Metazoan Parasites of Geophagus proximus, a Cichlidae Fish from the Eastern Amazon (Brazil)

The present study investigated the fauna of metazoan parasites of a Geophagus proximus population from the lower Tapajós River, in the state of Pará, northern Brazil. A total of 137 monogeneans were collected from the gills of G. proximus, including Sciadicleithrum kritskyi, Sciadicleithrum paranaensis and Sciadicleithrum geophagi, while 119 Raphidascaris (Sprentascaris) lanfrediae nematodes and 28 metacercariaes of digenea undetermined were collected from the intestine. Hosts harboring four species of parasites were predominant. The parasites had an aggregated dispersion pattern. The present study represents the first record of S. geophagi parasitizing G. proximus, increasing the geographic distribution of these parasite species to the Tapajós River basin.


Introduction
The Cichlidae Bonaparte, 1840 family comprises the greatest wealth of fish species, with 202 genera and around 1762 species [1].Cichlids are freshwater fish, but some species can tolerate variations in salinity and may invade brackish water [1].The family is widely geographically distributed and contains species with different life habits, with the majority of neotropical species presenting extragenital sexual dimorphism, wide variations in size and shape, diversified coloration and great potential for use in aquariums [1].
Among cichlid species, Geophagus proximus Castelnau, 1855 is endemic to South America, and is distributed in the Ucayali River in Peru and the Solimões-Amazon River, Tocantins River and the Trombetas River in Brazil [2].This benthopelagic fish inhabits riverbanks and lakes, feeding on small fruits, seeds, algae, crustaceans, insect larvae and mollusks [3] [4].Its sexual maturation occurs when it reaches approximately 12 cm in length, and it exhibits split spawning and the habits of incubating the eggs in the mouth and caring for its offspring after hatching [3].
Despite the wide geographical distribution of G. proximus and its importance for fishing, there are few studies on its parasitic fauna.[5] [6] have been registered.For this host from the Ilha Solteira Reservoir, on the Dourados River, in state of São Paulo (Brazil), [7] described Sciadicleithrum kritskyi Bellay, Takemoto, Yamada and Pavanelli, 2009 and Sciadicleithrum paranaensis Bellay, Takemoto, Yamada and Pavanelli, 2009.Austrodiplostomum compactum was also reported in G. proximus from the Nova Avanhandava Reservoir, on the Tietê River, also in the state of São Paulo, Brazil [8].
Knowledge of parasitic infracommunities and their relationships with host fish is of great importance, as parasites play a key role in ecosystems, regulating the abundance and density of natural populations, therefore stabilizing food chains and host community structure [5] [9] [10] [11].The present study therefore aimed to investigate the parasitic fauna of metazoans from G. proximus from Lake Juá in the Tapajós River basin, in the state of Pará, Brazil.

Materials and Methods
In September 2015, 23 specimens of G. proximus were collected in the Juá Lake located on the lower Tapajós River (2˚26'05.8''S54˚46'26.9''W), in the municipality of Santarém, state of Pará, in the eastern Amazon region of Brazil (Figure 1).Gill nets were used to capture the fish (20 and 30 mm of mesh).All the fish were then transported alive to Multiple Production Laboratory for Aquatic Organisms (LAMPOA) of the West Pará Federal University (UFOPA), for parasitological analysis.The identification of G. proximus was through the morphological characteristics [12].The study was carried out in accordance with the principles adopted by the Brazilian College of Animal Experimentation (COBEA).
All the fish were collected pursuant to a collection authorization granted by IBAMA/ICMBio-N˚ 46202-2/2015.After collection, each fish was euthanized by the spinal cord transection method, and the standard length (cm) and total weight (g) were measured.Then the mouth, gills, operculum and fins of each fish were examined to verify the presence of ectoparasites, and the viscera and gastrointestinal tract were analyzed for the presence of endoparasites.The collection, fixation and preparation of the parasites for identification followed the recommendations of [13].The identification of the parasites was in accordance with [6] and [14], following the morphological characteristics.
The ecological terms used (prevalence, mean intensity, mean abundance) were those recommended by [15] and dominance frequency was evaluated in accordance with [16].The degree of dispersion of each parasitic infra-community with prevalence >10% was evaluated using the Green index, as shown by the equation:

Results
A total of 23 specimens of G. proximus measuring x = 11.4 cm ± 1.5 cm and x = 21.0 g ± 8.5 g were analyzed, of which 95.7% were parasitized by one or more metazoan species, with the dominance of monogenoidean species.The species of parasites found were Sciadicleithrum kritskyi Bellay 1).
The species richness of the parasites varied from 0 to 5, although hosts infected by four species predominated (Figure 2).The parasites had an aggregated distribution pattern (Table 2).

Discussion
Different fish species are important hosts for the biological cycle of a variety of endoparasites, due to their behavior and feeding habits, which are important factors in the composition of their endoparasite fauna [9] [10] [18].In the present study of G. proximus, while a total of five species of parasites were found, of which three were monogenoidea, one was nematoda and one was digenea, ectoparasites predominated.The species richness of parasites in G. proximus was similar to that of the same host from the Paraná River basin, in state of Paraná, Brazil [7].On the other hand, it was less rich than that of Geophagus brasiliensis Quoy and Gaimard, 1824 from the Guandu River, in state of Rio de Janeiro, which presented fauna composed of 14 species of parasites [18], none of which occurred in the present study.Such differences are expected for congeneric species and those from different environments.
Aggregate distribution is a common pattern in freshwater fish parasites [19] and has been observed in other species of freshwater fish in Brazil low levels of infection, indicating that this host feeds on small mollusks in the studied environment.Depending on the region of Brazil, G. proximus has been infected by A. compactum [6] [8] and C. heluans [6].However, the species of digenea in G. proximus from the Amazon are unknown.

Conclusion
In conclusion, the parasite community in G. proximus was composed by ectoand endoparasites, with low species richness and moderate infection levels.
Geophagus proximus is an intermediate host for digeneans and R. (S.) lanfrediae.Finally, more studies with parasites of natural populations of G. proximus from different localities of Brazil are suggested, to better understand the parasitic ecology of these host fish.

Figure 1 .
Figure 1.Collection sites of Geophagus proximus in the lower Tapajós River, state of Pará, in Eastern Amazon (Brazil).

Figure 2 .
Figure 2. Species richness of metazoan parasites of Geophagus proximus from the lower Tapajós River, state of Pará, in Eastern Amazon (Brazil).
[10] [18] [20] [21][22].This pattern of parasitic distribution may be influenced by the width of the ecological niche, environmental heterogeneity, and immunological and behavioral differences between individual hosts[2] [10][22] [23][24] as well as indicating little competition between parasites of the same species, which are allowed to occur in great abundance in the same host and at the same infection site.

Table 1 .
Metazoan parasites of Geophagus proximus from the lower Tapajós River, state of Pará, in Eastern Amazon (Brazil).P: Prevalence, MI: Mean intensity, MA: Mean abundance, TNP: Total number of parasites, IS: Infection sites, FD: Frequency of dominance.

Table 2 .
Dispersion index (D), d-statistical test, Green index (G) for the infracommunities of metazoan parasites of Geophagus proximus from the lower Tapajós River, state of Pará, Eastern Amazon (Brazil).