Community of protozoans and metazoans parasitizing Auchenipterus nuchalis (Auchenipteridae), a catfish from the Brazilian Amazon

Comunidade de protozoários e metazoários parasitando Auchenipterus nuchalis (Auchenipteridae) da Amazônia brasileira

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, Mérona, Juras, & Jégu, 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 (Morozińska-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 Igarapé Fortaleza River, in the state of Amapá, northern Brazil.

Specimens of A. nuchalis examined had 19.9 ± 1.6 cm and 41.4 ± 11.6 g, and all were parasitized by species of protozoans and/or metazoans, such as Ichthyophthirius multifiliis Fouquet, 1876; Piscinoodinium pilullare Schäperclaus, 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.

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

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

The Brillouin diversity index was 0.67 ± 0.27, species richness was 3.5 ± 0.8, evenness was 0.43 ± 0.17 and dominance of Berger-Parker was 0.71 ± 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.

Figure 2.
Species richness of parasites in Auchenipterus nuchalis from Igarapé Fortaleza River, a tributary of the Amazon River system (Brazil).

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 = 0.0557Lt2.3315, r2 = 0.764) was negatively allometric, indicating greater increase in body weight than in size. The Kn of the hosts (Kn = 1.00 ± 0.032) was not different from the standard value.

Parasites have key functions in the ecosystems, controlling the structure of fish communities (Marcogliese, Gendron, Plante, & Fournier, 2006; Morozińska-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, Gonçalves, & Silva, 2014; Morozińska-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 (Tavares-Dias 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, Cárdenas, 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).

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.

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 Científico e Tecnológico (CNPq, Brazil).