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

The aim of this study was to investigate the parasites fauna of Ancistrus leucostictus, Hypostomus ventromaculatus, Ancistrus sp. and Hemiancistrus sp. from the Igarapé Fortaleza River (Amapá State, Brazil), besides making a checklist of the parasite species in Loricariidae from Brazil. A total of 53 fishes were collected from November 2013 to August 2014. In the hosts, a total of 1,559 parasites of seven taxa were collected: Unilatus unilatus, Trinigyrus mourei, undetermined metacercariae, Genarchella gernachella, Raphidascaris (Sprentascaris) sp., Gorythocephalus elongorchis and Proteocephalus sp. Ectoparasite species were frequent in the examined Loricariidae species, which also had larval stages of endoparasites. The hosts with the highest sampled number, H. ventromaculatus and Ancistrus sp., had the highest parasite species richness. Loricariidae species from Brazil are parasitized by species of Protozoa, Monogenea, Nematoda, Digenea, Acantocephala, Cestoda, Crustacea and Hirudinea, but monogeneans, digeneans and nematodes were the predominant taxa. 


Introduction
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 Ancistrus leucostictus Günther, 1864;Ancistrus Rafinesque, 1815, Hypostomus ventromaculatus Boeseman, 1968and 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.

Study area, fish and locality of collection
The Igarapé Fortaleza basin, located in the municipalities of Macapá and Santana (AP), is formed by a main channel and an extensive area of floodplains that suffer periodic flooding and is strongly influenced by the high rainfall of the Amazon region and the daily tides of the Amazon River, thus providing shelter and feeding for different species of fish. The regional vegetation is composed of plants with characteristics of flooded forests and herbaceous fields, and several species of macrophytes (Thomaz, Costa-Neto, & Tostes, 2004;Tavares-Dias, Oliveira, Gonçalves, & Silva, 2014).
From November 2013 to August 2014, fifty three specimens of A. leucostictus, sp., H. ventromaculatus, Ancistrus sp. and Hemiancistrus sp. were collected in Igarapé Fortaleza River, municipality of Macapá, State of Amapá, Brazil ( Figure 1). All fish were collected with gill nets of different mesh sizes, for parasitological analysis.

Collection procedures and analyses of parasites
All fish were weighed (g) and measured for total length (cm), and then necropsied for parasitological analysis. The mouth, opercula, gills and gastrointestinal tract were examined to collect the parasites (protozoans and metazoans). Gills were removed, fixed in formalin 5% and analyzed with the aid of a microscope. To quantify metazoan parasites, each viscera was dissected separately and washed with sodium chloride solution (0.85%) and examined under a stereomicroscope.
A review on the parasites of Loricariidae species in Brazil was performed by searching databases (SciELO, ISI, Scopus, Science Direct, Zoological Records, CAB Abstracts databases and Google Scholar), and available data regarding the parasitic fauna were added to Table 1.
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). Acta Scientiarum. Biological Sciences, v. 40, e40621, 2018

Discussion
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; 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 (Gonçalveset 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 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.

Conclusion
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.