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Revista Brasileira de Parasitologia Veterinária

On-line version ISSN 1984-2961

Rev. Bras. Parasitol. Vet. vol.22 no.4 Jaboticabal Oct./Dec. 2013

https://doi.org/10.1590/S1984-29612013000400020 

Full Article

Monogeneans (Dactylogyridae) parasitizing gills of Salminus hilarii from a Neotropical reservoir, Brazil

Monogenéticos (Dactylogyridae) parasitando brânquias de Salminus hilarii de uma represa Neotropical, Brasil

Heleno Brandão1  * 

Fábio Hideki Yamada1 

Gislayne de Melo Toledo1 

Edmir Daniel Carvalho2 

Reinaldo José da Silva1 

1Laboratório de Parasitologia de Animais Silvestres - LAPAS, Departamento de Parasitologia, Instituto de Biociências, UNESP - Universidade Estadual Paulista, Botucatu, SP, Brasil

2Laboratório de Biologia e Ecologia de Peixes, Departamento de Morfologia, Instituto de Biociências, UNESP - Universidade Estadual Paulista, Botucatu, SP, Brasil


ABSTRACT

With the aim of creating an inventory of the metazoan gill parasites of Salminus hilarii in the Taquari River, state of São Paulo, Brazil, five species of monogeneans (Anacanthorus contortus, A. bicuspidatus, Annulotrematoides parisellei, Jainus iocensis and Tereancistrum arcuatus) are reported the first time for this host. A total of 28 fish were sampled quarterly between April 2011 and January 2012, with 10 hosts in a lentic ecosystem and 18 in a lotic ecosystem. Quantitative ecological descriptors (prevalence, intensity of infestation and abundance) were calculated for the purpose to comparing the two ecosystems sampled (lentic and lotic ecosystems). However, no quantitative difference between the lentic and lotic ecosystems was observed. The present study has made available a checklist for species of the genus Anacanthorus and their hosts and geographical distribution in the Neotropical region up to the present time.

Key words: Ectoparasite; Monogenea; freshwater fish; Taquari River

RESUMO

Com o objetivo de inventariar os metazoários parasitos de brânquias de Salminus hilarii do rio Taquari, estado de São Paulo, Brasil, cinco espécies de monogenéticos (Anacanthorus contortus, A. bicuspidatus, Annulotrematoides parisellei, Jainus iocensis, e Tereancistrum arcuatus) foram registradas pela primeira vez para o presente hospedeiro. Um total de 28 peixes foi amostrado trimestralmente entre abril/2011 e janeiro/2012, com 10 hospedeiros no ecossistema lêntico e 18 no ecossistema lótico. Os descritores ecológicos quantitativos (prevalência, intensidade de infestação e abundância) foram calculados com o objetivo de comparar os dois ecossistemas amostrados (ecossistema lêntico versus ecossistema lótico). No entanto, nenhuma diferença quantitativa desses foi verificada entre os ecossistemas lêntico e lótico. O presente estudo disponibiliza uma lista de espécies do gênero Anacanthorus, os hospedeiro e distribuição geográfica na região Neotropical até o presente momento.

Palavras-Chave: Ectoparasito; Monogenea; peixe de água doce; rio Taquari

Introduction

Monogeneans included in Dactylogyridae are primarily parasites of the gills of marine and freshwater fish. The class Monogenea is the most diversified group and contains the largest number of species parasitizing Neotropical fish (BOEGER; VIANNA, 2006). Specific monogeneans are common helminths parasitizing bony fish worldwide (AKOLL et al., 2012), which is a factor justifying the importance of taxonomic knowledge of species of this class. Eiras et al. (2011) highlighted the increasing numbers of studies on monogeneans. However, the high number of monogenean species does not necessarily imply that this group has more species than other groups. This may simply have occurred because monogeneans have been more intensively studied than other groups.

Salminus hilarii Valenciennes, 1850, is a freshwater fish popularly known as "tabarana" in Brazil, and is considered to be a migratory species over large distances (BARBIERI et al., 2004). The geographical distribution of this species covers the main Brazilian river basins (Paraná, São Francisco, Tocantins, Amazon and Orinoco) (AGOSTINHO et al., 2007; GRAçA; PAVANELLI, 2007).

The present study underscores and broadens the importance of taxonomic knowledge of species of this parasite group. This is the first study to record occurrences of monogeneans at species level, parasitizing the gills of S. hilarii. Kohn et al. (1985) identified one nematode, two digenean, and two monogenean parasites of S. hilarii, but the last ones were only identified at superfamily level (Dactylogyridae).

The Taquari River, located in the state of São Paulo, is a tributary of the Paranapanema River, which is influenced by the Jurumirim reservoir. From studies on gill parasites of S. hilarii in this context, occurrences of five monogenean species were reported and their quantitative parameters were compared between lentic and lotic ecosystems.

Materials and Methods

Study area

The Jurumirim dam (23° 12′ 17″ S and 49° 13′ 19″ W) is the first of a cascade of dams on the Paranapanema River. The reservoir behind this dam is operated such that it regulates others further downstream. The dam was built in the late 1950s and operations began in 1962 (HENRY; NOGUEIRA, 1999). The Taquari River (23° 15′ 12″ S and 49° 12′ 34″ W), located in the state of São Paulo, is the second largest tributary of the Jurumirim reservoir (HENRY et al., 1999) (Figure 1).

Figure 1. Jurumirim reservoir on the upper Paranapanema River, Brazil. Sampling areas: *lentic and ** lotic ecosystems in the Taquari River (arrow). Source: satellite image from Google Earth Digital Globe 

Fish collection and laboratory procedure

Twenty-eight specimens of S. hilarii from the Taquari River were collected between April 2011 and January 2012 in order to study monogenean parasites. The fish were collected using nylon monofilament gillnets with mesh sizes of 3 to 14 cm and with standardized effort. Nets were deployed at 5:00 pm and gathered in at 7:00 am the following day (total exposure time: 14 h). Limnological parameters such as temperature (°C), pH and dissolved oxygen (mg O2.L-1) were measured with aid of a multi-parameter analyzer. Individuals were measured in terms of standard length (Ls , to the nearest 0.1 mm) and weight (to the nearest 0.1 g). The gills were frozen and subsequently removed and placed in vials containing 5% formalin solution. The parasites collected were preserved in alcohol 70%. Some parasite specimens were mounted unstained in Hoyer's medium in order to study the sclerotized structures, while others were stained with Gomori's trichrome to observe internal organs (EIRAS et al., 2006).

Hierarchical levels of study and statistical analysis

In accordance with Bush et al. (1997), the following community descriptors were calculated at the infracommunity level: prevalence (%), mean intensity of infestation and mean abundance for each parasite species. After checking the assumptions of normality (Lilliefors test), Pearson's linear correlation (r) was applied to examine the relationships between parasite abundance and the limnological parameters. The Mann-Whitney U test was performed to measure the effects of the lentic and lotic ecosystems on the abundance of each parasite species. Yates' corrected X 2 together with Spearman's rank correlation (rs) were also performed on pairs of co-occurring parasite species to investigate possible interspecific associations (i.e. co-operative or antagonistic relationships) (LUDWIG; REYNOLDS, 1988). The Z-test for proportions was performance to check differences in prevalence between infrapopulations of the lentic and lotic ecosystems.

The Berger-Parker index was applied to appraise the numerical dominance trends among parasite species (MAGURRAN, 1988). The variance-to-mean ratio of parasite abundance (dispersion index) and the discrepancy index, computed using the Quantitative Parasitology 3.0 software (RóZSA et al., 2000), were used to detect distribution patterns of the infrapopulations (POULIN, 1993). The Shannon index (H') was calculated to compared the biological diversity of communities in the lentic and lotic ecosystems (MAGURRAN, 1988). The hierarchical levels and terminology used in this study followed Bush et al. (1997) and Poulin (2004) and the significance level used was p < 0.05.

The monogenean species were identified as described by Cohen et al. (2012) and Boeger and Vianna (2006). Voucher specimens were deposited in the Helminthological Collection of the Institute of Biosciences (CHIBB), UNESP, Botucatu, São Paulo, Brazil.

Results

A total of 28 fish were captured and all were parasitized by one or more monogenean species (overall prevalence = 100%). About 35% of the fish examined were parasitized by three parasite species (Figure 2). Calculations on the absolute frequencies of the total parasites collected highlighted Anacanthorus contortus as the most important numerically (53.2%), followed by Annulotrematoides parisellei (20.9%), Tereancistrum arcuatus (15.1%), Jainus iocensis (7.4%) and A. bicuspidatus (3.4%). Salminus hilarii is a new host record for all the monogeneans identified.

Figure 2. Richness and intensity of infection in communities of monogeneans in the gills of Salminus hilarii in the Taquari River, upper Paranapanema River, Brazil. 

The component community was composed of five monogenean species totaling 417 specimens. Among these, 183 were collected in a lentic ecosystem and 234 in a lotic ecosystem, with means of 3.36 ± 7.53 and 2.6 ± 4.21, respectively. Comparing the prevalence and abundance of the component communities of the lotic and lentic ecosystems, no significant difference was observed. Fish from both ecosystems had the same magnitude of species richness and no differences in diversity (H'lentic = 1.19 and H'lotic = 1.27; degrees of freedom = 27; t test = 0.988; p > 0.05).

Comparing the component communities, A. contortus showed high values for quantitative descriptors in both the lentic and the lotic ecosystems, except for the prevalence values. Among these, A. parisellei in the lentic ecosystem stood out with prevalence of 80%. The parasite A. bicuspidatus presented the lowest prevalence and J. iocensis and T. arcuatus presented similar prevalences (Table 1).

Table 1. Prevalence (%), total abundance (TA), mean intensity ± standard error (MI ± SE) and mean abundance (MA) of monogenean species in Salminus hilarii in the Taquari River, upper Paranapanema River, Brazil. 

Monogenean species Lentic ecosystem (n = 10) Lotic ecosystem (n = 18)
% TA MI ± SE MA % TA MI ± SE MA
Anacanthorus contortus 70 109 10.9 ± 4.6 7.6 94.4 114 6.3 ± 1.6 5.7
Anacanthorus bicuspidatus 20 9 0.9 ± 0.6 0.2 16.7 5 0.3 ± 0.1 0.1
Annulotrematoides parisellei 80 31 3.1 ± 0.9 2.5 77.8 56 3.1 ± 0.8 2.5
Jainus iocensis 70 15 1.5 ± 0.4 1.1 33.3 16 0.9 ± 0.4 0.3
Tereancistrum arcuatus 70 19 1.9 ± 0.6 1.3 38.9 45 2.5 ± 0.7 1.0

Significant covariations of abundance were observed between pairs: A. contortus versus A. bicuspidatus, A. contortus versus T. arcuatus and A. parisellei versus T. arcuatus. Significant associations of prevalence were observed between pairs: A. contortus versus A. bicuspidatus and A. parisellei versus A. bicuspidatus (Table 2).

Table 2. Paired associations for monogenean species in Salminus hilarii in the Taquari River, upper Paranapanema River, Brazil. Spearman rank correlation (rs). Significant values *p ≤ 0.05. 

Monogenean species Yates-corrected chi-square (χ2)
1 2 3 4 5
(1) Anacanthorus contortus 18.31* 0.11 4.88* 0.79
(2) Anacanthorus bicuspidatus 0.408* 18.31* 4.01* 10.62*
(3) Annulotrematoides parisellei 0.284 0.013 4.88* 0.79
(4) Jainus iocensis 0.099 −0.007 0.345 1.16
(5) Tereancistrum arcuatus 0.489* 0.310 0.475* −0.115

Anacanthorus contortus had the highest dominance frequency at both sites (0.59 and 0.48 in lentic and lotic ecosystems, respectively). All the parasites had a typically aggregated distribution pattern, and A. bicuspidatus was the monogenean species that showed the highest discrepancy index values (Table 3).

Table 3. Values of variance-to-mean ratio for parasite abundance (ID) and discrepancy index (D) among monogenean parasites of Salminus hilarii in the Taquari River, upper Paranapanema River, Brazil. 

Monogenean species ID D
Anacanthorus contortus 13.256 0.603
Anacanthorus bicuspidatus 3.185 0.868
Annulotrematoides parisellei 3.441 0.520
Jainus iocensis 2.163 0.653
Tereancistrum arcuatus 3.213 0.577

In relation to the limnological variables (Table 4), the Pearson linear correlation (r) only revealed a statistical difference in the abundance of monogeneans in relation to pH: abundance versus temperature (R2 = 0.81; p = 0.09); abundance versus oxygen (R2 = 0.15; p = 0.61); and abundance versus pH (R2 = 0.89; p = 0.05). Considering the months of May to July to be the dry period and October to January to be the rainy period, greater abundance of monogeneans was observed during the rainy period (Figure 3).

Figure 3. Comparison of the abundance of monogeneans parasitizing the gills of S. hilarii in the Taquari River, upper Paranapanema River, Brazil, between the dry period (April to July) and the rainy period (October to January). Significantly different values in Mann-Whitney U test (p < 0.05). 

Table 4. Mean values and standard deviations of monthly limnological parameters in the Taquari River, between April 2011 and January 2012. 

Months Temperature (°C) Oxygen (mg/L) pH
Apr 18 ± 0.9 9.2 ± 0.8 5.8 ± 0.5
July 15.8 ± 0.5 10 ± 0.0 6.3 ± 0.5
Oct 23.8 ± 0.5 10 ± 0.0 7 ± 0
Jan 25 ± 0.8 8 ± 1 7 ± 0

Discussion

The present study reports occurrences of five monogenean species parasitizing S. hilarii in the Taquari River, Brazil. Individual species of Anacanthorus show varying ability to infest closely related host species. Furthermore, subgroups within Anacanthorus, based on the general morphology of the copulatory complex, appear to express high host specificity to familial groups within the Characidae. Because of these traits, species of Anacanthorus may provide valuable models for studying biogeography (KRITSKY et al., 1992). These characteristics may explain the higher abundance and mean intensity of infestations relating to A. contortus.

The genus Anacanthorus has large species diversity. To date, 70 species have been described, mostly from the Amazon region (Table 5). According to Van Every and Kritsky (1992), species diversity among Amazonian fish and their parasites may have resulted from lacustrine resource partitioning, similar to that proposed to explain cichlid diversity in some African lakes (LOWE-MCCONNELL, 1987) and Pliocene diversity in lake Idaho (SMITH, 1975).

Table 5. Checklist of Anacanthorus species and their hosts and geographical distribution in the Neotropical region. 

Species Host Family host Locality Reference
A. acuminatus Triportheus albus Characidae Amazon River, Brazil Kritsky et al. (1992)
Triportheus angulatus Characidae Amazon River, Brazil Kritsky et al. (1992)
Triportheus elongatus Characidae Amazon and Solimões Rivers, Brazil Kritsky et al. (1992)
A. alatus Triportheus albus Characidae Amazon River, Brazil Kritsky et al. (1992)
Triportheus elongatus Characidae Solimões River, Brazil Kritsky et al. (1992)
A. amazonicus Pristobrycon striolatus Serrasalmidae Samaumã Pond and Uatumã River, Brazil Van Every and Kritsky (1992)
Serrasalmus rhombeus Serrasalmidae Agua Branca Igarape, and Pitinga, Uatumã and Negro Rivers, Brazil Van Every and Kritsky (1992)
Serrasalmus rhombeus Serrasalmidae San Martín, Beni and Ichilo Rivers, Bolivia Córdova and Pariselle (2007)
Serrasalmus sp. Serrasalmidae Agua Branca Igarape, and Pitinga and Uatumã Rivers, Brazil Van Every and Kritsky (1992)
A. anacanthorus Pygocentrus nattereri Serrasalmidae Amazon River, Brazil Mizelle and Price (1965)
A. andersoni Triportheus angulatus Characidae Amazon River, Brazil Kritsky et al. (1992)
A. beleophallus Pristobrycon eigenmanni Serrasalmidae Negro River, Brazil Kritsky et al. (1992)
A. bellus Triportheus albus Characidae Amazon River, Brazil Kritsky et al. (1992)
Triportheus elongatus Characidae Amazon and Solimões Rivers, Brazil Kritsky et al. (1992)
Triportheus sp. Characidae Solimões River, Brazil Kritsky et al. (1992)
A. bicuspidatus Salminus brasiliensis Characidae Paraná River, Brazil Cohen et al. (2012)
A. brasilensis Pygocentrus nattereri Serrasalmidae Amazon River, Brazil Mizelle and Price (1965)
A. brevis Brycon melanopterus Characidae Xeruiny River, Brazil Mizelle and Kritsky (1969)
A. brevicirrus Brycon orthotaenia Characidae São Francisco River, Brazil Monteiro et al. (2010)
A. calophallus Triportheus elongatus Characidae Solimões River, Brazil Kritsky et al. (1992)
A. carinatus Triportheus angulatus Characidae Amazon River, Brazil Kritsky et al. (1992)
A. catoprioni Catoprion mento Serrasalmidae Uatumã and Amazon Rivers, Brazil Kritsky et al. (1992)
A. chaunophallus Triportheus angulatus Characidae Amazon River, Brazil Kritsky et al. (1992)
A. chelophorus Triportheus angulatus Characidae Amazon River, Brazil Kritsky et al. (1992)
Triportheus sp. Characidae Solimões River, Brazil Kritsky et al. (1992)
A. cinctus Pristobrycon striolatus Serrasalmidae Samaumã Pond and Uatumã River, Brazil Van Every and Kritsky (1992)
A. cladophallus Serrasalmus spilopleura Serrasalmidae Solimões River, Brazil Van Every and Kritsky (1992)
A. colombianus Oreochromis mossambicus Cichlidae Ruedasuelta Pond, Colombia Kritsky and Thatcher (1974)
Salminus affinis Characidae Jamundi River, Colombia Kritsky and Thatcher (1974)
A. contortus Salminus brasiliensis Characidae Paraná River, Brazil Cohen et al. (2012)
A. cornutus Triportheus angulatus Characidae Amazon River, Brazil Kritsky et al. (1992)
A. crytocaulus Pristobrycon striolatus Serrasalmidae Agua Branca Igarape, Samaumã Pond and Pitinga and Uatumã Rivers, Brazil Van Every and Kritsky (1992)
A. cuticulovaginus Salminus affinis Characidae Jamundi River, Colombia Kritsky and Thatcher (1974)
A. daulometrus Salminus brasiliensis Characidae Paraná River, Brazil Cohen et al. (2012)
A. dipelecinus Roeboides myersii Characidae Solimões and Negro Rivers, Brazil Kritsky et al. (1992)
A. douradensis Salminus brasiliensis Characidae Paraná River, Brazil Cohen et al. (2012)
A. elegans Brycon melanopterus Characidae Janauacá Lake, Brazil Kritsky et al. (1979)
A. euryphallus Triportheus albus Characidae Amazon River, Brazil Kritsky et al. (1992)
Triportheus angulatus Characidae Amazon River, Brazil Kritsky et al. (1992)
Triportheus elongatus Characidae Amazon River, Brazil Kritsky et al. (1992)
A. formosus Triportheus elongatus Characidae Amazon River, Brazil Kritsky et al. (1992)
Triportheus sp. Characidae Solimões River, Brazil Kritsky et al. (1992)
A. franciscanus Brycon orthotaenia Characidae São Francisco River, Brazil Monteiro et al. (2010)
A. furculus Triportheus elongatus Characidae Solimões River, Brazil Kritsky et al. (1992)
A. glyptophallus Triportheus angulatus Characidae Amazon River, Brazil Kritsky et al. (1992)
A. gravihamulatus Pristobrycon eigenmanni Serrasalmidae Uatumã River, Brazil Van Every and Kritsky (1992)
Serrasalmus rhombeus Serrasalmidae Agua Branca Igarape, and Pitinga and Uatumã Rivers, Brazil Van Every and Kritsky (1992)
Serrasalmus rhombeus Serrasalmidae Madre Dios River, Bolvia Córdova and Pariselle (2007)
Serrasalmus sp. Serrasalmidae Agua Branca Igarape, and Pitinga and Uatumã Rivers, Brazil Van Every and Kritsky (1992)
A. hoplophallus Myleus rubripinnis Serrasalmidae Uatumã River, Brazil Kritsky et al. (1992)
A. jegui Pristobrycon eigenmanni Serrasalmidae Uatumã River, Brazil Kritsky et al. (1992)
Pristobrycon sp. Serrasalmidae Uatumã River, Brazil Kritsky et al. (1992
Serrasalmus rhombeus Serrasalmidae San Martín, Beni, Madre Dios and Ichilo Rivers, Bolivia Córdova and Pariselle (2007)
Serrasalmus rhombeus Serrasalmidae Agua Branca Igarape, and Pitinga and Uatumã Rivers, Brazil Van Every and Kritsky (1992)
Serrasalmus spilopleura Serrasalmidae Solimões River, Brazil Kritsky et al. (1992)
Serrasalmus sp. Serrasalmidae Agua Branca Igarape, and Pitinga, Uatumã and Amazon Rivers, Brazil Kritsky et al. (1992)
A. kruidenieri Brycon melanopterus Characidae Janauacá Lake Amazon, Brazil Kritsky et al. (1979)
A. lasiophallus Pristobrycon striolatus Serrasalmidae Agua Branca Igarape, Samaumã Pond and Pitinga and Uatumã Rivers, Brazil Van Every and Kritsky (1992)
A. lepyrophallus Serrasalmus elongatus Serrasalmidae Negro River, Brazil Kritsky et al. (1992)
Serrasalmus sp. Serrasalmidae Amazon and Solimões Rivers, Brazil Kritsky et al. (1992)
A. lygophallus Triportheus angulatus Characidae Amazon River, Brazil Kritsky et al. (1992)
A. maltai Pygocentrus nattereri Serrasalmidae Mamoré River, Brazil Boeger and Kritsky (1988)
A. mastigophallus Pristobrycon eigenmanni Serrasalmidae Uatumã River, Brazil Kritsky et al. (1992)
A. mesocondylus Pristobrycon eigenmanni Serrasalmidae Uatumã and Negro Rivers, Brazil Van Every and Kritsky (1992)
Pristobrycon sp. Serrasalmidae Uatumã River, Brazil Van Every and Kritsky (1992)
Serrasalmus elongatus Serrasalmidae Solimões and Negro Rivers, Brazil Van Every and Kritsky (1992)
Serrasalmus rhombeus Serrasalmidae Agua Branca Igarape, and Pitinga, Uatumã and Negro Rivers, Brazil Van Every and Kritsky (1992)
Serrasalmus spilopleura Serrasalmidae Solimões River, Brazil Van Every and Kritsky (1992)
Serrasalmus sp. Serrasalmidae Agua Branca Igarape, and Pitinga, Uatumã and Solimões Rivers, Brazil Van Every and Kritsky (1992)
A. nanus Triportheus angulatus Characidae Amazon River, Brazil Kritsky et al. (1992)
A. neotropicalis Pygocentrus nattereri Serrasalmidae Amazon River, Brazil Mizelle and Price (1965)
A. palamophallus Pristobrycon eigenmanni Serrasalmidae Uatumã River, Brazil Kritsky et al. (1992)
A. parakruidenieri Salminus brasiliensis Characidae Paraná River, Brazil Cohen et al. (2012)
A. paraspathulatus Mylossoma aureum Serrasalmidae Guandu River, Brazil Azevedo et al. (2010)
Mylossoma duriventris Serrasalmidae Solimões River, Brazil Kritsky et al. (1992)
A. pedanophallus Myleus rubripinnis Serrasalmidae Uatumã River, Brazil Kritsky et al. (1992)
A. pelorophallus Triportheus elongatus Characidae Solimões River, Brazil Kritsky et al. (1992)
A. penilabiatus Colossoma macropomum Serrasalmidae National Department of Public Works against Drought, Brazil Pamplona-Basilio et al. (2001)
Piaractus brachypomus Serrasalmidae National Department of Public Works against Drought, Brazil Pamplona-Basilio et al. (2001)
Piaractus mesopotamicus Serrasalmidae Aquaculture Center (CAUNESP), Brazil Boeger et al. (1995)
Piaractus mesopotamicus Serrasalmidae National Department of Public Works against Drought, Brazil Pamplona-Basilio et al. (2001)
A. periphallus Serrasalmus sp. Serrasalmidae Amazon River, Brazil Kritsky et al. (1992)
A. pithophallus Triportheus angulatus Characidae Amazon River, Brazil Kritsky et al. (1992)
A. prodigiosus Serrasalmus elongatus Serrasalmidae Negro River, Brazil Van Every and Kritsky (1992)
Serrasalmus rhombeus Serrasalmidae Agua Branca Igarape, and Pitinga, Uatumã and Negro Rivers, Brazil Van Every and Kritsky (1992)
Serrasalmus sp. Serrasalmidae Agua Branca Igarape, and Pitinga, Uatumã and Solimões Rivers, Brazil Van Every and Kritsky (1992)
A. quinqueramus Triportheus albus Characidae Amazon River, Brazil Kritsky et al. (1992)
Triportheus elongatus Characidae Amazon River, Brazil Kritsky et al. (1992)
Triportheus sp. Characidae Solimões Rives, Brazil Kritsky et al. (1992)
A. ramosissimus Serrasalmus elongatus Serrasalmidae Solimões River, Brazil Van Every and Kritsky (1992)
A. ramulosus Triportheus albus Characidae Amazon River, Brazil Kritsky et al. (1992)
Triportheus elongatus Characidae Amazon River, Brazil Kritsky et al. (1992)
A. reginae Pygocentrus nattereri Serrasalmidae Solimões River, Brazil, and Amazon River, Loreto, Peru Boeger and Kritsky (1988), Iannacone and Luque (1993)
A. rondonensis Pygocentrus nattereri Serrasalmidae Mamoré River, Brazil Boeger and Kritsky (1988)
Serrasalmus rhombeus Serrasalmidae Madre Dios River, Bolivia Córdova and Pariselle (2007)
A. scapanus Serrasalmus spilopleura Serrasalmidae Solimões River, Brazil Van Every and Kritsky (1992)
A. sciponophallus Serrasalmus elongatus Serrasalmidae Solimões and Negro Rivers, Brazil Van Every and Kritsky (1992)
Serrasalmus rhombeus Serrasalmidae Agua Branca Igarape, and Pitinga, Uatumã and Negro Rivers, Brazil Van Every and Kritsky (1992)
Serrasalmus rhombeus Serrasalmidae San Martin, Beni, Madre Dios and Ichilo Rivers, Bolivia Córdova and Pariselle (2007)
Serrasalmus spilopleura Serrasalmidae Solimões River, Brazil Van Every and Kritsky (1992)
Serrasalmus sp. Serrasalmidae Solimões, Uatumã and Negro Rivers, Brazil Van Every and Kritsky (1992)
A. serrasalmi Pristobrycon sp. Serrasalmidae Uatumã River, Brazil Van Every and Kritsky (1992)
Serrasalmus elongatus Serrasalmidae Solimões and Negro Rivers, Brazil Van Every and Kritsky (1992)
Serrasalmus rhombeus Serrasalmidae Agua Branca Igarape, and Pitinga, Uatumã and Negro Rivers, Brazil Van Every and Kritsky (1992)
Serrasalmus sp. Serrasalmidae Agua Branca Igarape, and Pitinga, Uatumã and Negro Rivers, Brazil Van Every and Kritsky (1992)
A. spatulatus Colossoma bidens Serrasalmidae Janauacá Lake Amazon, Brazil Kritsky et al. (1979)
Colossoma macropomum Serrasalmidae Janauacá Lake Amazon, Brazil Kritsky et al. (1979)
Colossoma macropomum Serrasalmidae Delta Amacuro and Portuguesa, Venezuela Aragort et al. (2002), Centeno et al. (2004)
A. spinatus Myleus rubripinnis Serrasalmidae Uatumã River, Brazil Kritsky et al. (1992)
A. spiralocirrus Brycon amazonicus Characidae Amazon River, Brazil Andrade and Malta (2006)
Brycon melanopterus Characidae Janauacá Lake Amazon, Brazil Kritsky et al. (1979)
A. stachophallus Pygocentrus nattereri Serrasalmidae Amazon and Solimões Rivers, Brazil Kritsky et al. (1992)
Pygocentrus nattereri Serrasalmidae Solimões River, Brazil Boeger and Kritsky (1988)
Pygocentrus nattereri Serrasalmidae Amazon River, Loreto, Peru Iannacone and Luque (1993)
A. stagmophallus Myleus rubripinnis Serrasalmidae Uatumã River, Brazil Kritsky et al. (1992)
A. strongylophallus Triportheus elongatus Characidae Solimões River, Brazil Kritsky et al. (1992)
A. thatcheri Pygocentrus nattereri Serrasalmidae Solimões River, Brazil Boeger and Kritsky (1988)
A. tricornis Triportheus angulatus Characidae Amazon River, Brazil Kritsky et al. (1992)
Triportheus elongatus Characidae Solimões River, Brazil Kritsky et al. (1992)
A. xaniophallus Pristobrycon eigenmanni Serrasalmidae Uatumã River, Brazil Kritsky et al. (1992)
Pristobrycon sp. Serrasalmidae Uatumã and Negro Rivers, Brazil Kritsky et al. (1992)

So far, monogenean species of Anacanthorus have been recorded parasitizing twenty species of fish of the order Characiformes in the Neotropical region: Brycon amazonicus, Brycon melanopterus, Brycon orthotaenia, Catoprion mento, Colossoma bidens, Colossoma macropomum, Myleus rubripinnis, Mylossoma duriventris, Oreochromis mossambicus (= Tilapia mossambica), Piaractus mesopotamicus, Pristobrycon eigenmanni (= Serrasalmus eigenmanni), Pristobrycon striolatus, Pristobrycon sp., Pygocentrus nattereri, Roeboides myersii, Salminus brasiliensis, Serrasalmus elongatus, Serrasalmus rhombeus, Serrasalmus spilopleura, Serrasalmus sp., Triportheus albus, Triportheus angulatus, Triportheus elongatus, Triportheus sp. and Salminus affinis (KRITSKY et al., 1979; KRITSKY et al., 1992; KOHN; COHEN, 1998; FISCHER et al., 2003; ANDRADE; MALTA, 2006; MONTEIRO et al., 2010; COHEN et al., 2012).

The genus Jainus has been recorded in the following hosts in South America: Brycon amazonicus, B. cephalus, B. melanopterus, Chalceus macrolepidotus, Creatochanes affinis, Leporinus copelandii, Moenkhausia sanctaefilomenae, Salminus brasiliensis and Schizodon borellii (MIZELLE et al., 1969; KRITSKY et al., 1980; KOHN; COHEN, 1998; ANDRADE et al., 2001; ANDRADE; MALTA, 2006; TAKEMOTO et al., 2009; KARLING et al., 2011; COHEN et al., 2012). Tereancistrum has been recorded in Brycon amazonicus, B. melanopterus, Leporinus fasciatus, Prochilodus reticulatus and Salminus brasiliensis (KRITSKY et al., 1980; KOHN; COHEN, 1998; ANDRADE; MALTA, 2006; COHEN et al., 2012).

During this study, we observed differences in correlations between the abundance of monogeneans and pH, which possibly influenced the presence or absence of these organisms. However, studies on the physiology of the host are needed in order to confirm the degree of influence of the pH of these organisms.

Regarding parasite dispersion, in most cases, the parasites are almost universally aggregated between their hosts (KRASNOV; POULIN, 2010). That is to say, most of the hosts have few if any parasites, while a small number of hosts are infected with many parasites (POULIN, 1993). This pattern is expected in most animals in nature, as observed regarding monogeneans parasitizing the gills of S. hilarii in the present study, except for A. parisellei in the lentic gradient. This type of distribution is possibly related to variations in the characteristics of the environment or the behavior of living beings that try to group (NERING; ZUBEN, 2010).

According Thomas et al. (2005), considerable progress has been made in understanding the functional value of parasites in ecosystems. Numerous theoretical and empirical studies have shown that parasites, in spite of their small size, are biologically and ecologically important in ecosystems. The influence of monogeneans on fish behavior in nature is difficult to measure, but we considered them within the life history of the host in order to gain better understanding of both organisms within their ecological niches.

Knowledge of the geographical and systematic distribution of monogenean species is also of considerable importance, since these organisms can be used as tools to aid in understanding, conserving and preserving aquatic ecosystems.

The present study provides the first record of occurrences of the monogeneans A. contortus, A. bicuspidatus, A. parisellei, J. iocensis and T. arcuatus parasitizing the gills of the host S. hilarii in the Taquari River in the state of São Paulo, Brazil. This study contributes towards the knowledge of occurrences of these species of parasites in fish of the family Characidae and their geographical distribution, as well as listing the host species and geographical distribution of the genus Anacanthorus in South America.

Acknowledgements

The authors thank Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP process: 2011/22603-3) for the scholarship granted to the first author and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES process: AUX-PE-PNPD 3005/2010). They are grateful to the staff of the Fish Biology and Ecology Laboratory of the Institute of Biosciences, Botucatu, and Universidade Estadual Paulista (UNESP) for the structure provided for developing this work.

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Received: August 13, 2013; Accepted: November 1, 2013

* Corresponding author: Heleno Brandão, Departamento de Parasitologia, Instituto de Biociências, Universidade Estadual Paulista - UNESP, CEP 18618-970, Botucatu, SP, Brasil, e-mail: heleno_brandao@hotmail.com

Edmir Daniel de Carvalho (in memory)

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