor (Kn) differed significantly between parasitized and non-parasitized individuals, in which the parasitized hosts presented higher values of Kn. The abundance of the monogeneans Characithecium costaricensis and Diaphorocleidus sp. showed positive and significant correlations with the Kn. Considering the sex of the host, males had a higher parasite burden than females, although females present higher values of Kn. The parasitic burden of hosts did not show significant differences between seasonal periods. Introduction Parasites are key organisms of biodiversity and play an important ecological role, whether in population dynamics, species coexistence, or trophic interactions (Poulin, 1999; Hugot et al., 2001; Lefèvre et al., 2009). The parasite-host relationship can affect the entire community through its effects on species distribution and abundance (Horwitz and Wilcox, 2005). According to Bauer (1961), Gibbs (1985), and Le Cren (1951), parasites may have a negative effect on their hosts, which is reflected in a decrease in health conditions, reproductive fitness, and food conversion for use in cyclic activities. Astyanax bimaculatus (Linnaeus, 1758) (Characiformes: Characidae), popularly known as “lambari do rabo amarelo” (Mirande, 2010; Frick et al., 2018). Its distribution extends from northeastern Brazil and eastern South America to the Prata river basin (Sterba, 1973; Lima et al., 2003). According to Cordeiro et al. (2019), this species possesses adaptive plasticity associated with the reproductive mechanisms and strategies developed during its Correspondence: Fabio Hideki Yamada DOI: https://doi.org/10.22034/ijab.v10i5.1560 E-mail: fhyamada@hotmail.com DOR: 20.1001.1.23830956.2022.10.5.3.4 lifetime, allowing survival in the most varied habitats. To date, it has been recorded several parasitic associations to A. bimaculatus in several aquatic ecosystems in Brazil: Clinostomum complanatum (Rudolphi, 1814), Procamallanus (Spirocamallanus) hillari (Pinto & Deli, 1976) and Polymorphus sp. Luhe, 1911 in the Guandu River, Rio de Janeiro state (Abdallah et al., 2004); Magnivitellinum simplex (Kloss, 1966) in the Paraná river, Paraná state (Kohn et al., 2011); Prostosthenhystera obesa (Diesing, 1850) in the Paraná River, São Paulo state (Kohn et al., 1997); P. (Spirocamallanus) inopinatus (Artigas & Pereira, 1928), P. (S.) hillari, Halipegus sp. Looss, 1899 in the Mogi-Guaçu River, São Paulo state (Kohn and Fernandes, 1987); Rhabdochona acuminata (Molin, 1860) in the Lajes Reservoir, Rio de Janeiro state (Paraguassú and Luque, 2007); Lernaea cyprinacea (Linnaeus, 1758), weir in Antonio Prado municipality, Rio Grande do Sul state (Gallio et al., 2007); Myxobolus sp. in the Dantas river, Maranhão https://ij-aquaticbiology.com/index.php/ijab/article/view/1560 371 Int. J. Aquat. Biol. (2022) 10(5): 370-377 state (Silva et al., 2019); L. cyprinacea, Urocleidoides sp. Mizelle & Price, 1964, Rabdochona sp. Railliet, 1916, P. (S.) hilarii, P. obesa, Dolops sp. Audouin, 1837 in the São Francisco river, Sergipe state (Vasconcelos et al., 2013); and Quadrigyrus torquatus Van Cleave 1920 and Quadrigyrus nickoli Schmidt & Hugghins, 1973 in the Chumucuí river, Pará state (Fujimoto et al., 2013). For fish, the relative condition factor (Kn) may explain the health and welfare aspects of these organisms (Mozsár et al., 2015), food resources (Bolger and Connoly, 1989), nutritional status and response to environmental factors (Brown and Murphy, 2004) as well as seasonal changes in environmental conditions (Gomiero and Braga, 2005). In this context, the present study aimed (1) to characterize the metazoan parasite community of A. bimaculatus from Batateiras River, Caatinga domain; and (2) to evaluate the effects of the parasitism on its relative condition factor (Kn). Materials and methods The specimens of A. bimaculatus were collected from August 2018 to February 2020 in Batateiras River, Salgado River basin, municipality of Crato, Ceará state (7º13'57.52''S; 39º26'25.46''W) (Fig. 1), in two seasonal periods (Dry – from August to October and Rainy – from November to February). The individuals were measured (standard length (SL) to the nearest 0.1 mm) and weighed (to the nearest 0.1 g) at the laboratory. All the specimens were examined for ectoparasites (eyes, nostrils and gills) and endoparasites (stomach, intestine, liver, gonads, swim bladder and muscles) according to the parasitological methods of collection, fixation, preservation and preparation described by Eiras et al. (2006). The parasite identification was performed according to Moravec (1998), Thatcher (2006) and Cohen et al. (2013). The prevalence, mean abundance and mean intensity of the component communities were calculated according to Bush et al. (1997). The standard length (Ls) and total weight (Wt) of each host specimen were fitted in the Wt/Ls ratio. The values of the regression coefficients a and b were used in the estimates of expected weight values (We), using the equation We = a.Lsb. The relative Figure 1. Sampling area of Astyanax bimaculatus collected from August 2018 to February 2020, Batateiras River, Salgado river basin, municipality of Crato, Ceará state, Brazil. 372 Antunes et al./ Effect of parasitism on the relative condition factor of Astyanax bimaculatus condition factor (Kn) was then calculated, which is the quotient between the observed weight and the expected weight for a given length (Kn= Wt/We) (Le Cren, 1951). Spearman’s rank correlation coefficient (rs) was employed to verify correlations between Kn and parasite abundance (Zar, 2010). The Mann-Whitney test (U) was employed to verify the differences between the Kn of parasitized and non-parasitized hosts, hosts collected in dry and rainy seasonal periods, and males and females hosts. Also, the Mann-Whitney test (U) was used to verify differences in parasitic burden between males and females (Zar, 2010). The Chi-square test (X2) was performed to verify differences in the prevalence of parasites between the two seasonal periods (dry and rainy) and the sex of the host. The statistical analyzes were performed using the Statistica software package version 7.1 (Statsoft Inc., 2005) and the statistical significance level adopted was P≤0.05. Results and Discussion The parasitic community of A. bimaculatus was composed of 14 taxa, totaling 1,750 specimens of the parasite, with a mean total abundance of 7.23 specimens per fish, being the class Monogenea, the taxonomic group more representative. Of the 242 host specimens examined, 132 (average size of 5.06±0.109) and 110 (average size of 5.98±0.117) were collected in the dry and rainy seasons, respectively. The parasites Anachantocotyle anachantocotyle, Characithecium costaricensis, Characithecium sp.1, Characithecium sp.2, Diaphorocleidus sp., Urocleidoides trinidadensis, P. (Spirocamallanus) hilarii and Wallinia caririensis were present in both seasonal periods. While the Ascocotyle sp., Henneguya sp., Quadrigyrus sp., Dactylogyridae gen. sp., Diplostomidae gen. sp. and Spiroxys sp. were present in only one season. Characithecium costaricensis, Characithecium sp. 1, Diaphorocleidus sp., U. trinidadensis, Wallinia caririensisand P. (S.) hilarii presented a prevalence higher than 10% (Table 1). Parasitized individuals of A. bimaculatus showed Kn higher (0.89±0.03) than non-parasitized (0.65±0.02) (Z(U) = 4.7972; P<0.0001). The parasitic prevalence of Characithecium sp.1, Diaphorocleidus sp., A. anachantocotyle and W. caririensis were more prevalent in the rainy season. The host specimens presented an average Kn of 0.81±0.03 and 0.85±0.04 in the dry and rainy seasons, respectively; however, not significant (Z(U) = 1.5593; P<0.1189). The monogeneans C. costaricensis and Diaphorocleidus sp. showed positive and significant correlations between its abundance and the Kn of the analyzed hosts in both seasonal periods (Table 2). Of the 242 fish examined, 80 were females (average size of 6.26±0.195), 157 were males (average size of 5.90±0.06), and five undefined sex. The female specimens presented an average Kn of 1.00±0.05, significantly higher than the male (0.75±0.03) (Z(U) =4.9088; P<0.0001). The male hosts showed a significantly higher parasitic burden (978 specimens) than females (772 specimens) (Z(U) 1.9485; P<0.0514). The parasitic prevalence of C. costaricensis, Characithecium sp.1, and U. trinidadensis were more prevalent in the female host. The parasitic fauna of A. bimaculatus showed new occurrences and was predominantly by gill ectoparasite of class Monogenea. The second representative group was the digenetic trematodes recovered from the intestine, gills and eyes. The metacercariae of Ascocotyle sp. recovered from the gills of A. bimaculatus in Batateiras River, have already been described to Satanoperca pappaterra (Heckel, 1840) (Cichlidae) and Crenicichla niederleinii (Holmberg, 1891) (Cichlidae) in the Paraná River basin (Yamada et al., 2008). Furthermore, the parasites Procamallanus (S.) hilarii and Diplostomidae gen. sp. have already been registered for this host in other Brazilian ecosystems (Kohn and Fernandes, 1987; Abdallah et al., 2004, Vasconcelos et al., 2013). In the present study, the relative condition factor (Kn) of the parasitized hosts has been shown greater 373 Int. J. Aquat. Biol. (2022) 10(5): 370-377 than non-parasitized. This finding corroborates with Lizama et al. (2006) that found Kn significantly higher in parasitized fish than in non-parasitized. Although parasitism negatively affects the condition of the hosts (Bauer, 1970), the fish parasitized by the monogeneans C. costaricensis and Diaphorocleidus sp. showed positive and significant correlations between host Kn and their abundance in both seasonal periods. In this context, Moore (1987) pointed out that larger fish with high Kn can be able to harbor larger numbers of parasites and can tolerate greater intensities of infestations. Considering the seasonal periods, Characithecium sp.1, Diaphorocleidus sp., W. caririensis and A. anachantocotyle were more dominant in the rainy period. Several studies indicate that limnological factors could influence the dynamic of host-parasite interactions (Barker and Coneb, 2000; Lizama et al., 2006). The study area exhibits an intermittent regime (Rosa et al., 2004). Therefore, the Kn of A. bimaculatus showed no significant differences during the rainy and drought seasons. This plasticity indicates that A. bimaculatus is probably a resilient species and well-adapted to this aquatic ecosystem. Considering the sex of the host, males presented a higher parasitic burden than females. However, female specimens presented an average Kn significantly higher than males. The prevalence of three monogeneans species (C. costaricensis, Characithecium sp.1 and U. trinidadensis) was more prevalent in females, probably due to higher body mass and size, consequently, higher Kn than males. The distinction of parasitism about the sex of the Parasite species Dry Rainy P(%) MA±SE MI±SE P(%) MA±SE MI±SE Phylum Myxozoa Class Myxosporea Henneguya sp. – – – 1.81 0.1727±0.1408 9.5±5.500 Phylum Platyhelminthes Class Monogenea Anachantocotyle anachantocotyle 4.54 0.09±0.046 2.0±0.683 13.63 0.29±1.007 2.1±0.496 Characithecium costaricensis 34.84 1.189 ±0.238 3.4±0.553 26.36 0.627±0.163 2.3±0.494 Characithecium sp.1 34.84 1.795±0.326 5.1±0.712 15.45 0.436±0.157 2.8±0.819 Characithecium sp.2 6.06 0.09±0.033 1.5±0.189 10.90 0.136±0.417 1.2±0.13 Dactylogyridae gen. sp. – – – 0.90 0.009±0.009 1.0±0.000 Diaphorocleidus sp. 21.21 0.931±2.526 4.3±0.737 54.54 2.918±0.477 5.3±0.743 Urocleidoides trinidadensis 23.48 0.651±0.140 2.7±0.411 33.63 0.636±1.254 1.8±0.25 Class Trematoda Diplostomidae gen. sp. 1.51 0.045±0.033 3.0±1.00 – – – Ascocotyle sp. (metacercariae) 4.54 0.09±0.042 2.0±0.516 – – – Wallinia caririensis 13.63 0.924±0.370 6.7±2.324 28.18 3.209±0.803 11.3±2.285 Phylum Nematoda Class Chromadorea Procamallanus (Spirocamallanus) hilarii 10.60 0.143±0.04 1.3±0.169 13.63 0.272±0.078 2.0±0.323 Class Secernentea Spiroxys sp. (larvae) 2.27 0.03±0.018 1.3±0.333 – – – Phylum Acanthocephala Class Eoacanthocephala Quadrigyrus sp. – – – 1.81 0.018±0.012 1.0±0.000 Table 1. Ecological descriptors of the parasitic community of Astyanax bimaculatus, Batateiras River, Salgado River basin, municipality of Crato, Ceará state, Brazil, in the dry and rainy seasonal periods. MA = mean abundance; MI = mean intensity; P(%) = prevalence and SE = standard error. 374 Antunes et al./ Effect of parasitism on the relative condition factor of Astyanax bimaculatus hosts may be linked to energy needs, different feeding habits or physiological differences of the individual (González and Acuña, 2000). For instance, males of Cichla monoculus Agassiz, 1831 (Cichlidae) from the Upper Paraná River floodplain presented intensities of infestation of cestodes significantly higher than the females (Machado et al., 2000). Males of Astyanax altiparanae Garutti & Britski, 2000 (Characidae) from the Chavantes reservoir showed a higher parasitic burden than females (Zica, 2008). On the other hand, females of Salminus brasiliensis (Cuvier, 1816) (Bryconidae) from the Upper Paraná River floodplain presented high levels of infestation by the acanthocephalans and nematodes (Karling et al., 2013). In summary, the parasite communities of A. bimaculatus were characterized by high ectoparasite species richness, with monogeneans being numerically dominant; parasitized hosts showed the Kn higher than non-parasitized. Females could withstand a higher parasitic burden than males, and differences in Kn between seasonal periods. In general, it is expected that parasites cause deleterious effects on their host; therefore, it is difficult to define and measure those effects. This corroborates the finding of Kennedy (2009) and Price (1980) in which that there is no pattern or order in space or time in fish parasitological studies and that most of the populations of fish parasites live in conditions of imbalance, dominated by stochastic events, respectively. Acknowledgments This work was supported by the Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP) under the Grant # BP3- Parasite species Dry Rainy rs p rs p Phylum Myxozoa Classe Myxosporea Henneguya sp. – – 0.033 0.7280 Phylum Platyhelminthes Class Monogenea Anachantocotyle anachantocotyle -0.026 0.7674 -0.140 0.1429 Characithecium costaricensis 0.466 0.0001 0.266 0.0049 Characithecium sp.1 0.131 0.1344 0.148 0.1227 Characithecium sp.2 0.241 0.0053 0.008 0.9282 Dactylogyridae gen. sp. - - 0.164 0.086 Diaphorocleidus sp. 0.396 0.0001 0.305 0.0011 Urocleidoides trinidadensis 0.266 0.002 0.163 0.0886 Class Trematoda Diplostomidae gen. sp. 0.124 0.1559 – – Ascocotyle sp. (metacercariae) -0.109 0.1095 – – Wallinia caririensis 0.473 0.0001 0.133 0.1630 Phylum Nematoda Class Chromadorea Procamallanus (Spirocamallanus) hilarii -0.025 0.7727 0.338 0.0003 Class Secernentea Spiroxys sp. (larvae) 0.106 0.2257 – – Phylum Acanthocephala Class Eoacanthocephala Quadrigyrus sp. – – 0.220 0.0204 Table 2. Spearman’s rank correlation coefficient (rs) between the relative condition factor (Kn) and the parasitic abundance of Astyanax bimaculatus, Batateiras river, Salgado river basin, municipality of Crato, Ceará state, Brazil, in the dry and rainy seasonal periods. 375 Int. J. Aquat. Biol. (2022) 10(5): 370-377 0139-00039.01.06/19 (D.FA.) and BP3-0139 00039.01.00/18 (F.H.Y.); and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) under the Grant # 143996/2019-3 (B.A.F.S). References Abdallah V.D., Azevedo R.K., Luque J.L. (2004). Metazoários parasitos dos lambaris Astyanax bimaculatus (Linnaeus, 1758) A. parahybae Eigenmann, 1908 e Oigosarcus hepsetus (Cuvier, 1829) (Oesteichthyes: Characidae), do Rio Guandu, estado do Rio de Janeiro, Brasil. Brazilian Journal of Veterinary Parasitology, 13: 57-63. Barker D.E., Coneb D.K. (2000). Occurrence of Ergasillus celestis (Copepoda) and Pseudodactyloggryrus anguillae (Monogenea) among wild eels (Anguilla rostrata) in relation to stream flow, pH and temperature and recommendations for controlling their transmission among captive eels. Aquaculture, 187: 261-274. Bauer O.N. (1961). Relationships between host fishes and their parasites. In: V.A. Dogiel, G.K. Petrushevski, Y.I. Polyanski (Eds.). Parasitology of fishes. Translated by Z. Kabata. 1st. Ed. Edinburgo: Oliver and Boyd. pp: 84-103. Bauer O.N. (1970). Parasites and Diseases of USSR coregonids. In: C.C. Lindsey, C.S. Woods (Eds.). Biology of Coregonid fishes. University of Manitoba Press, Winnipeg. pp: 267-278. Bolger T, Connolly P.L. (1989). The selection of suitable indices for the measurement and analysis of fish condition. Journal of Fish Biology, 34: 171-182. Brown M.L., Murphy B.R. (2004). Seasonal dynamics of direct and indirect condition indices in relation to energy allocation in largemouth bass Micropterus salmoides (Lacépede). Ecology of Freshwater Fish, 13: 23-36. Bush A.O., Lafferty K.D., Lotz J.M., Shostak A.W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology, 83: 575-583. Cohen S.C., Justo M.C.N., Kohn A. (2013). South American Monogenoidea parasites of fishes, amphibians and reptiles. Rio de Janeiro: Oficina de Livros. 662 p. Cordeiro J.G., Rodrigues J., Rodrigues M.S., Bertolini R.M., Nobrega R.H., Yasui G.S., Maximino C., Siqueira-Silva D.G. (2019). Reproductive cycle of the tetra Astyanax bimaculatus (Characiformes: Characidae) collected in Amazonian streams. Zygote, 28: 37-44. Eiras J.C., Takemoto R.M., Pavanelli G.C. (2006). Métodos de estudo e técnicas laboratoriais em parasitologia de peixes. Ed. Eduem. 199 p. Fricke R., Eschmeyer W., Fong J.D. (2018). Eschmeyer's Catalog of Fishes. Available from: https://www.calacademy.org/scientists/projects/esch meyers-catalog-of-fishes. Retrieved 3/19/2022. Fujimoto R.Y., Almeida E.S., Diniz D.G., Eiras J.C., Martins M.L. (2013). Parasites of four ornamental fish from the Chumucuí River (Bragança, Pará, Brazil). Brazilian Journal of Veterinary Parasitology, 22: 34- 38. Gallio M., Silva A.S., Monteiro S.G. (2007). Parasitismo por Lernaea cyprinacea em Astyanax bimaculatus provenientes de um açude no município de Antonio Prado, Rio Grande do Sul. Acta Scientiae Veterinariae, 35: 209-212. Gibbs H.C. (1985). Effects of parasites on animal and meat production. In: Gaafar S.M., Howard Marsh W.E. R.E. (Ed.). World animal science B2: parasites, pests and predators. The Netherlands: Elsevier. pp: 7- 27. Gomiero L.M., Braga F.M.S. (2005). The condition factor of fishes from two river basins in São Paulo state, Southeast of Brazil state, Southeast of Brazil. Acta Scientiarum Biological Science, 27: 73-78. González M.T., Acunã E. (2000). Influence of host size and sex on the endohelminth infracommunities of the red rockfish Sebastes capensis off northem Chile. The Journal of Parasitology, 86: 854-857. Horwitz P., Wilcox B.A. (2005). Parasites, ecosystems and sustainability: an ecological and complex systems perspective. International Journal for Parasitology, 35: 725-732. Hugot J.P., Baujard P., Morand S. (2001). Biodiversity in helminths and nematodes as a field of study: an overview. Nematology, 3: 199-208. Karling L.C., Isaac A., Affonso I.P., Takemoto R.M., Pavanelli G.C. (2013). 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, Brazil. Journal of Helminthology, 87: 245-251. 376 Antunes et al./ Effect of parasitism on the relative condition factor of Astyanax bimaculatus Kennedy C.R. (2009). The ecology of parasites of freshwater fishes: the search for patterns. Parasitology, 136: 1653-1662. Kohn A., Moravec F., Cohen S.C., Canzi C., Takemoto R.M., Fernandes B.M.M. (2011). Helminths of freshwater fishes in the reservoir of the Hydroelectric Power Station of Itaipu, Paraná, Brazil. Check List, 7: 681-690. Kohn A., Fernandes B.M.M. (1987). Estudos comparativos dos Helmintos parasitos de peixes do Rio Mogi Guassu, coletados nas excursões realizadas entre 1927 e 1985. Memórias do Instituto Oswaldo Cruz, 82: 483-500. Kohn A., Fernandes B.M.M., Baptista-Farias M.F. (1997). Redescription of Prosthenhystera obesa (Diesing, 1850) (Callodistomidae, Digenea) with new host records and data on morphological variability. Memórias do Instituto Oswaldo Cruz, 92: 171-179. Le Cren E.D. (1951). The length-weight relationship and seasonal cycle in gonad weight and condition in the perch Perca fluviatilis. Journal of Animal Ecology, 20: 201-219. Lefèvre T., Lebarbenchon C., Gauthier-Clerc M., Missé D., Poulin R., Thomas F. (2009). The ecological significance of manipulative parasites. Trends in Ecology and Evolution, 24: 41-48. Lima F.C.T., Malabarba L.R., Buckup P.A., Silva J.F.P., Vari R.P., Harold A., Benine R., Oyakawa O.T., Pavanelli C.S., Menezes N.A., Lucena C.A.S., Malabarba M.C.S.L., Lucena Z.M.S., Reis R.E., Langeani F., Cassati L., Bertaco V.A., Moreira C., Lucinda P.H.F. (2003). Characidae, genera incertae sedis. In: R.E. Reis, S.O. Kullander, C.J. Ferraris Jr. (Eds.). Check List of the Freshwater Fishes of South and Central America. Porto Alegre, Edipucrs. pp: 106- 169. Lizama M.L.A.P., Takemoto R.M., Pavanelli G.C. (2006). Parasitism influence on the hepato, splenosomatic and weight/length relation and relative condition factor of Prochilodus lineatus (Valenciennes, 1836) (Prochilodontidae) of the Upper Paraná River floodplain, Brazil. Brazilian Journal of Veterinary Parasitology, 15: 116-122. Machado P.M., Almeida S.C., Pavanelli G.C., Takemoto R.M. (2000). Ecological aspects of endohelminths parasitizing Cichla monoculus Spix, 1831 (Perciformes: Cichlidae) in the Paraná River near Port Rico, State of Paraná, Brazil. Comparative Parasitology, 67: 210-217. Mirande J.M. (2010). Phylogeny of the Family Characidae (Teleostei: Characiformes): from characters to taxonomy. Neotropical Ichthyology, 8: 385-568. Moore J. (1987). Some roles of parasitic helminths in trophic interactions. A view from North America. Revista Chilena de Historia Natural, 60: 159-179. Moravec F. (1998). Nematodes of freshwater fishes of the Neotropical region. Czech Republic: Academia Praha. 464 p. Mozsár A., Boros G., Sály P., Nagy S.A. (2015). Relationship between Fulton’s condition factor and proximate body composition in three freshwater fish species. Journal of Applied Ichthyology, 31: 315-320. Paraguassú A.R., Luque J.L. (2007). Metazoários parasitos de seis espécies de peixes do reservatório de Lajes, estado do Rio de Janeiro, Brasil. Brazilian Journal of Veterinary Parasitology, 16: 121-128. Poulin R. (1999). The functional importance of parasites in animal communities: many roles at many levels? International Journal for Parasitology, 29: 903-914. Price P.W. (1980). The evolutionary biology of parasites. New Jersey, USA: Princeton University Press. 256 p. Rosa R.S., Gomes-Filho G., Menezes N.A., Shibatta O.A., Costa W.J.E.M. (2004). Biota aquática: áreas e ações prioritárias para conservação da caatinga. In: J.M.C. Silva, M. Tabarelli, M.T. Fonseca, L.V. Lins (Ed.). Biodiversidade da caatinga: áreas e ações prioritárias para a conservação. Brasília: Ministério do Meio Ambiente. pp: 163-71. Silva M.F., Sousa-Henrique D.D., Messias-Luz N., Borralho L.S., Oliveira J.D., Sindeaux-Neto J.L., Matos E.R. (2019). Myxobolus sp. (Myxozoa; Myxosporea) causing asymptomatic parasitic gill disease in Astyanax aff. bimaculatus (Characiformes; Characidae) in the Tocantins river basin, Amazon region, Brazil. Brazilian Journal of Veterinary Parasitology, 28: 739-743. Statsoft Inc. (2005). Statistica (data analysis software system), version 7.1. Sterba G. (1973). Freshwater fishery of the world. T.F.H. Publications. 1161 p. Thatcher V.E. (2006). Amazon Fish Parasites. 2ª ed. Bulgaria: Pensoft Publishers. 509 p. Vasconcelos A.C.P., Lopes A.C.M., Santos J.M.S., Jeraldo V.L.S., Melo C.M., Madi R.R. (2013). Molecular analysis and biodiversity of metazoan 377 Int. J. Aquat. Biol. (2022) 10(5): 370-377 parasites of the yellow tail lambari, Astyanax aff. bimaculatus (Teleostei, Characidae), in lower San Francisco, northeastern Brazil. Neotropical Helminthology, 7: 41-49. Yamada F.H., Takemoto R.M., Pavanelli G.C. (2008). Relação entre fator de condição relativo (Kn) e abundância de ectoparasitos de brânquias, em duas espécies de ciclídeos da bacia do rio Paraná, Brasil. Acta Scientiarum: Biological Sciences, 30: 213-217. Zar J.H. (2010). Biostatistical Analysis. 5th ed. New Jersey: Prentice-Hall. 944 p. Zica E.O.P. (2008). Análise parasitológica de peixes em sistemas de tilapicultura em tanques-redes e suas inter- relações com a ictiofauna residente e agregada. M.Sc. Dissertation. Universidade Estadual Paulista, São Paulo state, Brazil. 59 p.