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Community of protozoans and metazoans parasitizing Auchenipterus nuchalis (Auchenipteridae), a catfish from the Brazilian Amazon/Comunidade de protozodrios e metazoarios parasitando Auchenipterus nuchalis (Auchenipteridae) da Amazonia brasileira.

Introduction

Auchenipteridae are Neotropical Siluriformes that are distributed in 113 species and 16 genera, including the genus Auchenipterus Valenciennes, 1840 (Froese & Pauly, 2016). In general, they inhabit still waters and have nocturnal and pelagic habits (Ferraris Jr, 2003; Santos, Merona, Juras, & Jegu, 2004). Given the wide distribution in South America, occurrence in various habitats, carnivorous nature and an upper position in the food web, Auchenipteridae catfishes are good model host in ecological parasitology.

Auchenipterus nuchalis Spix and Agassiz, 1829, the species that is the subject of this study, has a distribution restricted to South America, mostly in the Amazon River basin, lower Tocantins River and in lower courses of some rivers from Suriname, French Guiana (Ferraris Jr, 2003; Froese & Pauly, 2016) and others countries from South America. This species reaches the maximum length of 25 cm. This catfish inhabits the banks of rivers and lakes and has a complete spawning that occurs in flooding season. It is a carnivorous fish that prey upon insects, crustaceans and other aquatic invertebrates (Santos et al., 2004), increasing the probability of this fish to become infected by adults or larvae of parasites. However, there are few studies on parasites of A. nuchalis, and in hosts from Brazil, it was reported only infection by Cucullanus brevispuculus (Moravec, Kohn, & Fernandes, 1997); in Argentina, by Crepidostomum macrorchis (Hamann, 1988; Chemes & Takemoto, 2011); in Paraguay, by Ichthyobodo sp., Trichodina sp., Ergasilus sp., Lernaea sp. (Insaurralde & Romero, 2013) and Creptotrema lamothei (Curran, 2008). Such works are taxonomic studies and therefore there are no reports on the parasites fauna of this Amazonian fish. However, parasites are a very important component of biocenosis and good indicators of environmental changes. Some species of parasites play a key role in the regulation of the abundance of host fish by affecting their growth, fertility and behavior (Morozinska-Gogol, 2015; Camargo et al., 2016; Pantoja, Silva, & Tavares-Dias, 2016). Thus, the aim of this paper was to provide information on the parasitic community and infracommunities in A. nuchalis of the Igarape Fortaleza River, in the state of Amapa, northern Brazil.

Material and methods

Fish and sampling area

From December 2012 to November 2013, 31 specimens of A. nuchalis were collected in the Igarape Fortaleza River (Figure 1) for parasitological analysis. All fish were collected with nets of different mesh sizes (10-30 mm). The present work was developed according to the principles adopted by the Brazilian College of Animal Experiments (COBEA) and with the authorization from ICMBio (# 232761) and with authorization from the Ethics Committee in the Use of Animals of Embrapa Amapa (# 004--CEUA/CPAFAP).

The Igarape Fortaleza basin is an important tributary of the Amazonas river system in the state of Amapa, in the Brazilian eastern Amazon region, and in the estuarine coastal sector. It has a river system with extensive floodplains, constituting physical systems with clogged river, drained by freshwater and connected to a main watercourse, influenced by high rainfalls and tides of the Amazonas River. This tributary eutrophicated by urbanization is widely used for refuge and feeding by many fish species (Gama & Halboth 2004; Tavares-Dias, Neves, Pinheiro, Oliveira, & Marinho, 2013; Pantoja et al., 2016).

Collection procedures and analyses of parasites

All fish were weighed (g) and measured for total length (cm), and then necropsied for parasitological analysis. Each specimen's mouth, opercula, gills and gastrointestinal tract were examined to collect parasites (protozoans and metazoans). Gills were removed and analyzed with the aid of a microscope. To quantify metazoan parasites, each viscera was dissected separately and washed in running water and all the material retained on a 154 |tm mesh was examined with the aid of a stereomicroscope. Previously described techniques were used to collect, fix, conserve, count and stain the parasites (Eiras, Takemoto, & Pavanelli, 2006; Boeger, & Viana, 2006).

To analyze the parasite infracommunities, the ecological terms used were those recommended by Bush, Lafferty, Lotz, & Shostak (1997). The index of dispersion (ID) and the index of discrepancy (D) were calculated using the Quantitative Parasitology 3.0 software to detect distribution pattern for each infracommunity of parasites (Rozsa, Reiczigel, & Majoros, 2000) in species with prevalence >10%. The significance of ID for each parasite species was tested using the d-statistics (Ludwig & Reynolds, 1988). The following descriptors for the parasites community were calculated: (1) species richness, (2) Brillouin diversity index (HB), (3) evenness (E) in association with diversity index, (4) Berger-Parker dominance index (d) and dominance frequency (percentage of the infracommunities in which a parasite species is numerically dominant) (Rohde, Hayward, & Heap, 1995; Magurran, 2004), using the Diversity software (Pisces Conservation Ltd., UK).

Fish data on total weight and length were used to calculate the relative condition factor (Kn) of hosts, which was compared to a standard value (Kn = 1.00) using the Mann-Whitney test (U). Body weight (g) and total length (cm) were used to calculate the relative condition factor (Kn) of fish using the length-weight relationship (W = a[L.sup.b]) after logarithmic transformation of length and weight and subsequent adjustment of two straight lines, obtaining lny = lnA + Blnx (Le-Cren, 1951). The Spearman correlation coefficient (rs) was used to determine possible correlations of parasite abundance with the length and weight, as well as with the species richness and Brillouin diversity of hosts (Zar, 2010).

Results

Specimens of A. nuchalis examined had 19.9 [+ or -] 1.6 cm and 41.4 [+ or -] 11.6 g, and all were parasitized by species of protozoans and/or metazoans, such as Ichthyophthirius multifiliis Fouquet, 1876; Piscinoodinium pilullare Schaperclaus, 1954, Lom, 1981 (Protozoa); Cosmetocleithrum striatuli Abdallah, Azevedo and Luque, 2012 (Monogenoidea), Procamallanus (Spirocamallanus) inopinatus Travassos, Artigas and Pereira, 1928 (Nematoda) and metacercariae of Posthodiplostomum sp. (Digenea). However, protozoan species were predominant (Table 1). For I. multifiliis (ID= 2.134, d= 5.62, D= 0.396), for P. pilullare (ID = 3.382, d= 6.12, D = 0.537) and for P. (S.) inopinatus (ID = 1.846, d = 2.66, D = 0.361) there was aggregated dispersion, while C. striatuli (ID = 0.863, d = -0.44, D = 0.222) showed a uniform dispersion.

The Brillouin diversity index was 0.67 [+ or -] 0.27, species richness was 3.5 [+ or -] 0.8, evenness was 0.43 [+ or -] 0.17 and dominance of Berger-Parker was 0.71 [+ or -] 0.16. However, the predominance was of hosts parasitized by four parasite species (Figure 2). Correlation between the length of hosts and parasite species richness (rs = 0.009, p = 0.961) and the Brillouin diversity (rs = 0.151, p = 0.452) was not found.

There was no correlation between the abundance of I. multifiliis and the length (rs = -0.123, p = 0.542) and weight (rs = -0.152, p = 0.449) of the host, as well as between the abundance of P. pilullare and length (rs = 0.229, p = 0.249) and weight (rs = 0.016, p = 0.936). There was also no correlation between the abundance of C. striatuli and length (rs = 0.066, p = 0.742) and weight (rs = -0.099, p = 0.622) of the hosts. However, a weak correlation between the abundance of P. (S.) inopinatus and the length (rs = 0.469, p = 0.013) and weight (rs = 0.369, p = 0.05) was detected.

For A. nuchalis, the equation of the weight (W) length (L) relationship (Wt = 0.0557[Lt.sup.23315], [r.sup.2] = 0.764) was negatively allometric, indicating greater increase in body weight than in size. The Kn of the hosts (Kn = 1.00 [+ or -] 0.032) was not different from the standard value.

Discussion

Parasites have key functions in the ecosystems, controlling the structure of fish communities (Marcogliese, Gendron, Plante, & Fournier, 2006; Morozinska-Gogol, 2015; Camargo et al., 2016). A variety of abiotic and biotic factors, e.g., pollution, eutrophication, seasonality, environmental changes, etc, and relationships with other species, determine the distribution of organisms, including the parasites (Tavares-Dias, Oliveira, Gongalves, & Silva, 2014; Morozinska-Gogol, 2015; Camargo et al., 2016; Pantoja et al., 2016). The A. nuchalis parasites component community consisted of three species of ectoparasites--I. multifiliis, P. pilullare and C. striatuli, and one species of endoparasites in larval and adult stage, the P. (S.) inopinatus, a nematode of complex life cycle. However, the protozoans I. multifiliis and P. pilullare were dominant because both ectoparasites have direct life cycle and great capacity for reproduction in eutrophic environments (Marcogliese et al., 2006; Pinheiro, Tavares-Dias, Dias, Santos, & Marinho, 2013; Tavares-Dias et al., 2014; Pantoja et al., 2016), such as the ecosystem investigated here (TavaresDias et al., 2014; Pantoja et al., 2016). Therefore, these parasites may be excellent indicators of changes in environmental conditions.

Ichthyophthirius multifiliis and P. pilullare are protozoans that are globally widespread and well-adapted to different environmental conditions, once these parasites have no parasitic specificity to hosts (Omeji, Solomon, & Obande, 2010; Tavares-Dias et al., 2013; Pantoja et al., 2016). These parasites occur mostly in environments with low oxygen levels, as observed in this study (Tavares-Dias et al., 2013). In gills from A. nuchalis, the levels of infection of these protozoans were lower than those reported for some fish species of the same study region (Tavares-Dias et al., 2013; Bittencourt, Pinheiro, Cardenas, Fernandes, & Tavares-Dias, 2014), and were not correlated with the host size, as reported for Hoplosternum littorale (Pinheiro et al., 2013) and Astyanax altiparanae (Camargo et al., 2016). In contrast, for other fish species, the host size has been recognized as a factor influencing the parasites abundance (Omeji et al., 2010; Tavares-Dias et al., 2013).

Cosmetocleithrum striatuli is a monogenoidean dactylogyrid described by Abdallah, Azevedo, and Luque (2012) of Trachelyopterus striatulus Steindachner, 1877, an Auchenipteridae fish from the Guandu River, state of Rio de Janeiro (Brazil). This species of monogenoidean was also verified parasitizing the gills of Trachelyopterus coriaceus and Trachelyopterus galeatus of the Igarape Fortaleza River (Pantoja et al., 2016). In the gills of A. nuchalis of this study, infection by C. striatuli showed uniform dispersion and these high levels of infection were similar to those reported for T. striatulus at the Guandu River (Mesquita, Azevedo, Abdallah, & Luque, 2011). These high infection levels seem to be related to the preference of A. nuchalis for lentic habitats and with environmental eutrophication, because both factors can facilitate the transmission of these ectoparasites with a direct life cycle (Marcogliese et al., 2006; Mesquita et al., 2011). In addition, such results indicate that these fish seem to tolerate heavy infestation by C. striatuli, even though monogenoideans attached to hosts to feed on the gills and epidermis cause increase in production of mucus (Camargo et al., 2016).

In general, digeneans and nematodes larvae dominate the endohelminth parasite fauna of forage fish species (Marcogliese et al., 2006; Lizama, Takemoto, & Pavanelli, 2009). The low infection by metacercariae of Posthodiplostomum sp. in the gills of A. nuchalis suggests that this fish is a secondary intermediate host that consumes mollusks, which are primary intermediate hosts for this digenean that in general have as definitive hosts the fish eating-birds (Marcogliese et al., 2006; Nguyen, Li, Makouloutou, Jimenez, & Sato, 2012; Ritossa, Flores, & Viozzi, 2013). However, the high prevalence and abundance of larval stages and adults of the nematode P. (S.) inopinatus suggests that A. nuchalis, a carnivorous fish (Santos et al., 2004; Froese & Pauly, 2016), is consuming crustaceans in the studied environment. Therefore, A. nuchalis is a definitive host for P. (S) inopinatus, and the presence of this nematode is related to the feeding behavior of this fish. The non-expected low abundance of endoparasite species in A. nuchalis seems to be related to urban eutrophication, which can lead to slight reductions in parasite diversity. In addition, the parasite species composition in different regions may also reflect the local food-web structure and the biodiversity distribution of the various invertebrate groups (Marcogliese et al., 2006; Camargo et al., 2016).

Conclusion

The parasites component community of A. nuchalis was characterized by the presence of species with higher prevalence and abundance, and by low values of parasite species richness. Auchenipterus nuchalis showed a parasite community with dominance of ectoparasites (protozoans and monogenoideans) and low presence of endoparasites with heteroxenous life cycle, indicating that this fish might occupy an intermediate trophic level in the food web. Parasites with direct life cycles like the ectoparasites were, therefore, the most prevalent in this host that inhabit lentic environment, which leads to the accumulation of eggs and larval stages of parasites, especially of these organisms that have a short life-span and high reproduction rate. Therefore, these facts cause the accumulation of these ectoparasites mainly in the lentic habitat of A. nuchalis. Furthermore, parasitism did not affect the body conditions of the hosts and the host size had no influence. Finally, this was the first study on the parasites community of this Amazonian fish host.

Doi: 10.4025/actascibiolsci.v39i1.32836

Acknowledgements

The present work was developed according to the principles adopted by the Brazilian College of Animal Experiments (COBEA) and with authorization from ICMBio (# 23276-1). Dr. M. Tavares-Dias was granted (# 303013/2015-0) a Research Fellowship from Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq, Brazil).

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Received on July 22, 2016.

Accepted on December 14, 2016.

Marcos Tavares-Dias

Empresa Brasileira de Pesquisa Agropecuaria, Embrapa Amapa, Rodovia Juscelino Kubitschek, km 5, 2600, 68903-419, Macapa, Amapa, Brazil. Email: marcos.tavares@embrapa.br

Caption: Figure 1. Collection sites of Auchenipterus nuchalis in Igarape Fortaleza River, a tributary from the Amazon River system (Brazil).

Caption: Figure 2. Species richness of parasites in Auchenipterus nuchalis from Igarape Fortaleza River, a tributary of the Amazon River system (Brazil).
Table 1. Parasite infracommunities in Auchenipterus nuchalis
(n = 31) from Igarape Fortaleza River, a tributary of the
Amazon River system in the state of Amapa (Brazil).
P: Prevalence, MI: Mean intensity, MA: Mean abundance,
TNP: Total number of parasites, FD: Frequency of
dominance, SI: Site of infection.

Parasites                                p (%)    MI

Ichthyophthirius multifiliis             81.5    256.8
Piscinoodinium pilullare                 63.0    195.8
Cosmetocleithrum striatuli                100    28.1
Posthodiplostomum sp. (metacercariae)     7.4     4.0
Procamallanus (Spirocamallanus)           100    411.1
  inopinatus (adults)
Procamallanus (Spirocamallanus)          14.8    213.0
  inopinatus (larvae)

Parasites                                         MA            TNP

Ichthyophthirius multifiliis             209.3 [+ or -] 195.4   5650
Piscinoodinium pilullare                 123.3 [+ or -] 169.6   3329
Cosmetocleithrum striatuli                28.1 [+ or -] 11.2    758
Posthodiplostomum sp. (metacercariae)      0.3 [+ or -] 1.4      8
Procamallanus (Spirocamallanus)           411.1 [+ or -] 3.8    111
  inopinatus (adults)
Procamallanus (Spirocamallanus)           31.6 [+ or -] 95.3    852
  inopinatus (larvae)

Parasites                                Range   FD (%)      SI

Ichthyophthirius multifiliis             0-775    0.53      Gills
Piscinoodinium pilullare                 0-576    0.32      Gills
Cosmetocleithrum striatuli               5-51     0.07      Gills
Posthodiplostomum sp. (metacercariae)     0-7      --       Gills
Procamallanus (Spirocamallanus)          1-20     0.01    Intestine
  inopinatus (adults)
Procamallanus (Spirocamallanus)          0-390    0.08    Intestine
  inopinatus (larvae)
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Title Annotation:texto en ingles
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Publication:Acta Scientiarum. Biological Sciences (UEM)
Date:Jan 1, 2017
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