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Host-parasite interaction between crustaceans of six fish species from the Brazilian Amazon/Interacao hospedeiro-parasite entre crustaceos de seis especies de peixes da Amazonia brasileira.


Crustaceans are zooplankton that may influence the preferential habitats of fish due to their dual role of potential prey and parasite (Semmens, Luke, Bush, McCoy, & Johnson, 2006; Piasecki & Avenant-Oldewage 2008). Fish may be parasitized by species of crustaceans of various taxa, especially Copepoda, Branchiura and Isopoda. In Brazil, 136 species of crustaceans are listed for parasitizing freshwater fish, most of which are Copepoda (about 60%), followed by Isopoda (about 20%) and Banchiura (about 20%) (Luque, Vieira, Takemoto, Pavanelli, & Eiras, 2013). Some crustacean species are host and site-specific, whereas other parasites frequently have no preference (Hoshino, Hoshino, & Tavares-Dias, 2014; Tavares-Dias, Dias-Junior, Florentino, Silva, & Cunha, 2015) due to the evolution in the host-parasite relationship (Morley, 2007). Several species have a wide distribution pattern at different localities, whereas others develop a well-restricted geographical pattern (Tavares-Dias et al., 2015). Moreover, some crustacean species may affect fish breathing when they parasitize their gills, with negative influence on hosts' swimming and growth (Semmens et al., 2006; Guidelli, Isaac, Takemoto, & Pavanelli, 2003), causing negative impact to fishing and aquaculture.

During decades, some hydrographic basins and sub-basins in the Brazilian Amazon have undergone severe social and environmental impacts due to the construction of reservoirs for the production of electric power (Tundisi, Matsumura-Tundisi, & Tundisi, 2008). The case of the Araguari basin river, in the state of Amapa, northern Brazil, is typical, where the Coaracy Nunes Reservoir (Coaracy Nunes HPP) has been operating for more than 30 years. The most abundant fish species in this reservoir, the oldest of the region, are Ageneiosus ucayalensis Castelnau, 1855 (Auchenipteridae), Hemiodus unimaculatus Bloch, 1794 (Hemiodontidae), Serrasalmus gibbus Castelnau, 1855 (Serrasalmidae), Geophagus proximus Castelnau, 1855 (Cichlidae), Acestrorhynchus falcirostris Cuvier, 1819 (Acestrorhynchidae) and Psectrogaster falcata Eigenmann and Eigenmann, 1889 (Curimatidae) (Sa-Oliveira, Vasconcelos, Pereira, Isaac-Nahum, & Teles-Junior, 2013), each with a different life history. Moreover, the parasitic fauna of these Amazonian fish species is not yet known.

In wild fish populations, parasitic crustaceans may be influenced by factors related to the host's life history, which includes environment, body size, physiology, behavior, immunology and diet (Acacio, Varella, & Malta, 2012; Carvalho, Del-Claro, & Takemoto, 2003; Fontana, Takemoto, Malta, & Mateus, 2012; Guidelli, Takemoto, & Pavanelli, 2009; Walker, Harris, Velde, & Bonga, 2008). Besides the lack of information on the parasite species that occur in these fish species, the variables that influence the parasite assemblage structure are also unknown. Therefore, information on the variables affecting the assemblage structure is important for in-depth knowledge of the host-parasite interaction (Fontana et al., 2012; Guidelli et al., 2009; Morley, 2007; Tavares-Dias, Oliveira, Goncalves, & Silva, 2014).

The host-parasite interactions between crustaceans and six fish species of a reservoir from eastern Amazon, northern Brazil, were investigated. The environmental variables that affect this interaction will also be assessed.

Material and methods

Study area

Current analysis was conducted in the reservoir of the Coaracy Nunes Hydroelectric Power Plant (Figure 1) on the middle Araguari river, municipality of Ferreira Gomes, state of Amapa, northern Brazil (00[degrees]54'11.8"N; 51[degrees]15'35.5"W). The reservoir has a drainage area of 23.5 [km.sup.2] with a mean depth of 15 m. Around the reservoir there are two riverine communities (Paredao and Caldeirao) coupled to agricultural areas and private properties for leisure and recreation (Sa-Oliveira et al., 2013). The reservoir has areas with few aquatic macrophytes, mainly Eichornia crassipes and Eleocharis sp., and a large amount of decaying arboreal vegetation due to non-deforestation.

Hosts fish

Hemiodus unimaculatus is a non-migratory fish that occurs in the undisturbed zones of swamps or in the lower parts of stream. The species is omnivorous, mainly consuming algae, detritus and other aquatic invertebrates. Mature at 11 cm of length, the fish's spawning is limited during the rainy season. P. falcata is a non-migratory and detritivorous benthopelagic fish, feeding on detritus and microorganisms associated with the substrate. Its maximum length is approximately 17.0 cm. G. proximus is a non-migratory and omnivorous benthopelagic fish, mainly feeding on plants, mollusks, insects and other aquatic invertebrates. Its maximum length is approximately 23.0 cm. A. ucayalensis is a non-migratory benthopelagic fish occurring in the undisturbed zones of swamps or the lower sections of streams. It is a carnivorous species, consuming fish, insects and other aquatic invertebrates. Its maximum length is approximately 29.0 cm. A. falcirostris is a piscivorous fish, but young specimens may also consume shrimps. Its maximum length is approximately 40 cm and spawning occurs with greater intensity at the end of the dry season and at the beginning of the flood season. S. gibbus is a piscivorous fish with benthopelagic and non-migratory habits. Its maximum length is approximately 21.0 cm (Froese & Pauly, 2016; Santos, Merona, Juras, & Jegu, 2004).

Sampling design

With bimonthly collections between October 2012 and August 2013, at six distant sampling sites, 889 [+ or -] 498 m (544-1777 m) from each other, in the Coaracy Nunes HPP, (Figure 1), 65 species of P. falcata (18.2 [+ or -] 3.9 cm and 138.4 [+ or -] 96.7 g), 63 A. ucayalensis (16.3 [+ or -] 2.8 cm and 39.7 [+ or -] 18.3 g), A. falcirostris (18.2 [+ or -] 3.2 cm and 62.4 [+ or -] 36.0 g), 56 H. unimaculatus (14.8 [+ or -] 2.3 cm and 51.5 [+ or -] 19.9 g) 36 S. gibbus (10.9 [+ or -] 2.5 cm and 26.9 [+ or -] 36.6 g) and G. proximus (14.4 [+ or -] 4.2 cm and 84.9 [+ or -] 77.5 g) were collected, for the analysis of their crustacean ectoparasites fauna.

Water temperature, pH, electrical conductivity and water dissolved oxygen were obtained with a multi-parameter meter at each of the six sampling sites (YSI 85, USA). A pHmeter (YSI 60, USA) determined pH. Whereas turbidity was obtained by a microprocessed Plus II turbidimeter, transparency was obtained with a Secchi disk. Rainfall rates were retrieved from the National System of Environmental Data (Sinda-INPE) of the Coaracy Nunes Hydro-Meteorological Station (Table 1).

Simple gillnets of different meshes (20, 30, 40, 50, 60 mm), with 100 m in length, were used. Permanence time of each network was 12 hours, with inspections at every two hours. Standard length in centimeters and total weight in grams was obtained for each fish. Its sex was microscopically identified according to methodology by Vazzoler (1996). After collection, the fish were packed in a plastic drum, with 10% formalin, and transported to the Laboratory of Ichthyology and Limnology of the Universidade Federal do Amapa (Macapa, Brazil). Current study was developed following the principles by the Brazilian College of Animal Experimentation (Cobea).


Parasitological analysis

Mouth, tegument and fins of each fish were examined on the spot, immediately after capture, to verify the presence of crustacean ectoparasites.

The collected gills were fixed in 5% formalin and examined with a stereomicroscope for the collection and counting of parasites. The crustaceans' species collected were kept in 70% glycerin-alcohol and prepared for identification according to methods described by Eiras, Takemoto, & Pavanelli (2006). The ecological terms used were those recommended by Bush, Lafferty, Lotz, & Shostak (1997).

The dominance frequency (percentage of infracommunities in which the species is numerically dominant) was calculated according to Rohde, Hayward, & Heap (1995). Dispersion index (ID) and Poluin Discrepancy Index (D) were assessed with Quantitative Parasitology 3.0 software to detect the distribution pattern of each infracommunity of parasites (Rozsa, Reiczigel, & Majoros, 2000) with prevalence [greater than or equal to] 10% and hosts with samples > 30 specimens. ID significance for each infracommunity was tested with d-statistic (Ludwig & Reynolds, 1988).

Data analysis

Standard length and weight data determined the relative condition factor (Kn), comparing parasitized and non-parasitized fish (Le-Cren, 1951) by test t. Spearman's correlation coefficient (rs) was used to determine possible correlations of parasites abundance with length and Kn of hosts. G-test determined the sex effect of the hosts in the prevalence of parasites, and Mann-Whitney test (U), with normal approach of Z, was employed to compare the abundance of species of parasites between male and female hosts (Zar, 2010).

Spearman coefficient (rs) determined possible correlations of prevalence and abundance of parasites in fish species with rainfall rates, water temperature, electrical conductivity, dissolved oxygen, pH, turbidity and transparency using the data of each collection.


Two hundred and ninety-six fish were examined and 878 parasite specimens from three crustacean species were found: Excorallana berbicensis Boone, 1918 (N = 862 specimens), Ergasilus turucuyus Malta & Varella, 1996 (M = 11 specimens) and Argulus chicomendesi Malta & Varella, 2000 (N = 5 specimens). Further, 30.6% of the 62 specimens of A. falcirostris examined were parasitized by E. berbicensis and E. turucuyus; 28.6% of the 56 specimens of H. unimaculatus examined were parasitized by E. berbicensis and E. turucuyus; 34.9% of the 63 specimens of A. ucayalensis examined were parasitized by E. berbicensis only; 40 and 42.9% of the 65 specimens of P. falcata and 14 specimens of G. proximus respectively were parasitized by A. chicomendesi and E. berbicensis; 19.4% of the 36 specimens of S. gibbus examined were parasitized by E. berbicensis only.

High prevalence, mean intensity and dominance of E. berbicensis were assessed for all host species. E. turucuyus and A. chicomendesi presented low prevalence parasites, parasitizing only two infested host species (Table 2). E. berbicensis revealed aggregated dispersion, except in S. gibbus that had random dispersion. E. turucuyus showed random dispersion in A. falcirostris (Table 3).

Non-parasitized specimens predominated in the examined host species whilst none of the host species was parasitized by more than two species of crustacean ectoparasites (Figure 2).

Crustacean parasites were collected at a wide variety of sites in the hosts, such as mouth, gills, pectoral, pelvic, dorsal, anal, caudal fins and tegument of the hosts. The prevalence of parasites in sites of infestation was different, but prevalence was low in S. gibbus. Among the infestation sites, high prevalence was found predominantly on the body surface of the five host species, except G. proximus (Figure 3).


Prevalence and abundance of E. berbicensis was not influenced by the host' sex (Table 4).

There were no significant differences for Kn of parasitized and non-parasitized fish in A. ucayalensis, H. unimaculatus, S. gibbus, G. proximus, A. falcirostris and P. falcata (Table 5).

In the case of A. falcirostris, the abundance of E. berbicensis showed a negative correlation with Kn (rs = -0.259; p = 0.042) of host and a positive correlation with length (rs = 0.258; p = 0.042). For P. falcata, abundance of E. berbicensis correlated with Kn (rs = -0.293; p = 0.018), with no correlation with hosts' length (rs = 0.130; p = 0.302). Abundance of E. berbicensis showed no correlation with Kn (rs = -0.333; p = 0.245) and length (rs = 0.179; p = 0.542) of G. proximus, as well as with length (rs = -0.171, p = 0.209) and Kn (rs = 0.121; p = 0.375) of H. unimaculatus. The abundance of E. berbicensis showed no correlation with length (rs = 0.079; p = 0.536) and Kn (rs = -0.167; p = 0.192) of A. ucayalensis, as well as with length (rs = -0.298; p = 0.078) and Kn (rs = 0.209; p = 0.220) of S. gibbus. In the case of A. falcirostris, there was no correlation of abundance of E. turucuyus with length (rs = -0.017; p = 0.896) and Kn (rs = -0.138; p = 0.286) of hosts.


The prevalence of E. berbicensis was positively correlated with rainfall levels and water temperature for A. falcirostris. In the case of A. ucayalensis, G. proximus and P. falcata, there was also a positive correlation of the prevalence of Corallanidae with water oxygen, temperature and pH levels. Abundance of E. berbicensis was negatively correlated with the oxygen levels for A. ucayalensis whilst the abundance of E. berbicensis was positively correlated with water temperature and pH with those of G. proximus and P. falcata, respectively. No correlation of prevalence and abundance of these limnological parameters was found for S. gibbus and H. unimaculatus (Table 6).


The parasitic crustacean fauna in A. ucayaiensis, H. unimacuiatus, S. gibbus, G. proximus, A. faicirostris and P. faicata consisted of A. chicomendesi, E. turucuyus and E. berbicensis, with dominance of E. berbicensis. Arguius chicomendesi (Acacio et al., 2012; Luque et al., 2013; Tavares-Dias et al., 2015), and E. turucuyus (Malta & Varella, 1996; Luque et al., 2013; Hoshino, Hoshino, & Tavares-Dias, et al., 2014) have been recorded in fish species from Amazon. E. berbicensis is a parasite that is only slightly known in freshwater fish. Similarly, other little known crustacean species were also reported infesting different fish species (see Oda et al., 2015; Tavares-Dias et al., 2015).

Although Excoraiiana Stebbing, 1904 are Corallanidae that occur predominantly in marine environments substrates (Delaney, 1989), they have also been reported parasitizing a few species of marine Teleostei and Chondrichthyes (Williams-Jr & Bunkley-Williams, 1994; Semmens et al., 2006). E. berbicensis, the sole representative of freshwater corallanids, originally described in 1918 by Boone in the zooplankton from Berbice river (British Guiana), parasitized all the hosts analyzed in current study. However, the first reports on E. berbicensis in freshwater fish were given in 1925 and 1936 by Van Name, who detected the parasite in the gills and tegument of L. grossidens from British Guiana. Later, in 1969, Monod reported the same corallanid species on gills of the shark N. brevirostris collected in freshwater areas of French Guiana, in the Amazon region (Stone & Head, 1989). Subsequently, the occurrence of E. berbicensis was reported in A. inermis of the Crustacean Collection of the National Institute of Amazonian Researches (Thatcher, 1995), probably originating from the state of Para, in the eastern Amazon region, Brazil. Therefore, current analysis is the second epidemiological study of E. berbicensis for freshwater fish species.

In the case of reservoirs from the southeastern region of Brazil, Ergasiius sp. and non-identified Cymothoidae were crustaceans parasitizing A. fasciatus, H. affinis, L. castaneus and H. maiabaricus (Paraguassu & Luque 2007). Ergasiius sp. and non-identified Vaigamidae were the crustaceans parasitizing I. iabrosus (Moreira, Ito, Takemoto & Pavanelli, 2005) and A. osteomystax (Tavernari et al., 2009), respectively. In 12 species of hosts from a reservoir in Iran, only Cyprinus carpio, Barbus iacerta and Capoeta trutta were parasitized, and parasitic crustaceans community was constituted only by Lernaea cyprinacea and Tracheiiastes poiycoipus (Bozorgnia, Youssefi, Barzegar, Hosseinifard, & Ebrahimpour, 2012). However, the low richness of the crustacean species in hosts analyzed in current study was similar to other freshwater fish species from different localities in Brazil (Acacio et al., 2012; Moreira et al., 2005; Paraguassu & Luque 2007). Infestations of ectoparasites crustaceans may be influenced by various biotic and abiotic factors (Guidelli et al., 2009; Tavares-Dias et al., 2015), but the fish population density may also be a determining factor in hosts' parasites richness in ecosystems with homogeneous physical and chemical characteristics such as the reservoir studied (Takemoto et al., 2009).

This first study on the crustacean ectoparasites of A. faicirostris, A. ucayaiensis, G. proximus, H. unimacuiatus, P. faicata and S. gibbus showed greater parasitism of E. berbicensis, followed by low infestation of E. turucuyus and A. chicomendesi. Such results indicate a low parasitic specificity of E. berbicensis. However, in Pygocentrus nattereri of the Araguaia river (Brazil), infestations were caused by Arguius sp., D. carvaihoi, Braga patagonica, Amphira branchialis and Asotana sp., predominantly by argulid species (Carvalho, Arruda, & Del-Claro, 2004). Moreover, highest infestation of E. berbicensis occurred in G. proximus and P. falcata, and the lowest in S. gibbus. The highest parasitism of E. turucuyus occurred in A. falcirostris. G. proximus and P. falcata are fish with a sluggish behavior and this feature may have facilitated the establishment of E. berbicensis; contrastingly, S. gibbus is a fish of active behavior. Mamani, Hamel, & Van Damme (2004) argued that the sluggish fish lifestyle could make them more vulnerable to infectious forms of crustacean ectoparasites in the larval stage.

Excorallana berbicensis was collected from the tegument, mouth and gills of A. falcirostris, A. ucayalensis, G. proximus, H. unimaculatus, P. falcata and S. gibbus, predominantly on the tegument of these hosts. In general, Excorallana spp. infests gills, mouth and nasal cavity of marine teleost species (Delaney, 1984; Williams-Jr & Bunkley-Williams, 1994; Semmens et al., 2006). However, it was observed that E. berbicensis has a low restriction to site for infestation and settled mainly on the hosts' tegument which is the largest area available for fixation. The life history of Excorallana species is little known since the marine species of these ectoparasites seem to emerge from the criptofauna for temporarily parasitize fish, microcrustaceans, ascidians, sponges and mollusks (Delaney, 1989). Guzman, Obando, Brusca, & Delane (1988) reported that the females of E. tricornis occidentalis were found associated to substrates during the reproduction period.

Parasitic copepod species have a direct and short lifecycle. Many species find their hosts by close relationship with fish attacking them during their life cycle (Piasecki & Avenant-Oldewage, 2008; Tavares-Dias et al., 2015). E. turucuyus were found only on gills of H. unimaculatus and A. falcirostris and showed similar and low infestation level for the two hosts. However, such infestation levels were lowest than those reported for A. falcatus and A. falcirostris from the Pacaas Novos river, in western Amazon, Brazil (Malta & Varella, 1996). Only females are parasites among the species of Ergasilidae, releasing infective forms that freely swim until they find a fish to infect; the males live freely in the zooplankton (Malta & Varella, 1996; Piasecki & Avenant-Oldewage, 2008).

The infestation of E. berbicensis in A. ucayalensis, H. unimaculatus, S. gibbus, G. proximus, A. falcirostris and P. falcata showed an aggregated dispersion, a typical pattern for parasitic crustacean species of freshwater fish (Hoshino, Hoshino, & Tavares-Dias, 2014; Tavares-Dias et al., 2015). In contrast, there was a random dispersion of E. turucuyus in A. falcirostris and of E. berbicensis in S. gibbus. Such overdispersion may be related to diverse factors, including environmental, ecophysiological and immunological conditions and variations in the parasites' exposure time of host fish, as well as other factors (Poulin, 1993; Mamani et al., 2004; Tavares-Dias et al., 2015; Walker et al., 2008). However, random dispersion pattern may be related to a reduced opportunity to colonize this host (Guidelli et al., 2003).

A. chicomendesi was found only on the tegument of G. proximus and P. falcatus, with low and similar levels of infestation. In the case of P. nattereri and S. marginatus from the Paraguay river, Brazil (Fontana et al., 2012) and in the case of S. rhombeus from the Solimoes river, Brazil (Acacio et al., 2012), low levels of infestation of the same argulid species were also reported. Therefore, A. chicomendesi has low parasitic specificity and causes low parasitism in wild fish populations, although high infestations are known in farmed fish (Acacio et al., 2012). Since aquatic macrophytes are substrates for the reproduction of argulid species (Piasecki & Avenant-Oldewage, 2008), their low abundance may be related to the reduced abundance of these plants in the reservoir under analysis. This is the first record of A. chicomendesi for G. proximus and P. falcata.

The host's sex did not influence the infestation levels of E. berbicensis in the fish under analysis. Guidelli et al., (2009) did not find any difference in the infestation levels by Gamispatulus schizodontis for males and females of Leporinus lacustris from the Parana basin river (Brazil). In spite of the fact that high testosterone levels have been implied in the immunosuppression of males which favors parasitism when compared with that of females (Poulin, 1996), studies have not confirmed this information. Thereby, Tavares, and Luque (2004) argued that differences in parasitic infestation levels between fish sex might be related especially with ecological and behavioral differences between males and females.

Several parasites may have a deleterious effect on hosts, with consequences on body conditions. Thereby, the condition factor of wild and farmed fish populations, a quantitative measure of hosts welfare (Fontana et al., 2012; Guidelli et al., 2009; Hoshino, Hoshino, & Tavares-Dias, 2014), may be successfully employed as a tool to detect such negative effects of parasitism. However, in the hosts under analysis, Kn was not affected by parasitic infestation levels. Guidelli et al., (2009) reported similar results for L. lacustris infested by G. schizodontis. In contrast, in the case of P. nattereri and S. maculatus infested by D. bidentata and Dolops sp. (Fontana et al., 2012) and for Astyanax intermedius infested by Paracymothoa astyanaxi, Kn decreased due to parasitic infestation levels (Gomiero, Souza, & Braga, 2012).

Host size, indicating fish age, has been a factor influencing the infestation levels of ectoparasites crustaceans (Guidelli et al., 2003; Tavares-Dias et al., 2015; Walker et al., 2008). However, the abundance of E. berbicensis and E. turucuyus showed no correlation with the host length in A. ucayalensis, H. unimaculatus, S. gibbus, G. proximus, A. falcirostris and P. falcata, or the correlations were weak. Results may be due to the small length range for A. ucayalensis (12-17 cm), H. unimaculatus (11-18 cm), S. gibbus (7-12 cm), G. proximus (8-17 cm), A. falcirostris (14-19 cm) and P. falcata (12-24 cm). Similarly, in the case of P. nattereri, S. maculatus and S. marginatus of the Paraguay river, no abundance correlation of D. bidentata, D. longicauda, D. sp., A. multicolor, A. chicomendesi and Dipteropeltis hirundo with size of hosts was reported (Fontana et al., 2012).

Wild fish usually coexist in equilibrium with parasites within the environment, but this balance in the parasite-host-environment interactions, when broken by environmental changes, may negatively affect hosts and, consequently, increase their susceptibility to infections by parasitic crustaceans (Carvalho et al., 2003; Fontana et al., 2012; Guidelli et al., 2009; Morley, 2007). Changes in environmental quality have a relevant role in the parasitic infestations of ectoparasites crustaceans. In this study, rainfall and water temperature rates increased the infestation of E. berbicensis on A. falcirostris. Similarly, temperature increase favored the infestation of E. berbicensis on G. proximus, as well as the water pH increase in P. falcata. However, dissolved oxygen levels increased the prevalence of E. berbicensis in A. ucayalensis, but decreased its abundance. Pech, Aguirre-Macedo, Lewis, and Vidal-Martinez (2010) also reported that rainfall influenced the infestation levels by Argulus sp. and Ergasilus sp. on Cichlasoma urophthalmus from the Yucatan Peninsula (Mexico).


High parasitism did not affect the body conditions of A. ucayalensis, H. unimaculatus, S. gibbus, G. proximus, A. falcirostris and P. falcata, with a high abundance of E. berbicensis and low abundance of E. turucuyus and A. chicomendesi. In current study, the aggregation of these hosts may have facilitated E. berbicensis infestations. Results show that the hosts' size and sex were factors that did not influence parasitic infestation levels, although other characteristics of the environment had a strong influence. Since environmental factors influenced infestation levels by E. berbicensis, further studies on the seasonal variation of these ectoparasites may be more conclusive.

Doi: 10.4025/actascibiolsci.v38i1.29601


The authors thank the "Conselho Nacional de Desenvolvimento Cientifico e Tecnologico" (CNPq, Brazil) for the productivity scholarship awarded to Dr. M. Tavares-Dias.


Acacio, M., Varella, A. M. B., & Malta, J. C. O. (2012). The parasitic crustaceans of Serrasalmus rhombeus (Linnaeus, 1776) (Characiformes: Serrasalmidae) from floodplain lakes of the Solimoes river, Central Amazon, Brazil. Neotropical Helminthology, 6(2), 179-184.

Bozorgnia, A., Youssefi, M. R., Barzegar, M., Hosseinifard, S. M., & Ebrahimpour, S. (2012). Biodiversity of parasites of fishes in Gheshlagh (Vahdat) Reservoir, Kurdistan Province, Iran. World Journal of Fish and Marine Sciences, 4(3), 249-253.

Bush, A. O., Lafferty, K. D., Lotz, J. M., & Shostak, A. W. (1997). Parasitology meets ecology on its own terms: (Margolis et al. rev.). The Journal of Parasitology, 83(4), 575-583.

Carvalho, L. N., Arruda, R., & Del-Claro, K. (2004). Host-parasite interaction between the piranha Pygocentrus nattereri (Characiformes: Characidae) and isopods and branchiurans (Crustacea) in the Rio Araguaia basin, Brazil. Neotropical Ichthyology, 2(2), 93-98.

Carvalho, L. N., Del-Claro, K., & Takemoto, R. M. (2003). Host-parasite interaction between branchiurans (Crustacea: Argulidae) and piranhas (Osteichthyes: Serrasalminae) in the Pantanal wetland of Brazil. Environmental Biology of Fishes, 67(3), 289-296.

Delaney, P. M. (1984). Isopods of the genus Excorallana Stebbing, 1904 from the Gulf of California, Mexico (Crustacea, Isopoda, Corallanidae). The Bulletin of Marine Science, 34(1), 1-20.

Delaney, P. M. (1989). Phylogeny and biogeography of the marine isopod Family Corallanidae (Crustacea, Isopoda, Flabellifera). Contributions in Sciences, 409, 1-75.

Eiras, J. C., Takemoto, R. M., & Pavanelli, G. C. (2006). Metodos de estudo e tecnicas laboratoriais em parasitologia de peixes (2a ed., Vol. 1). Maringa, PR: Eduem.

Fontana, M., Takemoto, R. M., Malta, J. C. O., & Mateus, L. A. F. (2012). Parasitism by argulids (Crustacea: Branchiura) in piranhas (Osteichthyes: Serrasalmidae) captured in the Caicara Bay, upper Paraguay river, Pantanal, Mato Grosso State, Brazil. Neotropical Ichthyology, 10(3), 653-659.

Froese, R., Pauly & D. FishBase. (2016). World wide web electronic publication. Available from: <http://>. Access on: Jun. 13, 2016.

Gomiero, L. M., Souza, U. P., & Braga, F. M. S. (2012). Condition factor of Astyanax intermedias Eigenmann, 1908 (Osteichthyes, Characidae) parasitised by Paracymothoa astyanaxi Lemos de Castro, 1955 (Crustacea, Cymothoidae) in the Grande river, Serra do Mar State Park--Santa Virginia Unit, Sao Paulo, Brazil. Brazilian Journal of Biology, 72(2), 379-388.

Guidelli, G., Takemoto, R. M., & Pavanelli, G. C. (2009). Ecologia das infrapopulacoes ectoparasitas das cavidades nasais de Leporinas lacustris (Anostomidae) da planicie de inundacao do alto Rio Parana, Brasil. Acta Scientiarum. Biological Sciences, 31(2), 209-214.

Guidelli, G. M., Isaac, A., Takemoto, R. M., & Pavanelli, G. C. (2003). Endoparasite infracommunities of Hemisorubim platyrhynchos (Valenciennes, 1840) (Pisces: Pimelodidae) of the Baia River, upper Parana River floodplain, Brazil: specific composition and ecological aspects. Brazil. Brazilian Journal of Biology, 63(2), 261-268.

Guzman, H. M., Obando, V. L., Brusca, R. C., & Delane, P. M. (1988). Aspects of the population biology of the marine isopod Excorallana tricornis occidentalis Richardson, 1905 (Crustacea: Isopoda: Corallanidae) at Cano Island, Pacific Costa Rica. The Bulletin of Marine Science, 43(1), 77-87.

Hoshino, M. D. F. G., Hoshino, E. M., & Tavares-Dias, M. (2014). First study on parasites of Hemibrycon surinamensis (Characidae), a host from the eastern Amazon region. Revista Brasileira de Parasitologia Veterinaria, 23(3), 343-347.

Le-Cren, E. D. (1951).The lenght-weitht relationship and seasonal cycle in gonad weight and condition in the perch (Perca fluviatilis). Journal of Animal Ecology, 20(2), 201-219.

Ludwig, J. A., & Reynolds, J. F. (1988). Statistical ecology: a primer on methods and computing, New York, US: Wiley-Interscience Pub.

Luque, J. L., Vieira, F. M., Takemoto, R. M., Pavanelli, G. C., & Eiras, J. C. (2013). Checklist of Crustacea parasitizing fishes from Brazil. Checklist, 9(6), 1449-1470.

Malta, J. C. O., & Varella, A. M. B. (1996). Ergasilus turucuyus sp. n. (Copepoda: Ergasilidae) das branquias de Acestrorhynchus falcatus (Bloch, 1794) e A. falcirostris (Cuvier, 1819) (Characiformes: Characidae) da Amazonia Brasileira. Acta Amazonica, 26(1/2), 69-76.

Mamani, M., Hamel, C., & Van DAmme, P. A. (2004). Ectoparasites (Crustacea: Branchiura) of Pseudoplatystoma fasciatum (surubi) and P. tigrinum (chuncuina) in Bolivian white-water floodplains. Ecologia en Bolivia, 39(2), 9-20.

Moreira, S. T., Ito, K. F., Takemoto, R. M., & Pavanelli, G. C. (2005). Ecological aspects of the parasites of Iheringichthys labrosus (Lutken, 1874) (Siluriformes: Pimelodidae) in reservoirs of Parana basin and upper Parana floodplain, Brazil. Acta Scientiarum. Biological Sciences, 27(4), 317-322.

Morley, N. J. (2007). Anthropogenic effects of reservoir construction on the parasite fauna of aquatic wildlife. EcoHealth, 4(4), 374-383.

Oda, F. H., Graca, R. J., C. Tencatt, L. F. C, Tavares, L. E. R., Froehlich, O., & Takemoto, R. M. (2015). The poorly known Riggia acuticaudata (Crustacea: Isopoda) parasitizing Ancistrus sp. (Siluriformes: Loricariidae) from the Paraguay River basin, Brazil, with comments on its reproductive biology. Comparative Parasitology, 82(1), 25-28.

Paraguassu, A. R., & Luque, J. L. (2007). Metazoarios parasitos de seis especies de peixes do reservatorio de Lajes, estado do Rio de Janeiro. Revista Brasileira de Parasitologia Veterinaria, 16(3), 121-128.

Pech, D., Aguirre-Macedo, M. L., Lewis, J. W., & Vidal-Martinez, V. M. (2010). Rainfall induces time-lagged changes in the proportion of tropical aquatic hosts infected with metazoan parasites. International Journal for Parasitology, 40(8), 937-944.

Piasecki, W., & Avenant-Oldewage, A. (2008). Diseases caused by Crustacea. In J. C. Eiras, H. Segner, T. Wahli, & B. G. Kapoor. (Eds.), Fish diseases (p. 1115-1200). Enfield, US: Science Publishers.

Poulin, R. (1993). The Disparity between observed and uniform distributions: A new look at parasite aggregation. International Journal for Parasitology, 23(7), 937-944.

Poulin, R. (1996). Sexual inequalities in helminth infections: a cost of being male. The American Naturalist, 147(2), 287-295.

Rohde, K., Hayward, C., & Heap, M. (1995). Aspects of the ecology of metazoan ectoparasites of marine fishes. International Journal for Parasitology, 25(8), 945-970.

Rozsa, L., Reiczigel, J., & Majoros, G. (2000). Quantifying parasites in samples of hosts. The Journal of Parasitology, 86(2), 228-232.

Santos, G. M., Merona, B., Juras, A. A., & Jegu, M. (2004). Peixes do baixo Rio Tocantins: 20 anos depois da Usina Hidreletrica Tucurui. Brasilia, DF: Eletronorte.

Sa-Oliveira, J. C., Vasconcelos, H. C. G., Pereira, S. W. M., Isaac-Nahum, V. J., & Teles-Junior, A. P. (2013). Caracterizacao da pesca no reservatorio e areas adjacentes da UHE Coaracy Nunes, Ferreira Gomes, Amapa-Brasil. Biota Amazonia, 3(3), 83-96.

Semmens, B. X., Luke, K. E., Bush, P. G., MCcoy, C. M. R., & Johnson, B. C. (2006). Isopod infestation of posts pawning Nassau grouper around Little Cayman Island. Journal of Fish Biology, 69, 933-937.

Stone, I., & Head, R.W. (1989). Excorallana delaneyi, n. sp. (Crustacea: Isopoda: Excorallanidae) from the Northeastern Gulf of Mexico, with observations on adult characters and sexual dimorphism in related species of Excorallana Stebbing, 1904. Gulf Research Reports, 8(2), 199-211.

Takemoto, R. M., Pavanelli, G. C., Lizama, M. A. P., Lacerda, A. C. F., Yamada, F. H., Moreira, L. H. A., ... Bellay, S. (2009). Diversity of parasites of fish from the upper Parana river floodplain, Brazil. Brazilian Journal of Biology, 69(2), 691-705.

Tavares, L. E. R., & Luque, J. L. (2004). Community ecology of metazoan parasites of the later Juvenile Common Snook Centropomus undecimalis (Osteichthyes: Centropomidae) from the coastal zone of the State of Rio de Janeiro. Brazilian Journal of Biology, 64(3), 523-529.

Tavares-Dias, M., Oliveira, M. S. B., Goncalves, R. A., & Silva, L. M. A. (2014). Ecology and seasonal variation of parasites in wild Aequidens tetramerus, a Cichlidae from the Amazon. Acta Parasitologica, 59(1), 158-164.

Tavares-Dias, M, Dias-Junior, M. B. F., Florentino, A. C., Silva, L. M. A., & Cunha, A. C. (2015). Distribution pattern of crustacean ectoparasites of freshwater fish from Brazil. Brazilian Journal of Veterinary Parasitology, 24(2), 136-147.

Tavernari, F. C., Takemoto, R. M., Guidelli, G. M., Lizama, M. A. P.,

Lacerda, A. C. F., & Pavanelli, G. C. (2009). Parasites of Auchenipterus osteomystax (Osteichthyes, Auchenipteridae) from two different environments, Rosana's reservoir and upper Parana River floodplain, Brazil. Acta Scientiarum. Biological Sciences, 31(1), 49-54.

Thatcher V. E. (1995). Comparative pleopod morphology of eleven species of parasitic isopods from Brazilian fish. Amazoniana, 13(3-4), 305-314.

Tundisi, J. G., Matsumura-Tundisi, T., & Tundisi, J. E. M. (2008). Reservoirs and human wellbeing: new challenges for evaluating impacts and benefits in the neotropics Brazil. Brazilian Journal of Biology, 68(4), 1133-1135.

Vazzoler, A. E. A. M. (1996). Biologia da reproducao de peixes teleosteos: teoria e pratica. Maringa, PR: Eduem.

Walker, P. D., Harris, J. E., Velde, G. V. D., & Bonga, S. E. W. (2008). Effect of host weight on the distribution of Argulus foliaceus (L.)(Crustacea, Branchiura) within a fish community. Acta Parasitologica, 53(2), 165-172.

Williams-Jr., E. H., Bunkley-Williams, L., & Sanner, C. (1994). New host and locality records for copepod and isopod parasites of Colombian marine fishes. Journal of Aquatic Animal Health, 6(4), 362-364.

Zar, J.H. (2010). Biostatistical analysis. New Jersey, US: Prentice Hall.

Received on October 25, 2015.

Accepted on January 12, 2016.

Huann Carllo Gentil Vasconcelos (1) and Marcos Tavares-Dias (1,2) *

(1) Programa de Pos-graduacao em Biodiversidade Tropical, Universidade Federal do Amapa, Macapa, Amapa, Brasil. (2) Embrapa Amapa, Rodovia Juscelino Kubitscheck, Km 5, 2600, 68903-419, Macapa, Amapa, Brasil. *Author for correspondence. E-mail:
Table 1. Physical and chemical parameters of water in the
reservoir of the Coaracy Nunes HPP dam in eastern Amazon,
northern Brazil, at the collection sites of crustacean species
parasitizing six fish.

Parameters                 Mean [+ or -] SD       Range
Temperature ([degrees]C)   27.9 [+ or -] 1.6     25.8-31.8
Electrical conductivity    20.9 [+ or -] 2.2      18.8-26.1
  ([micro]S [cm.sup.-1])
Dissolved oxygen           5.3 [+ or -] 1.1       4.4-6.3
  (mg [L.sup.-1])
Turbidity (NTU)            5.8 [+ or -] 1.5       5.1-7.2
Transparency (m)           1.3 [+ or -] 0.3       0.9-1.7
Rainfall rates (mm)        203.7 [+ or -] 397.5   28.5-541.6

Table 2. Parasitological indexes of crustacean species
parasitizing six fish in a reservoir of the Coaracy Nunes
HPP dam in eastern Amazon, northern Brazil. P: prevalence,
MA: mean abundance, MI: mean intensity, TNP: total number
of parasites.

                   A. falcirostris           A. ucayalensis
                   (N = 62)                  (N = 63)

Parasite species   P      MA     MI    TNP   P      MA    MI    TNP
                   (%)                       (%)

Argulus            0      0     0     0      0      0     0     0
Ergasilus          12.9   0.1   1.1   9      0      0     0     0
Excorallana        22.6   2.2   9.6   134    34.9   1.9   5.6   123

                   G. proximus (N = 14)       H. unimaculatus (N = 56)

Parasite species   P      MA     MI     TNP   P      MA    MI    TNP
                   (%)                        (%)

Argulus            7.1    0.1    1.0    1     0      0     0     0
Ergasilus          0      0      0      0     3.6    0.1   1.0   2
Excorallana        42.9   18.3   42.7   256   28.6   1.1   3.9   63

                      P. falcata (N = 65) S. gibbus (N = 36)

Parasite species   P (%)   MA    MI     TNP   P (%)   MA    MI    TNP

Argulus            6.1     0.1   1.0    4     0       0     0     0
Ergasilus          0       0     0      0     0       0     0     0
Excorallana        38.5    4.3   11.2   279   19.4    0.2   1.0   7

Table 3. Index of dispersion (ID), d-statistic and
discrepancy index (D) for crustacean species parasitizing
six fish species in a reservoir of the Coaracy Nunes HPP
dam in eastern Amazon, northern Brazil.

Parasites species     A. falcirostris         A. ucayalensis

                      ID      d       D       ID      d       D

Ergasilus turucuyus   1.095   0.558   0.869   --      --      --
Excorallana           3.474   9.587   0.837   3.211   8.954   0.760

Parasites species     H. unimaculatus         P. falcata

                      ID      d       D       ID      d        D

Ergasilus turucuyus   --      --      --      --      --       --
Excorallana           3.242   8.444   0.795   4.850   13.646   0.758

Parasites species     S. gibbus

                      ID      d        D

Ergasilus turucuyus   --      --       --
Excorallana           0.829   -0.688   0.784

Table 4. Effect of sex on the prevalence and abundance of
Excoraiiana berbicensis in six fish species of a reservoir of the
Coaracy Nunes HPP dam in eastern Amazon, northern Brazil. G:
test-G; Z: Mann-Whitney with approach in Z.

 Prevalence Abundance

Hosts species    Male   Female   G       p       Z             p

A.falcirostris   21     41       1.324   0.417   0.922   0.356
A. ucayalensis   29     34       0.005   0.843   0.469   0.639
G. proximus      8      6        2.486   0.309   0.904   0.366
H.unimaculatus   37     19       0.944   0.507   1.073   0.283
P.falcata        28     37       0.014   0.889   0.225   0.822
S. gibbus        22     14       2.481   0.275   1.006   0.356

Table 5. Relative condition factor (Kn) of six fish species in a
reservoir of the Coaracy Nunes HPP dam in eastern Amazon,
northern Brazil, parasitized and non-parasitized by crustacean

Host species     Non-parasitized        Parasitized

A.falcirostris   1.000 [+ or -] 0.038   0.999 [+ or -] 0.051
A.ucayalensis    0.999 [+ or -] 0.058   1.000 [+ or -] 0.046
G. proximus      1.000 [+ or -] 0.039   1.000 [+ or -] 0.043
H.unimaculatus   0.999 [+ or -] 0.035   0.999 [+ or -] 0.031
P.falcata        1.000 [+ or -] 0.050   1.000 [+ or -] 0.043
S. gibbus        1.003 [+ or -] 0.098   1.001 [+ or -] 0.130

Host species     t-test   p

A.falcirostris   0.039    0.969
A.ucayalensis    -0.024   0.981
G. proximus      0.007    0.994
H.unimaculatus   -0.007   0.994
P.falcata        -0.008   0. 992
S. gibbus        0.053    0.958

Table 6. Spearman's correlation coefficient (rs) of prevalence
and abundance of Excoraiiana berbicensis with water physical
and chemical parameters for six fish species in a reservoir
of the Coaracy Nunes HPP dam in eastern Amazon, northern
Brazil. * p < 0.05, ** p < 0.001.

Prevalence of parasites

                A. faicirostris    A. ucayalensis     G. proximus

                   rs        p        rs        p       rs        p

Precipitation   0.899 **   0.015    -0.086    0.872    0.621    0.188
Temperature     0.812 *    0.049    0.371     0.468   0.828 *   0.042
Conductivity     -0.058    0.913    -0.257    0.623    0.414    0.414
ph               0.074     0.889    0.522     0.288    0.315    0.543
Transparence     -0.358    0.486      --       --     -0.213    0.685
Oxygen           0.116     0.827   0.886 **   0.019     --       --
Turbidity        -0.406    0.425    -0.086    0.872   -0.414    0.414

Abundance of infestation

Precipitation    0.314     0.544    0.086     0.872    0.676    0.140
Temperature      0.486     0.329    0.029     0.957   0.845 *   0.034
Conductivity     0.429     0.396    0.543     0.266    0.510    0.305
ph               0.289     0.577    -0.116    0.827    0.189    0.720
Transparence     0.088     0.868    0.265     0.612   -0.104    0.844
Oxygen           -0.371    0.468   -0.829 *   0.042   -0.169    0.749
Turbidity        -0.257    0.623    -0.143    0.787   -0.507    0.304

Prevalence of parasites

                       H.          P. faicata         S. gibbus

                  rs       p        rs        p       rs       p

Precipitation   -0.529   0.279    0.143     0.787   -0.086   0.872
Temperature     -0.353   0.492    0.200     0.704   -0.486   0.329
Conductivity    -0.029   0.956    0.086     0.872   -0.143   0.787
ph              0.702    0.120   0.812 *    0.049   0.232    0.658
Transparence    -0.591   0.217    -0.795    0.060   -0.794   0.060
Oxygen          0.353    0.492    0.028     0.957   -0.314   0.544
Turbidity       0.677    0.139    0.429     0.397   0.714    0.111

Abundance of infestation

Precipitation   -0.464   0.354    0.086     0.872   -0.086   0.872
Temperature     -0.377   0.461    0.314     0.544   -0.486   0.329
Conductivity    -0.116   0.827    0.143     0.787   -0.143   0.787
ph              0.721    0.106   0.899 **   0.015   0.232    0.658
Transparence    -0.717   0.109    -0.618    0.191   -0.794   0.060
Oxygen          0.319    0.538    0.143     0.787   -0.314   0.544
Turbidity       0.754    0.084    0.314     0.544   0.714    0.111
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Title Annotation:articulo en portuguese
Author:Vasconcelos, Huann Carllo Gentil; Tavares-Dias, Marcos
Publication:Acta Scientiarum. Biological Sciences (UEM)
Article Type:Ensayo
Date:Jan 1, 2016
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