Introduction

Astyanax fasciatus (Cuvier, 1819) is popularly known as the banded astyanax and it is an abundant species in several drainage basins in the Americans (^{FROESE & PAULY, 2013}). It is classified as a foraging species, and it is well distributed along the São Francisco river (^{BUCKUP et al., 2007}), serving as an important food source for larger fish. Although banded astyanax do not have significant commercial value, they are often eaten as snacks, especially by the riverine population, and they are also used as bait for sport fishing (^{SANTOS et al., 1995}).

Larval specimens of Spiroxys sp. were found in A. fasciatus in Mexico (^{MORAVEC, 1998}). With regard to the same host species on the Nicaraguan coast, ^{Aguirre-Macedo et al. (2001)} identified larvae of Brevimulticaecum sp., Contracaecum sp. and Spiroxys sp. Subsequently, ^{Salgado-Maldonado (2008)} also discovered Procamallanus neocaballeroi (Caballero-Deloya, 1977) and Procamallanus rebecae (Andrade-Salas, Pineda-López, & García-Magaña, 1994) in Central America.

In the upper São Francisco river, ^{Moreira et al. (1994)} recorded occurrences of larvae of Contracaecum sp. and described Procamallanus saofranciscencis (^{Moreira et al., 1994}) in A. fasciatus. ^{Brasil-Sato (2003)} further listed occurrences of several species of adult parasitic nematodes in fish in the São Francisco river basin: Cosmoxynema vianai Travassos, 1948; Cosmoxynemoides aguirrei Travassos, 1948; Cucullanus pinnai Travassos, Artigas & Pereira, 1928; Neocucullanus neocucullanus Travassos, Artigas & Pereira, 1928; Procamallanus freitasi Moreira, Oliveira & Costa, 1991; Procamallanus inopinatus Travassos, Artigas & Pereira, 1928; P. saofranciscencis, Rondonia rondoni Travassos, 1920; Travassosnema travassosi Costa, Moreira & Oliveira, 1991; Travnema araujoi Fernandes, Campos & Artigas, 1983; and Travnema travnema Pereira, 1928. Larval specimens of several nematode species were also listed by Brasil-Sato (op. cit.): Contracaecum sp., Cucullanus sp., Dichelyne sp., Eustrongylides sp., Goezia sp., Hysterothylacium sp. and Philometra sp. In addition, ^{Santos et al. (2009)} identified larval specimens of Spiroxys sp. in three species of carnivorous fish: Pygocentrus piraya (Cuvier, 1819); Serrasalmus brandtii Lütken, 1875; and Cichla kelberi Kullander & Ferreira, 2006), in the Três Marias Reservoir. Finally, larval specimens of Rhabdochona sp. were found in Conorhynchos conirostris Valenciennes, 1840, by ^{Brasil-Sato & Santos (2005)}.

The aims of this study were to investigate parasitism in A. fasciatus and contribute towards enriching knowledge of the ichthyoparasitology of the São Francisco river. Thus, it had the specific objectives of recording the species of parasitic nematodes of banded astyanax and also measuring their parasitic parameters (prevalence, mean intensity and mean abundance).

Materials and Methods

A total of 74 specimens of A. fasciatus were provided by technical staff of thee regional development company CODEVASF in Três Marias, Minas Gerais, under authorization from the State Forestry Institute of Minas Gerais (IEF-MG). These fish were collected in the upper São Francisco river, located in the municipality of Três Marias, in the state of Minas Gerais (18°12’32”S, 45°15’41”W) in January 2011 and January 2012. The host necropsies and parasite processing procedures followed ^{Eiras et al. (2006)}. The parasitological descriptors used were those prescribed by ^{Bush et al. (1997)}. Nematode measurements are presented in millimeters. The measurement ranges are presented in the results tables, and these values are followed by the means and their respective standard deviations. Morphometry was ascertained using a Nikon Alphaphot-2 microscope with a calibrated reticle coupled to the ocular lens. Parasite voucher specimens were deposited in the Helminthological Collection of the Oswaldo Cruz Institute (CHIOC), state of Rio de Janeiro, Brazil. A numbering system was used, as indicated in the results (Table 1). The host voucher specimen was deposited in the Fish of the Museum, University of São Paulo (MZUSP, 95161), state of São Paulo, Brazil.

Results and Discussion

The parasite fauna of A. fasciatus consisted of eleven nematode species, which are presented in Table 1 with their respective parasitic indeces. Nine species were represented by larval specimens and had characterized A. fasciatus as a noteworthy intermediate host in their parasitic cycles. Five species (Brevimulticaecum sp., Contracaecum sp., Cystidicoloides sp., Hysterothylacium sp. and Spiroxys sp.) out of these nine in the larval stage presented prevalence higher than 10%. Two nematode species were represented by adult specimens: Spinitectus rodolphiheringi Vaz & Pereira, 1934 and P. saofranciscencis. For these A. fasciatus was characterized as the definitive host. The prevalence of P. saofranciscencis was higher than 10%.

The results from the morphometric analysis, i.e. characterization of the peculiarities of nematode species identified in A. fasciatus in this study, are shown in Tables 2 -5. Exceptionally, the data on Goezia sp. were based on a single specimen (n = 1; P = 1.35%) that was found in the stomach. Its measurements in millimeters (length × width) were as follows: body, 1.723 × 0.105; esophagus, 0.208 × 0.025; ventriculus, 0.028 × 0.025; nerve ring from the anterior extremity, 0.108; spines of the ventricular appendix region, 0.005; distance between the ring spines of the ventricular appendix region, 0.006; ventricular appendix, 0.743; cecum appendix, 0.088; and tail, 0.058. In the same region of Brazil, ^{Santos-Clapp & Brasil-Sato (2014)} also observed larvae of Goezia sp. in C. kelberi, showing low prevalence (1.8%). Four species have been described in Brazil: G. spinulosa in Arapaima gigas from Mexiana Island, Amazon river, state of Pará (^{SANTOS & MORAVEC, 2009}) and from the Araguaia river, state of Mato Grosso do Sul (^{MENEZES et al., 2011}); Astronotus ocellatus, Micropterus salmoides and Pseudoplatystoma corruscans from the Araguaia and Amazon rivers (Pará) (^{MORAVEC, 1998}); G. brasiliensis in the characid Brycon hilarii and in Pseudoplatystoma corruscans from the Paraná river, Foz do Iguaçú and G. brevicaeca in Brycon hilarii from the Paraná river, Foz do Iguaçú (^{MORAVEC et al., 1994}; ^{MORAVEC, 1998}); and G. leporini in Leporinus macrocephalus from Batatais, state of São Paulo (^{MARTINS & YOSHITOSHI, 2003}).

Differing from our study, ^{Santos & Moravec (2009)} and ^{Martins & Yoshitoshi (2003)} found high prevalences of adults and larvae in the species G. spinulosa (90%) and G. leporini (65%), respectively. Massive presence of these species gives rise to attacks mainly on the stomach, causing gross lesions and high mortality among the fish.

With regard to S. rodolphiheringi, one male, one female, and one juvenile were found in A. fasciatus. Their measurements and features were in line with what was reported by ^{Moravec (1998)}. In the São Francisco river, adult specimens of S. rodolphiheringi were found in Franciscodoras marmoratus (Reinhardt, 1874) (^{SANTOS & BRASIL-SATO, 2004}). Thus, the presence of adult specimens of S. rodolphiheringi in A. fasciatus increases the list of known hosts in the São Francisco basin.

In this study, the features of P. saofranciscencis specimens in A. fasciatus, as well as their measurements, were equivalent to what was presented by ^{Moravec (1998)}. Procamallanus saofranciscencis was identified in fish of the families Characidae (^{VICENTE & PINTO, 1999}) and Acestrorhynchidae (^{MOREIRA et al., 1994}) in the upper São Francisco river. Larval specimens of Procamallanus sp., which had already been identified in this basin, have also been found in Characidae (^{VICENTE & PINTO, 1999}) and Pimelodidae (^{BRASIL-SATO & SANTOS, 2005}). Based on the presence of the larval specimens (Procamallanus sp.) and adults of P. saofranciscencis in A. fasciatus, it can be seen that this foraging fish takes part in the cycle of these species as intermediate and definitive hosts, respectively, and this enlarges the list of hosts for this nematode group in the São Francisco basin.

Larval specimens of Cystidicoloides sp. had already been found in Leporinus friderici (Bloch, 1794) in the upper Paraná river by ^{Takemoto et al. (2009)}. Thus, A. fasciatus is a new host and enlarges the list of the known intermediate hosts of Cystidicoloides sp. in the São Francisco basin.

In this study, larval specimens of Rhabdochona sp. were also found in A. fasciatus. They had previously been found in C. conirostris by ^{Brasil-Sato & Santos (2005)}. The results obtained in A. fasciatus in this study indicate that foraging fish play a role as intermediate hosts for some species of Rhabdochona Railliet, 1916, thus enlarging the list of hosts in the upper São Francisco river.

Larval specimens of Spiroxys sp. were identified in A. fasciatus in Mexico (^{Moravec, 1998}). In the upper São Francisco river, ^{Santos et al. (2009)} and ^{Santos-Clapp & Brasil-Sato (2014)} reported occurrences of these larvae in the carnivorous fish Cichla kelberi Kulander & Ferreira, 2006). In the present study, these larvae were also found in A. fasciatus, thus showing that this fish acts as an intermediate host for these parasites.

The occurrences of larval specimens of Hysterothylacium sp., Eustrongylides sp. and Goezia sp. in A. fasciatus enlarges the list of hosts in the São Francisco river, especially given that occurrences of these species had already been identified in several families of fish in the upper São Francisco river (^{BRASIL-SATO, 2003}; ^{SANTOS-CLAPP & BRASIL-SATO, 2014}).

Larvae of Brevimulticaecum sp. were first described in fish by ^{Moravec et al. (1997)}, but ^{Bruce et al. (1994)} asserted that fish rarely act as intermediate hosts for Brevimulticaecum sp. According to ^{Moravec (1998)}, amphibians are intermediate hosts for Brevimulticaecum spp. and, as ^{Bruce et al. (1994)} stated, the most common definitive hosts are reptiles. In the Neotropical region (Peru, Venezuela, Nicaragua, Mexico, and Brazil), larvae have been found in the following fish species: A. fasciatus; Gymnotus carapo Linnaeus, 1758; Gymnotus inaequilabiatus (Valenciennes, 1839); Loricariichthys brunneus (Hancock, 1828); Leporinus elongatus Valenciennes, 1850; Leporinus lacustris Amaral Campos, 1945; L. friderici, Hemisorubim platyrhynchos (Valenciennes, 1840); Hoplias malabaricus (Bloch, 1794); Myleus levis Eigenmann & McAtee, 1907; Pseudoplatystoma corruscans (Spix & Agassiz, 1829); Pygocentrus nattereri (Cuvier, 1819); Serrasalmus marginatus (Valenciennes, 1837); Sorubim lima (Bloch & Schneider, 1801); and Rhamdia guatemalensis (Günther, 1864) (^{MORAVEC, 1998}; ^{AGUIRRE-MACEDO et al., 2001}; ^{VIEIRA et al., 2010}). Adult specimens of Brevimulticaecum regoi Sprent, 1990, were found in the rays Potamotrygon motoro (Müller & Henle, 1841) and Potamotrygon castexi Castello & Yagolkowski, 1969, in southeastern Peru (^{REYDA, 2008}). The present study provides the first record of Brevimulticaecum sp. larvae parasitizing A. fasciatus, and this occurrence widens their known geographical distribution in the Neotropical region for the São Francisco river basin. The minimum and maximum values for the measurements on ten larval specimens of Brevimulticaecum sp., followed by their means and standard deviations, are presented in Table 2.

Conclusion

This study highlights occurrences of and quantitative data on eleven species of parasitic nematodes of A. fasciatus in the São Francisco river. The most prevalent species characterizing the nematodes fauna of A. fasciatus were, in larval form, Hysterothylacium sp. and Contracaecum sp., followed by Spiroxys sp., Cystidicoloides sp., and Brevimulticaecum sp; and, in adult form, P. saofranciscencis. Except for Contracaecum sp. and P. saofranciscencis, A. fasciatus represents a new host for these nematode species. These results aid in elucidating the biodiversity of parasites in fish in the Neotropical region; they also add to research projects under development in the São Francisco basin.