INTRODUCTION

Fish are the main sources of protein for many Amazonian riverine populations, which have the highest per capita fish consumption in the world (^{Petrere Júnior et al. 2007}; ^{Isaac et al. 2015}). Many species of different Characiformes fish are consumed in the Amazon region, mainly Colossoma macropomum Cuvier, 1818, known locally as tambaqui. This omnivorous fish is exclusively frugivorous during the adult phase and, during the juvenile phase, tends to feed on zooplankton, mainly on cladocerans, copepods and chironomids (^{Soares et al. 2011}; ^{Morais and O´Sullivan 2017}). One important point that has been highlighted is the trophic level of the wild fish population in determining the abundance and species richness of parasites (^{Takemoto et al. 2009}; ^{Poulin and Leung 2011}; ^{Oliveira et al. 2017}; ^{Tavares-Dias et al. 2017}).

Parasitism is one of the most common lifestyles on Earth, but parasites are rarely included in the studies (^{Chambouvet et al. 2015}; ^{Oliveira et al. 2017}). The parasitic fauna of C. macropomum has been studied in floodplain lakes of the middle and lower Solimões River (^{Malta 1984}; ^{Morey and Malta 2016}), and in the lower Amazonas River, in the state of Pará (^{Fischer et al. 2003}) These studies reported that wild C. macropomum populations harbor ectoparasite and endoparasite species of diverse taxa, which display a variety of strategies in their life cycles, which may be either direct or indirect. In fish, body size of hosts has emerged also as a significant predictor of the burden of parasites (^{Poulin 2004}; Poulin and Leung 2011). In addition, factors such as the ecology of both freshwater fish and parasites, as well as environmental conditions, influence parasite fauna in populations of wild fish (Fischer et al. 2003; Poulin and Leung 2011; Oliveira et al. 2017;^{Tavares-Dias et al. 2017}). Considering the wide distribution of tambaqui in Amazon river systems, the parasitic fauna of natural populations of tambaqui has been little addressed. The aim of this study was therefore to investigate the parasitic fauna of metazoans in C. macropomum from the lower Jari River, a tributary of the Amazonas River in the State of Pará, northern Brazil.

MATERIAL AND METHODS

Fish and collection site

Between October and December 2016 (low river season), 34 specimens of C. macropomum (29.8 ± 5.6 cm total length and 774.8 ± 481.9 g body mass) were collected in the lower Jari River, in the municipality of Gurupá, State of Pará, northern Brazil (Figure 1). The fish were caught using gill nets, with mesh sizes from 50 to 70 mm, under authorization of ICMBio license # 44268-4.

Figure 1 Site of collection of Colossoma macropomum for parasitological analyses in the lower Jari River, and its location in the south of the state of Pará, in northern Brazil. This figure is in color in the electronic version. 

The Jari River is an important tributary of the Amazonas River in the eastern Amazon, Brazil. It rises in the Park of the Tumucumaque Mountains, on the Suriname-Brazil border and flows to the South of the state of Amapá. The basin of the Jari River from its mouth is strongly influenced by the daily tides of the Amazonas River (^{EPE 2011}) and by the presence of a varied amount of suspended organic matter (^{Abreu and Cunha 2015}).

This study was developed in accordance with the principles recommended by the Brazilian College of Animal Experimentation (Cobea) and with the authorization from Ethics Committee in the Use of Animals of Embrapa Amapá (# 004 - CEUA/CPAFAP).

RESULTS

All the fish examined were parasitized by species of Monogenea, Nematoda, Acanthocephala, Digenea, Crustacea, Acarina and Hirudinea, but the dominance was of monogenean species (Table 1). The parasites presented aggregate dispersion, except for Contracaecum sp., that had uniform dispersion, and Procamallanus (S.) inopinatus that had random dispersion (Table 2). A total of 4966 parasites were collected, between ecto- and endoparasites, but the component community was dominated by ectoparasite species. Percentage of ectoparasites was 73.3% and percentage of endoparasites was 26.7%. In addition, four species of endoparasites larvae were found.

The species richness varied between 1 and 9 (4.9 ± 1.9), the Brillouin index between 0 and 1.52 (0.80 ± 0.42), evenness between 0 and 0.63 (0.31 ± 0.17) and the Berger-Parker dominance index between 0.39 and 1.00 (0.69 ±0.21). There was a predominance of hosts with 4 - 6 species of parasites (Figure 2). The length and body weight of the hosts was significantly and positively correlated with species richness of parasites (rs = 0.38, p = 0.02, and rs = 0.53, p = 0.001, respectively), but had no significant correlation with the Brillouin diversity index (rs = 0.21, p = 0.23, and rs = 0.23, p = 0.19, respectively).

Figure 2 Species richness of metazoan parasites in Colossoma macropomum from the lower Jari River, in the state of Pará (Brazil). 

The length of hosts was not correlated with the abundance of parasite species, but the body weight showed a weak positive correlation only with the abundance of M. bogeri (rs = 0.36, p = 0.04) and L. brinkmanni (rs = 0.45, p = 0.009), and positive correlation with the abundance of E. turucuyus (rs =0.52, p = 0.02).

DISCUSSION

In wild fish populations, richness and diversity of parasites are affected by the relationship of the parasite community with the trophic level and life stage of the host, physical and chemical environmental factors, and presence of viable intermediate hosts (^{Takemoto et al. 2009}; ^{Fischer et al. 2003}; ^{Tavares-Dias et al. 2017}; ^{Oliveira et al. 2017}). Colossoma macropomum from the lower Jari River were parasitized by four species of monogeneans, three nematodes, one acanthocephalan, one digenean, four crustaceans, one mite and one leech, but with dominance of monogeneas and overdispersion of parasites. For C. macropomum from the middle Solimões River and lower Amazonas River, three species of monogeneans, two nematodes, acanthocephalan, one digenean and two crustaceans were reported (Fischer et al. 2003). The diversity of endoparasites in C. macropomum is due to the mode of life of this migrating fish, and mainly to its diet in the juvenile phase, that consists mainly of cladocerans, copepods and chironomids (^{Soares et al. 2011}; ^{Morais and O’Sullivan 2017}), which are intermediate hosts of endoparasites.

Monogeneans are common ectoparasites in the parasitic community of freshwater fish in various lentic environments, which favor the swimming of the larval form (oncomiracidium) to find hosts in their direct life cycle (^{Dogiel 1961}; ^{Tavares-Dias et al. 2017}). Populations of C. macropomum, as the one studied here, prefer sites with nutrient-rich waters and near the margin of rivers and lakes (^{Morais and O’Sullivan 2017}), which would explain the diversity and dominance of monogeneans in the Jari River. The levels of infection by monogeneans in our samples were higher than those described by ^{Fischer et al. (2003}) for C. macropomum in the Amazonas and Solimões rivers, and may be due to differences in environmental conditions.

Larvae of Spectatus spectatus, Contracaecum sp. and Procamallanus (Spirocamallanus) inopinatus were found in C. macropomum from the Jari River. ^{Fischer et al. (2003}) reported parasitism by Procamallanus sp. and Spirocamallanus sp. in C. macropomum from the Solimões and Amazonas rivers. The level of N. buttnerae infection in C. macropomum from the Jari River was lower than that found by Fischer et al. (2003). Infections by endoparasite species depend on the presence of infective stages in the environment, and the amount of contaminated ingested food items (^{Oliveira et al. 2017}; ^{Tavares-Dias et al. 2017}). Neoechinorhynchus buttnerae were found to accumulate in the C macropomum population with the growth of the host individuals (Fischer et al. 2003). Severe tissue alterations occurred in the intestine of C. macropomum in association with N. buttnerae, including desquamation, abrasion, compression, hypertrophy of goblet cells and disappearance of villi on the mucosa, leukocyte infiltration in the submucosa and muscle layer, metaplasia with loose connective tissue substitution, edema of blood vessels and necrotic foci (^{Matos et al. 2017}).

Metacercariae of Cladorchiidae were found in the gills, intestine and pyloric cecum of C. macropomum from the Jari River, and with higher level of infection then that found in a single individual from the Solimões River (^{Fischer et al. 2003}). These digeneans have a complex life cycle. The cercariae of Cladorchiidae emerge from mollusks, the intermediate host and are eaten by a crustacean, which, in turn, is eaten by the definitive host fish (^{Bullard and Overstreet 2008}), such as C. macropomum, to complete its life cycle.

The community of crustaceans in C. macropomum from the Jari River was composed of Ergasilus turucuyus, A. multicolor, P. gamitanae and Braga patagonica, with dominance of E. turucuyus. ^{Fischer et al. (2003}) reported low infestation of G. jaraquensis and P. gamitanae, and ^{Malta (1984}) found low infestation of Dolops carvalhoi, A. multicolor and Argulus sp. in C. macropomum. However, only the abundance of E. turucuyus had a significant positive correlation with the body weight of the hosts. Host body size generally explains only a portion of the interspecific variance in the numbers of parasite species infecting different host species (^{Poulin 2004}; Poulin and Leung 2011), because correlation of parasite abundance with host body size is not universal (Poulin 2004).

We found mites on the gills of C. macropomum. In fish, mites are usually found in the gills, integument, and digestive tract, but there are few records of encapsulated larvae on the wall of the pharynx and esophagus, and adults in a variety of vertebrates, including fish and piscivorous birds (^{Lizama et al. 2013}). ^{Takemoto et al. (2009}) also reported infestation of mites in Geophagus proximus and Serrasalmus marginatus from the Paraná River (Brazil). This low infection by leeches in the gills of C. macropomum may have been accidental. Similar findings have been also reported by ^{Morey and Malta (2016}) for C. macropomum.

CONCLUSIONS

The parasitic community of Colossoma macropomum in the lower Jari River was characterized by the first time, and ectoparasites with high prevalence and abundance, as well as endoparasites in the larval stage were found. This was the first report of Ergasilus turucuyus for C. macropomum. There was a high overdispersion of parasites, low parasite species richness and low evenness, but with moderate Brillouin diversity. Finally, host size was not a factor structuring the parasite community, because the length of hosts did not influence parasite abundance, while body weight of hosts had little influence on abundance.