Parasites in Loricariidae from Brazil: checklist and new records for fish from the Brazilian Amazon

Parasitos de Loricariidae do Brasil: checklist e novos registros para peixes da Amazônia brasileira

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Loricariidae is the most species-rich of freshwater fishes, with more than 915 valid species, distributed in 106 genera and six subfamilies (Lithogeneinae, Neoplecostominae, Ancistrinae, Hypoptopomatinae, Hypostominae and Loricariinae) and occurs in Costa Rica, Panama and South America (Alonso, Terán, Aguilera, & Mirande, 2016; Nelson, Grande, & Wilson, 2016). However, the highest occurrence of Loricariidae species is in the Amazon River basin system (Soares et al., 2011). Fish species of this family have size ranging from 2.5 to 61.0 cm and detritivorus feeding habit, since they feed on debris, algae and invertebrates associated with the sediments of water bodies (Soares et al., 2011). Some species of Loricariidae such as Ancistrusleucostictus Günther, 1864; Ancistrus Rafinesque, 1815, Hypostomus ventromaculatus Boeseman, 1968 and Hemiancistrus Bleeker, 1862 are known for the Igarapé Fortaleza, a tributary of the Amazon River in the State of Amapá, eastern Amazon region (Brazil), the locality of this study. Loricariid species are fish that occupy a lower position in the food chain (Soares et al., 2011), thus they have a low parasitic fauna (Gonçalves, Oliveira, Santos, & Tavares-Dias, 2014).

Parasites play an important role in ecosystems, since they can regulate the abundance of host fish populations, destabilize food chains and alter the structure of communities of hosts (Luque & Poulin, 2007; Lagrue, Kelly, Hicks, & Poulin, 2011; Cardoso, Oliveira, Neves & Tavares-Dias, 2017; Baia, Florentino, Silva & Tavares-Dias, 2018). As parasites are components of most ecosystems, occurring in all food webs and at all trophic levels, several vertebrate and invertebrate species serve as hosts for one or more species of parasites (Lagrue et al., 2011; Cardoso et al., 2017; Baia et al., 2018). In wild fish populations, parasite communities differ in richness and diversity according to their behavior, diet of hosts and the parasite life cycle. The different species of fish living in sympatry may present a similar pattern of parasites when compared to species living in allopatry (Cardoso et al., 2017). Thus, this study compared the parasite fauna in A. leucostictus, H. ventromaculatus, Ancistrus sp. and Hemiancistrus sp. from the Igarapé Fortaleza River, and presented a checklist of the parasite species in Loricariidae from Brazil.

Species of Protozoa, Monogenea, Nematoda, Digenea, Acantocephala, Cestoda, Crustacea and Hirudinea were found parasitizing species of Loricariidae from Brazil, but the most frequent taxonomic groups are Monogenea, Digenea and Nematoda (Table 1). However, the greatest species richness is for Monogenea (Figure 2).

The weight, total length and number of examined hosts are listed in Table 2.

A total of 1,559 parasites were collected from 53 fish specimens, which infected gills and gut of hosts. Unilatus unilatus Mizelle et Kritsky, 1967 and Trinigyrus mourei Boeger and Bemont-Jégu, 1994 were the most frequent parasites, infecting four host species, followed by Genarchella gernachella Travassos 1928 and larvae of Raphidascaris (Sprentascaris) Peter and Cassone, 1984. Larvae of Proteocephalus Weinland, 1858 occurred only in one host species. Hypostomus ventromaculatus harbored the highest diversity of parasites, followed by Ancistrus sp. (Table 3).

Figure 1
Collection site of the Loricariidae species in Igarapé Fortaleza basin in the Amapá Satate (Brazil).

Table 1.
Checklist of parasite species in Loricariidae fish from the Brazil.

Table 3
Parasitic indices four Loricariidae species from the Igarapé Fortaleza River, Amapá State, Brazil.

Figure 2
Richness of the parasite taxa in Loricaridae species from the Brazil.

Table 2
Body parameters of Loricariidae species from the Igarapé Fortaleza River, Amapá State (Brazil)

Some patterns of composition and structure of the parasite community in Loricariidae from Brazil were detected: (a) presence of ectoparasites (Protozoa, Monogenea, Crustacea and Hirudinea) and endoparasites (Nematoda, Digenea, Acantocephala and Cestoda); (b) dominance of Austrodiplostomum compactum Lutz, 1928; (c) infracommunities of ectoparasites richer and more diverse than endoparasites; (d) the presence of endoparasites at the larval stage with high prevalence and low abundance; (e) overdispersion of parasites and (f) interspecific associations of parasite infracommunities (Table 1). There are few studies on parasites in Loricariidae species in the Igarapé Fortaleza basin (Gonçalves et al., 2014; Cardoso et al., 2017). However, this was the first study for A. leucostictus, H. ventromaculatus, Ancistrus sp. and Hemiancistrus sp.

In wild fish populations, the parasitic fauna depend on internal and external factors such as: seasonal variations, habitat, limnological characteristics, water body depth, local biota, biological and physiological characteristics of the hosts, trophic level of thost population and geography of region (Dogiel, 1961; Lagrue et al., 2011; Cardoso et al., 2017; Baia et al., 2018). The parasites, including monogeneans, can then be positively or negatively influenced by environmental stressors, mainly by anthropic actions that favor the eutrophication of water bodies, altering the parasites abundance in polluted environments (Takemoto et al., 2009).

Monogenea has life cycle in a single host and, in general, of a same family of fish, such as Loricariidae, which are commonly parasitized by species of Demidospermus, Paranaella, Trinigyrus and Unilatus (Boeger & Vianna, 2006; Braga, Aráujo, & Boeger, 2014). In general, monogeneans are found in low prevalence and abundance in wild fish populations, when the environmental characteristics do not facilitate the reproduction of these ectoparasites (Tavares-Dias, Rigôr, Pinheiro, Oliveira, & Marinho, 2013). Unilatus unilatus and T. mourei have been reported infecting diverse Loricariidae species from Brazil (Table 1), and now also A. leucostictus, Ancistrus sp., H. ventromaculatus and Hemiancistrus sp., which are new hosts for such monogeneans.

Digeneans are parasites of different host species and have mollusks as primary intermediate hosts, and fish can be intermediate, paratenic or definitive hosts (Ferrari-Hoeinghaus et al., 2007; Cardoso et al., 2017). Genarchellagernachella does not have host specificity, since it infects several Characiformes and Siluriformes fish from Brazil, which can be definitive hosts for this digenean specie (Cardoso et al., 2017). Undetermined metacercariae and G. gernachella were found in A. leucostictus, Ancistrus sp. and H. ventromaculatus, but the greatest prevalence occurred in intestine of H.ventromaculatus. This was the first report of G. genarchella for Ancistrus sp., A. leucostictus and H. ventromaculatus.

Species of Raphidascaris (Sprentascaris) are nematodes with little known life cycle, but require fish and aquatic crustaceans as intermediate hosts; in addition amphibians, aquatic insects, zooplankton, etc. which are less likely to be intermediate or paratenic hosts (Moravec, 1998). For A. leucostictus, Ancistrus sp. and Hemiancistrus sp., there were varied infection levels of Raphidascaris (Sprentascaris) sp. Raphidascaris (S.) hipostomi Peter and Cassone, 1984 and Raphidascaris (S.) mahnerti Peter and Cassone, 1984 (Table 1) are known infecting Loricariidae species, but this was the first record of Raphidascaris (Sprentascaris) sp. for A. leucostictus, Ancistrus sp. and Hemiancistrus sp.

Acanthocephalans are endoparasites of fish, birds and mammnal (Cardoso et al., 2017). Gorytocephalus elongorchis Thatcher (1979), a parasite of Loricariidae species (Table 1), was found only in H. ventromaculatos, which are new hosts for this acanthocephalan. Species of Proteocephalus are common cestodes of Siluriformes, which consume planktonic crustaceans (Copepoda and Cyclopoida) that serve as intermediate hosts. Thus, some species of Siluriformes can be definitive hosts, with direct infection after consuming microcrustaceans (Scholz, 1999; Cardoso et al., 2017). Plerocercoids of Proteocephalus sp. were found only in H. ventromaculatus, which can be secondary intermediate host for this endoparasite. In addition, H. ventromaculatos is a new host for Proteocephalus sp.

Ectoparasites were predominant in the examined Loricariidae species, which also had species of endoparasites at the larval stage. The hosts with the highest number of collected samples (H. ventromaculatus and Ancistrus sp.) had a higher richness of parasite species. The species of Loricariidae from Brazil present ecto- and endoparasites, but the predominance is of ectoparasites. Species of monogeneans, digeneans and nematodes are the most diversified parasites in Brazilian Loricariidae.

Dr. M. Tavares-Dias receives a Research Fellowship (# 303013/2015-0) from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil).