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Revista Brasileira de Parasitologia Veterinária

Print version ISSN 0103-846XOn-line version ISSN 1984-2961

Rev. Bras. Parasitol. Vet. vol.26 no.1 Jaboticabal Jan./Mar. 2017  Epub Feb 06, 2017

https://doi.org/10.1590/s1984-29612016074 

Original Article

Nematodes of Astyanax fasciatus (Actinopterygii: Characidae) and their parasitic indices in the São Francisco river, Brazil

Nematoides de Astyanax fasciatus (Actinopterygii: Characidae) e seus índices parasitários do rio São Francisco, Brasil

Flavia Guerra Vieira-Menezes1 

Danielle Priscilla Correia Costa1 

Marilia Carvalho Brasil-Sato2  * 

1Curso de Pós-graduação em Ciências Veterinárias, Universidade Federal Rural do Rio de Janeiro – UFRRJ, Seropédica, RJ, Brasil

2Departamento de Biologia Animal, Universidade Federal Rural do Rio de Janeiro – UFRRJ, Seropédica, RJ, Brasil


Abstract

The endoparasite fauna of Astyanax fasciatus from the upper São Francisco river was investigated and ecological parameters and morphological and morphometric data on the parasites are presented. A total of 74 specimens of banded astyanax were collected downstream from the Três Marias dam, municipality of Três Marias, Minas Gerais (18°12’32”S, 45°15’41”W) in January 2011 and January 2012. Eleven taxa of Nematoda were found: Contracaecum sp.; Hysterothylacium sp.; Goezia sp.; Brevimulticaecum sp.; Procamallanus sp.; Procamallanus (Spirocamallanus) saofranciscencis; Cystidicoloides sp.; Spinitectus rodolphiheringi; Rhabdochona sp.; Spiroxys sp.; and Eustrongylides sp.. The fauna of A. fasciatus consisted of by larval specimens of Contracaecum sp., Hysterothylacium sp., Brevimulticaecum sp., Cystidicoloides sp., and Spiroxys sp., and by adult specimens of P. saofranciscencis, whose prevalence was greater than 10%. Thus, this fish acts as an intermediate host of some species of larval nematodes especially, Anisakidae and Acanthocheilidae (Brevimulticaecum sp., new host record and new locality). It participates in transmitting species such Rhabdochona sp. to carnivorous fish and also acts as a definitive host for P. saofranciscencis and S. rodolphiheringi in the upper São Francisco river.

Keywords:  Anisakidae; Brevimulticaecum sp.; endoparasites; nematodes

Resumo

A fauna endoparasitária de Astyanax fasciatus do alto rio São Francisco foi investigada e os parâmetros ecológicos e os dados morfométricos e morfológicos dos parasitos apresentados. Um total de 74 espécimes de lambaris foi coletado à jusante da barragem de Três Marias, município de Três Marias, Minas Gerais (18°12’32”S, 45°15’41”W), em janeiro de 2011 e de 2012. Onze táxons de Nematoda foram encontrados: Contracaecum sp., Hysterothylacium sp., Goezia sp., Brevimulticaecum sp., Procamallanus sp., Procamallanus (Spirocamallanus) saofranciscencis, Cystidicoloides sp., Spinitectus rodolphiheringi, Rhabdochona sp., Spiroxys sp. e Eustrongylides sp.. A fauna de A. fasciatus foi caracterizada por espécimes larvais de Contracaecum sp., Hysterothylacium sp., Brevimulticaecum sp., Cystidicoloides sp., Spiroxys sp. e por espécimes adultos de P. saofranciscencis, cuja prevalência foi maior que 10%. Assim, o lambari atua como hospedeiro intermediário de algumas espécies de nematoides larvais, especialmente, Anisakidae e Acanthocheilidae (Brevimulticaecum sp., novos hospedeiro e localidade); participa na transmissão de espécies como Rhabdochona sp., para peixes carnívoros, e atua também como hospedeiro definitivo para P. saofranciscencis e S. rodolphiheringi no alto Rio São Francisco.

Palavras-chave:  Anisakidae; Brevimulticaecum sp.; endoparasitos; nematoides

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.

Table 1 Prevalence (%), mean intensity (MI), mean abundance (MA), and their respective standard deviations (SD), followed by amplitude (A), importance of values (IV), and site of infection for nematodes found in Astyanax fasciatus (Cuvier, 1819) of the upper São Francisco river, State of Minas Gerais, Brazil. 

Nematode species P(%) MI ± SD MA ± SD A IV Site
Larval specimens
Anisakidae
Contracaecum sp.
CHIOC n. 37853
58.11 5.70 ± 10.17 3.31 ± 8.22 1-57 Se AC, E, F, AI, PI
Goezia sp. 1.35 1.00 0.01 ± 0.12 1 Sa E
Rhaphydascaridae
Hysterothylacium sp.
CHIOC n. 37854
59.46 4.16 ± 3.89 2.47 ± 3.62 1-19 Se AC, E, F, IC, AI, PI
Acanthocheilidae
Brevimulticaecum sp.
CHIOC n. 37851
10.81 1.88 ± 2.10 0.20 ± 0.88 1-7 Sa AC, IC
Camallanidae
Procamallanus sp. 1.35 3.00 0.04 ± 0.35 3 Sa AC
Cystidicolidae
Cystidicoloides sp.
CHIOC n. 37852
12.16 1.22 ± 0.44 0.15 ± 0.43 1-2 Sa AC, AI
Spinitectus rodolphiheringi* 1.35 1.00 0.01 ± 0.12 1 Sa E
Rhabdochonidae
Rhabdochona sp.** 5.41 8.75 ± 11.03 0.47 ± 2.99 1-25 Sa AC, IC, AI
Gnathostomatidae
Spiroxys sp.
CHIOC n. 37860
22.97 3.59 ± 7.62 0.82 ± 3.88 1-33 Sa AC, E, F, IC
Dioctophymatidae
Eustrongylides sp. 1.35 1.00 0.01 ± 0.12 1 Sa AC
Adult specimens
Procamallanus saofranciscencis
CHIOC n. 37857 (male)
CHIOC n. 37858 (female)
21.62 1.06 ± 0.25 0.23 ± 0.45 1-2 Sa IC, AI
Spinitectus rodolphiheringi 2.70 1.00 0.03 ± 0.16 1 Sa E

Sa = satellite species; Se = secondary species; AC = abdominal cavity; E = stomach; F = liver; IC = intestinal cecum; AI = anterior intestine; PI = posterior intestine.

Developmental stages: *juvenile; **larval and juvenile.

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).

Table 2 Morphometry of the larval specimens of the Contracaecum sp., Hysterothylacium sp., and Brevimulticaecum sp. in Astyanax fasciatus (Cuvier, 1819) of the upper São Francisco river, State of Minas Gerais, Brazil. 

Character of nematodes Contracaecum sp.
Larval specimens (n=10)
Hysterothylacium sp.
Larval specimens (n=10)
Brevimulticaecum sp.
Larval specimens (n=10)
X ± SD Min. Max. X ± SD Min. Max. X ± SD Min. Max.
BodyL
BodyW
3.520 ± 0.833 2.750 4.550 1.695 ± 0.114 1.568 1.833 3.563 ± 0.722 2.155 4.616
0.140 ± 0.038 0.093 0.197 0.062 ± 0.022 0.012 0.078 0.091 ± 0.019 0.050 0.118
EsophagusL
EsophagusW
0.259 ± 0.041 0.201 0.309 0.167 ± 0.016 0.143 0.183 0.442 ± 0.088 0.303 0.550
0.027 ± 0.013 0.015 0.042 * * * 0.018 ± 0.002 0.015 0.020
VentriculusL
VentriculusW
0.055 ± 0.018 0.041 0.083 0.026 ± 0.021 0.015 0.064 0.046 ± 0.007 0.035 0.053
0.023 ± 0.011 0.011 0.032 0.024 ± 0.003 0.020 0.028 0.036 ± 0.005 0.025 0.043
Ventricular appendixL
Ventricular appendixW
0.559 ± 0.120 0.367 0.682 0.821 ± 0.074 0.713 0.880 - - -
* * * * * * - - -
Nerve ring 0.182 ± 0.030 0.144 0.220 0.115 ± 0.010 0.105 0.125 0.124 ± 0.027 0.090 0.153
Excretory * * * 0.111 ± 0.009 0.100 0.125 0.166 ± 0.014 0.143 0.185
Intestinal caecumL
Intestinal caecumW
0.314 ± 0.101 0.227 0.482 0.027 ± 0.001 0.025 0.028 0.215 ± 0.064 0.113 0.370
* * * * * * 0.029 ± 0.006 0.018 0.038
Tail 0.102 ± 0.022 0.074 0.130 0.052 ± 0.003 0.048 0.055 0.089 ± 0.014 0.075 0.113
Tooth * * * * * * 0.004 ± 0.001 0.003 0.004

X = mean; SD = standard deviation; Min. and Max. = minimum and maximum values for the measurement.

Characters: L = length; W = width; -lacks; *not measured.

Table 3 Morphometry of Procamallanus saofranciscencis Moreira, Oliveira & Costa, 1994 (male and female specimens) and Procamallanus sp. (larval specimens) in Astyanax fasciatus (Cuvier, 1819) of the upper São Francisco river, State of Minas Gerais, Brazil. 

Character of nematodes Procamallanus saofranciscencis
Male specimens (n=10)
Procamallanus saofranciscencis
Female specimens (n=7)
Procamallanus sp.
Larval specimens (n=3)
X ± SD Mín. Máx. X ± SD Mín. Máx. sp. 1 sp. 2 sp. 3
BodyL
BodyW
4.410 ± 0.454 3.725 4.998 8.954 ± 3.132 6.250 14.975 1.653 1.260 1.490
0.221 ± 0.033 0.175 0.300 0.321 ± 0.057 0.250 0.425 0.049 0.033 0.045
Buccal
CapsuleL
Buccal
CapsuleW
0.074 ± 0.008 0.063 0.090 0.085 ± 0.026 0.035 0.108 0.048 0.040 0.040
0.074 ± 0.011 0.063 0.084 0.123 ± 0.020 0.103 0.155 0.033 0.150 0.015
Basal ringL
Basal ringW
0.055 ± 0.008 0.045 0.070 0.078 ± 0.007 0.070 0.090 0.025 0.010 0.010
0.008 ± 0.001 0.008 0.010 0.015 ± 0.001 0.013 0.015 0.008 * 0.013
Spiral number 13.8 ± 1.414 12 16 16 ± 1.155 14 18 * - -
Muscular
esophagusL
0.324 ± 0.020 0.285 0.350 0.396 ± 0.046 0.350 0.468
Muscular
esophagusW
0.112 ± 0.013 0.098 0.140 0.139 ± 0.007 0.133 0.150 0.200 0.138 0.125
Glandular esophagusL
Glandular esophagusW
0.502 ± 0.038 0.452 0.570 0.569 ± 0.045 0.530 0.638
0.138 ± 0.020 0.098 0.173 0.166 ± 0.013 0.148 0.183
Nerve ringA 0.191 ± 0.011 0.173 0.208 0.217 ± 0.028 0.178 0.248 * * *
Excretory poreA 0.258 ± 0.026 0.228 0.310 0.313 ± 0.050 0.243 0.390 * * *
SpiculesLa 0.103 ± 0.015 0.080 0.113 - - - * * *
SpiculesS 0.084 ± 0.017 0.063 0.671 * * *
VulvaB - - - 3.748 ± 1.564 2.400 6.76 * * *
Tail 0.185 ± 0.018 0.155 0.215 0.177 ± 0.024 0.140 0.213 * * *

X = mean; SD = standard deviation; Min. and Max. = minimum and maximum values for the measurement.

Characters: L = length; W = width; A = distance from the anterior end of body; B = distance from the posterior end of body; La = large; S = small; -lacks; *not measured; undifferentiated esophagus.

Table 4 Morphometry of larval specimens of Cystidicoloides sp., Rhabdochona sp., and Spiroxys sp. in Astyanax fasciatus (Cuvier, 1819) of the upper São Francisco river, State of Minas Gerais, Brazil. 

Character of nematodes Cystidicoloides sp.
Larval specimens (n=10)
Rhabdochona sp.
Larval specimens (n=10)
Spiroxys sp.
Larval specimens (n=11)
X ± SD Mín. Máx. X ± SD Mín. Máx. X ± SD Mín. Máx.
BodyL 4.615 ± 0.579 3.785 5.704 3.409 ± 1.601 1.646 7.164 2.145 ± 0.402 1.725 2.871
BodyW 0.104 ± 0.027 0.056 0.127 0.078 ± 0.027 0.044 0.127 0.056 ± 0.008 0.043 0.069
VestibuleL 0.097 ± 0.015 0.075 0.125 - - -
VestibuleW 0.004 ± 0.001 0.004 0.005 - - -
Prostom - - - 0.022 ± 0.005 0.015 0.030 - - -
Vestibule
Including prostom
- - - 0.087 ± 0.012 0.065 0.103 - - -
Pseudolabia 0.008 ± 0.002 0.005 0.010 - - - 0.019 ± 0.001 0.018 0.021
Deirids - - - 0.039 ± 0.006 0.034 0.045 0.325 ± 0.030 0.288 0.365
Muscular esophagusL 0.214 ± 0.092 0.148 0.380 0.218 ± 0.066 0.138 0.323 0.115 ± 0.026 0.080 0.150
Muscular esophagusW 0.223 ± 0.006 0.015 0.038 * * * 0.021 ± 0.004 0.015 0.025
Glandular esophagusL 1.601 ± 0.417 1.003 2.208 1.212 ± 0.451 0.480 2.080 0.599 ± 0.168 0.212 0.818
Glandular esophagusW 0.055 ± 0.020 0.023 0.083 * * * 0.046 ± 0.007 0.037 0.058
Nerve ringA 0.158 ± 0.010 0.144 0.168 0.132 ± 0.013 0.110 0.150 0.175*
Excretory poreA 0.229 ± 0.054 0.162 0.285 1.157 ± 0.040 0.095 0.200 0.200 ± 0.016 0.175 0.228
VulvaB - - - 3.1001n - - -
Tail 0.096 ± 0.014 0.075 0.115 1.139 ± 0.035 0.093 0.185 0.084 ± 0.014 0.063 0.118

Characters: L = length; W = width; A = distance from the anterior end of body; B = distance from the posterior end of body; -lacks; *not measured; ★measured near prostom; 1n = 1.

Table 5 Morphometry of Spinitectus rodolphiheringi Vaz & Pereira, 1934 (male, female, and juvenile specimens) in Astyanax fasciatus (Cuvier, 1819) of the upper São Francisco river, State of Minas Gerais, Brazil. 

Character of nematodes Spinitectus rodolphiheringi
male (n=1)
Spinitectus rodolphiheringi
female (n=1)
Spinitectus rodolphiheringi
female juvenile (n=1)
BodyL 2.450 4.400 1.940
BodyW 0.069 0.235 0.137
Spine of anterior region 0.008 0.008 0.008
Spine of posterior region 0.004 0.004 0.004
First ring of spines 0.043 0.081 0.053
Vestibule 0.034 0.040 0.035
Muscular esophagusL 0.150 0.235 0.110
Muscular esophagusW * * *
Glandular esophagusL 0.688 1.043 0.680
Glandular esophagusW * * *
Nerve ringA 0.158 * *
Excretory poreA * 0.188 0.120
SpiculesLa 0.093 - -
SpiculesS 0.060 - -
VulvaB - 0.740 0.295
Eggs ovalL - 0.037 -
Eggs ovalW - 0.023 -
Tail 0.075 * 0.060

Characters: L = length; W = width; A = distance from the anterior end of body; B = distance from the posterior end of body; La = large; S = small; -lacks; *not measured.

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.

Acknowledgements

The authors wish to thank Dr Yoshimi Sato and Dr Edson Sampaio, researchers at the Hydrobiology and Fish-farming Station of CODEVASF, in Três Marias, Minas Gerais, for their assistance throughout the research process. The authors also wish to acknowledge the CEMIG/CODEVASF agreement that provided appropriate facilities for producing this article. “The first author was granted a fellowship by the Brazilian National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq)”.

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Received: June 08, 2016; Accepted: September 19, 2016

*Corresponding author: Marilia Carvalho Brasil-Sato. Departamento de Biologia Animal, Universidade Federal Rural do Rio de Janeiro – UFRRJ, Rodovia BR 465, Km 7, CP 74539, CEP 23851-970, Seropédica, RJ, Brasil. e-mail: mcbsato@ufrrj.br

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