Microsoft Word - 29-Bio_15145 546 Original Article Biosci. J., Uberlândia, v. 30, n. 2, p. 546-555, Mar./Apr. 2014 PARASITIC INFECTIONS IN TWO BENTHOPELAGIC FISH FROM AMAZON: THE AROWANA Osteoglossum bicirrhosum (Osteoglossidae) AND OSCAR Astronotus ocellatus (Cichlidae) INFECÇÕES PARASITÁRIAS EM DOIS PEIXES BENTOPELÁGICOS DA AMAZÔNIA: O ARUANÃ Osteoglossum bicirrhosum (Osteoglossidae) E APAIARI Astronotus ocellatus (Cichlidae) Marcos TAVARES-DIAS 1 ; Tayana Jessi Suwa Mesquita SOUSA 2 ; Ligia Rigor NEVES 1 1. Laboratório de Aquicultura e Pesca, Embrapa Amapá, Macapá, AP, Brasil. marcos.tavares@embrapa.br; 2. Universidade Federal do Amazonas - UFAM, Coari, AM, Brasil. ABSTRACT: The parasitic fauna of wild Osteoglossum bicirrhosum from central Amazon (Brazil) and wild Astronotus ocellatus from eastern Amazon (Brazil) as well as the host-parasite relationship were evaluated. 87.5% O. bicirrhosum were parasitized only by Gonocleithrum aruanae (Monogenoidea). 92.8% A. ocellatus were parasitized by Ichthyophthirius multifiliis (Ciliophora), Gussevia asota (Monogenoidea), Posthodiplostomum sp. metacercariae (Diplostomidae), Procamallanus inopinatus adults and Contracaecum larvae (Anisakidae). High levels of infection by G. aruanae occurred in O. bicirrhosum while in A. ocellatus the highest levels of infection were caused by helminthes ectoparasites such as G. asota, and endoparasites such as Posthodiplostomum sp., P. inopinatus and Contracaecum sp. There was a significant (p>0.05) negative correlation between the intensity of helminthes species and the relative condition factor (Kn) from A. ocellatus, indicating that these parasites are pathogenic for hosts. The parasite fauna of O. bicirrhosum was scarce, while the parasites for A. ocellatus were mainly helminthes species, including adults and larval forms. Such differences on parasites fauna of both omnivore hosts may due to their history life as well as environmental and biological factors. KEYWORDS: Condition Factor. Helminthes. Parasites. Freshwater Fish. INTRODUCTION Belonging to the Osteoglossidae family, the arowana Osteoglossum bicirrhosum Cuvier, 1829 occurs in the Amazon River Basin and in the Rupununi and Oyapock Rivers (FERRARIS- JUNIOR, 2003). A benthopelagic fish with a sedentary life-style, it can jump out of water to catch prey in nearby branches, which allows this species exploring a variety of arboreal preys, such as insects, arachnids and other small vertebrates. A small portion of its diet consists of small fish; it is an omnivorous species and also feeds on crustaceans and mollusks, showing no variations in the type of food from a hydrological period to another (SANTOS et al., 2006; AGUDELO- ZAMORA et al., 2007; SOARES et al., 2008). All these characteristics indicate that this is a carnivore- insectivore fish. Reproduction occurs between the end of the dry season (December) and the beginning of the flooding season (January). The females begin the process of sexual maturity at 55 cm out of standard length (SOARES et al., 2008). The Oscar Astronotus ocellatus Agassiz, 1831 is a Cichlidae geographically distributed in South America, in the Amazonas River Basin, including Brazil, Peru, Colombia and French Guiana (SANTOS et al., 2006; SOARES et al., 2008). However, it is currently found in river basins from the Northeast, Southeast and Southern Brazil (AZEVEDO et al., 2007). This species is widely used as food source by the Amazonian riverine and urban populations. Moreover, it is used as ornamental fish in several countries around the world (SILVA et al., 1993). It is a benthopelagic fish with preference for lentic environments finding protection under submerged branches and trunks. It can ambush and capture prey and escape over short distances; it is an omnivorous species, with carnivorous trend, feeding on fish, crustaceans, gastropods and larvae of aquatic insects (SANTOS et al., 2006; AZEVEDO et al., 2007; SOARES et al., 2008). Spawning occurs between the onset of flooding (December) and dry season (July) and the first gonadal maturation happens at 25 cm of length and 15-24 months of age (SOARES et al., 2008). Despite the economic importance of O. bicirrhosum (ORTIZ; JOSÉ IANNACONE, 2008; COSTA et al., 2009) and A. ocellatus (AZEVEDO et al., 2007; SOARES et al., 2008) for aquarists, as well as source the importance as food for the riverine population from several areas of the Received: 08/05/12 Accepted: 05/06/13 547 Parasitic infections... TAVARES-DIAS, M.; SOUSA, T. J. S. M.; NEVES, L. R. Biosci. J., Uberlândia, v. 30, n. 2, p. 546-555, Mar./Apr. 2014 Amazon, a little is known about the parasitic fauna of these Amazon fish. Populations of arowana O. bicirrhosum from natural environments have been parasitized by the monogenoideans Gonocleithrum aruanense, G. coenoideum, G. cursitans, G. planacroideum and G. planacrus (KRITSKY; THATCHER, 1983), digeneans Caballerotrema aruanense (THATCHER, 1980; PELEGRINI et al., 2006), nematode Camallanus acaudattus (FERRAZ; THATCHER, 1990) and the pentastomida Sebekia sp. (PELEGRINI et al., 2006). In contrast, farmed arowana have been parasitized by G. cursitans, Trichodina sp. and C. acaudattus (VAZQUEZ et al., 2007). For A. ocellatus has been described parasitism by the monogenoideans Gussevia asota, G. astronoti and G. rogersi (KRITSKY et al., 1989; AZEVEDO et al., 2010; ABDALLAH et al., 2008), larvae of nematode Contracaecum sp., crustacean Lamproglena sp., leeches Placobdella sp. and acanthocephalan Polymorphus sp., mollusks Glochidiae larvae (AZEVEDO et al., 2007) and Posthodiplostomum sp. (TAVARES-DIAS et al., 2011). In most aquatic ecosystems fish are hosts to parasites, which may affect the fish biology, mainly when they are intermediate hosts for larval parasites. Parasites may also alter the behavior of their hosts in order to increase their probability of survival, resulting in increased susceptibility of infecting the host to predation, enhancing the transmission by influence of predator–prey interactions (CHOUDHURY; COLE, 2008; BULLARD; OVERSTREET, 2008; POULIN; LEUNG, 2011). For these reason, the fish parasites may be used as indicators of environmental impacts. The aim of this study was to evaluate the parasites fauna in wild populations of O. bicirrhosum from State of Amazonas (central Amazon) and of A. ocellatus from State of Amapá (eastern Amazon), Brazil. In addition, it provides an important baseline for comparative studies on host- parasite relationships in O. bicirrhosum and A. ocellatus from natural environments that may be much important for comparison on diseases studies regarding these fish when in fish farm, whose likelihood of infections can be higher and pathologies are devastating. MATERIAL AND METHODS Fish and study area In October 2008, 28 specimens of Osteoglossum bicirrhosum (32-68 cm and 370- 1.610 g) were collected from River Coari Grande (04o33’297”S, 64o 35’909”W), a tributary of the middle Solimões, in the municipality of Coari, State of Amazonas (central Amazon), Brazil. In addition, from May to June 2009, 26 specimens of Astronotus ocellatus (19-26 cm and 192-470 g) were collected from River Preto (00o11’59.1”N, 051º32’89.3”W), a tributary of the Amazonas River, in the municipality of Mazagão, State of Amapá (eastern Amazon), Brazil, for parasitological studies. All fish were collected using different fishing nets (IBAMA: 11884-1). Parasitological Analysis All fish were weighed (g), measured in total length (cm) and then necropsy was performed. The gills were removed and analyzed under microscope. The gastro-intestinal tract was removed, placed in Petri dishes containing NaCl (0.8%) and examined under stereomicroscope. The methodology used for collection and fixation of parasites (EIRAS et al., 2006; Thatcher, 2006) and for their quantification (TAVARES-DIAS et al., 2001a, b) were according to the previous recommendations. The parasites identification was conducted according to KRITISKY et al. (1983), KRITSKY et al. (1989), MORAVEC (1998), THATCHER (2006) and LUQUE et al. (2011). The ecological terms adopted were those recommended by BUSH et al. (1997). Parasite-host relationship Data on weight and total length were used to determine the relative condition factor (Kn) of the fish (LE-CREN, 1951). Spearman’s rank correlation coefficient (rs) was used to determine possible correlations between hosts’ weight and length with the intensity of parasites (ZAR, 1999). RESULTS From the examined arowana O. bicirrhosum, 87.5% had their gills parasitized by Gonocleithrum aruanae Kristy & Thatcher, 1983 (Monogenoidea, Dactylogyridae), but no other parasite was found. For A. ocellatus from the Preto River (AP), 92.8% of the examined hosts fish had their gills parasitized by Ichthyophthirius multifiliis Fouquet, 1876 (Protozoa, Ciliophora), Gussevia asota Kritsky, Thatcher & Boeger, 1989 (Monogenoidea, Dactylogyridae) and metacercariae of Posthodiplostomum Dubois, 1936 (Digenea, Diplostomidae) and their intestine by adult forms of Procamallanus (Spierocamallanus) inopinatus Travassos, Artigas & Pereira, 1928 (Nematoda, Camallanidae) and larvae of Contracaecum Railliet and Henry, 1912 (Nematoda, Anisakidae). High levels of infection by monogenoidea were observed 548 Parasitic infections... TAVARES-DIAS, M.; SOUSA, T. J. S. M.; NEVES, L. R. Biosci. J., Uberlândia, v. 30, n. 2, p. 546-555, Mar./Apr. 2014 in O. bicirrhosum, while the highest rates of infection in A. ocellatus were caused by helminthes G. asota, P. inopinatus and Contracaecum sp. (Table1). Table 1. Parasites in Osteoglossum bicirrhosum from the Coari Grande River, State of Amazonas (central Amazon) and in Astronotus ocellatus from Preto River, State of Amapá (eastern Amazon). P: Prevalence, MI: Mean intensity, MA: Mean abundance and TNP: Total number of parasites. With regard the species richness in the community, there was predominance of parasitized fish for A. ocellatus, mainly by one and three species (Figure 1). Figure 1. Species richness of parasites in Astronotus ocellatus from Preto River, State of Amapá, eastern Amazon. There was no correlation of G. aruanae intensity with the body weight (rs=-0.178; p=0.360), total length (rs= -0.290; p=0.134) or Kn (rs= -0,187; p=0,337) from O. bicirrhosum (Figure 2). Similarly, there was no correlation of helminthes intensity with the body weight (rs= 0.037; p=0.854) and the total length (rs= 0.046; p=0.820) from A. ocellatus Fish species Osteoglossum bicirrhosum (N=32) Astronotus ocellatus (N=28) Taxa/Parasites P (%) MI MA TNP P (%) MI MA TNP PROTOZOA Ichthyophthirius multifiliis - - - - 42.9 11.495.1 6.569 183.921 MONOGENOIDEA Gonocleithrum aruanae 87.5 340.1 297.6 9.523 - - - - Gussevia asota - - - - 39.3 76.9 46.7 1.307 NEMATODA Procamallanus (S.) inopinatus - - - - 39.3 3.7 2.3 63 Contracaecum sp. (larvae) - - - - 25.0 2.4 0.6 17 DIGENEA Posthodiplostomum sp. (metacercariae) - - - - 21.4 5.3 1.1 32.0 549 Parasitic infections... TAVARES-DIAS, M.; SOUSA, T. J. S. M.; NEVES, L. R. Biosci. J., Uberlândia, v. 30, n. 2, p. 546-555, Mar./Apr. 2014 Figure 2. Correlation between the intensity of monogenoideans Gonocleithrum aruanae and the Kn in Osteoglossum bicirrhosum (N=28) from the Coari Grande River, State of Amazonas, central Amazon, Brazil. The Kn of A. ocellatus showed negative correlation with the intensity of helminthes (Figure 3), which indicates that the hosts body condition was affected by these parasites in. Figure 3. Correlation between the intensity of helminthes (Gussevia asota, Posthodiplostomum metacercariae, Procamallanus inopinatus and Contracaecum larvae) and the Kn in Astronotus ocellatus (N= 26) from Preto River, State of Amapá, eastern Amazon, Brazil. DISCUSSION Helminthes were the main components of the parasitic fauna of A. ocellatus from the Preto River in eastern Amazon, and O. bicirrhosum from the Coari Grande River in central Amazon, both omnivore fish species. However, parasite fauna of A. ocellatus accounted on one Protist, one Monogenoidea, one Digenea and two Nematoda, while O. bicirrhosum was parasitized only by Gonocleithrum aruanae. Such results may be due to different life history of these hosts, as well as the 550 Parasitic infections... TAVARES-DIAS, M.; SOUSA, T. J. S. M.; NEVES, L. R. Biosci. J., Uberlândia, v. 30, n. 2, p. 546-555, Mar./Apr. 2014 heterogeneity from environmental and hosts’ biological factors. Protozoan parasites have a wide range of life-cycles and cause diseases in freshwater fish. Among the most important ectoparasites of fish are the ciliated Protozoans; the most pathogenic of them is the I. multifilis, which infects fish either from tropical or temperate regions (TAVARES-DIAS et al., 2001a; DICKERSON, 2006; EIRAS et al., 2010). In addition, it has worldwide distribution and infects any farmed or wild species, from juvenile to adults, and may cause high mortality rates in fish farms. Besides, when natural outbreaks of ichthyophthiriasis occur in wild fish populations, they can have devastating effects (RAISSY et al., 2010). In the gills of A. ocellatus from Preto River in State Amapá, there was high parasitism by I. multifiliis, similar to what occurred in Capoeta damascina from Armand River, Iran (RAISSY et al., 2010). However, infection levels were higher than the ones for Oxydoras niger from Lake Coari, in the state of Amazonas, Brazil (SILVA et al., 2011) and for Capoeta aculeata from the Choghakhor lagoon, Iran (RAISSY; ANSARI, 2011). In Brazil, despite the occurrence of I. multifiliis in some fish from natural environments, there are still no reports of outbreaks. In the gills of arowana O. bicirrhosum from Coari Grande River (in State of Amazonas), only the Monogenoidea G. aruanae was found. However, for this same fish from Januacá Lake, also in the State of Amazonas, Kritsky; Thatcher (1983) identified other four species of monogenoideans, G. coenoideum, G. cursitans, G. planacroideum and G. planacrus besides the G. aruanae. In the gills of Oscar A. ocellatus from the Preto River, there was infection by monogenoidean G. asota, while for this same host in the Guandu River (State of Rio de Janeiro), there was parasitism by G. asota and G. astronoti (AZEVEDO et al., 2010). Infections by monogenoideans Gonocleithrum spp. in O. bicirrhosum from Coari Grande River (AM) were higher than those caused by G. asota in A. ocellatus from the Preto River (AP). Although the prevalence of G. asota in A. ocellatus from this study was lower than the prevalence for this same host from the Guandu River (AZEVEDO et al., 2007), the intensity and abundance here were higher. Such differences are due to the fact that the hosts are benthopelagic fish from different environments. Since monogenoideans parasites have a direct lifecycle, they occur more frequently in lentic environments, which favor their transmission (AZEVEDO et al., 2007; GRAÇA; MACHADO, 2007) to hosts such as A. ocellatus, which show a preference for this type of habitat (AZEVEDO et al., 2007). However, during the breeding period, the arowana O. bicirrhosum nests in mud and stones, in areas of calm water for the spawning and care of its offspring. During three months of parental care (SANTOS et al., 2006; SOARES et al., 2008), parents do not feed and therefore are more exposed to infections by parasites. Many endohelminth parasites have complex life-cycles that involve two or more hosts, because they have indirect life-cycles. Larval stages occur in one or more intermediate hosts, followed by sexual reproduction of mature adults in the definitive host. Intermediate hosts are essential for the completion of larval development and the parasite sometimes undergoes a period of asexual multiplication within them. Paratenic hosts are additional non-obligatory hosts in the lifecycle, which larval parasites can infect but in which they do not undergo any further development before infecting the next intermediate or definitive host. Intermediate and paratenic hosts are often affected by the presence of these parasites, becoming more susceptible to predators, which are the definitive hosts, and thus allowing the completion of parasite lifecycle (THATCHER, 2006; BULLARD; OVERSTREET, 2008; POULIN; LEUNG, 2011). Fish can be intermediate, paratenic or definitive hosts from nematode species (THATCHER, 2006; TAKEMOTO et al., 2009; EIRAS et al., 2010). In this study, it was observed the presence of Contracaecum sp. larvae and P. inopinatus adults in A. ocellatus, similarly to what was reported for Metynnis lippincottianus from the Paraná River (MOREIRA et al., 2009). Nematodes of the genus Contracaecum are parasites that in the adult stage are preferably found in fish-eating birds, which are their definitive hosts. However, fish can act as intermediate or paratenic hosts (CHOUDHURY; COLE, 2008; MOREIRA et al., 2009). Fish acting as paratenic hosts get the parasites by predating smaller fish, which in turn become infected through the ingestion of infected copepods, mollusks, gastropods, coelenterates and/or ctenophores or even larvae of Contracaecum sp. on its free-living stage (MADI; SILVA, 2005; CHOUDHURY; COLE, 2008). Therefore, Contracaecum spp. at larval stage is often found in intermediate fish host (CHOUDHURY; COLE, 2008). Chironomids are intermediate hosts of P. (S) inopinatus (MOREIRA et al., 2009), which have been listed as the most frequent nematode species parasitizing Brazilian freshwater fish (EIRAS et al., 2010), because it has no parasitic specificity. 551 Parasitic infections... TAVARES-DIAS, M.; SOUSA, T. J. S. M.; NEVES, L. R. Biosci. J., Uberlândia, v. 30, n. 2, p. 546-555, Mar./Apr. 2014 For A. ocellatus from Preto River (in the eastern Amazon), the rates of infection by Contracaecum sp. larvae were similar to those of P. inopinatus. However, these rates of parasitism by Contracaecum sp. larvae were lower than those described for A. ocellatus from Guandu River in State of Rio de Janeiro (AZEVEDO et al., 2007). However, the rates of infection by P. inopinatus in A. ocellatus in this study were similar to those reported for M. lippincottianus (prevalence= 43.2% and mean intensity= 2.3) from the Paraná River basin, Brazil (MOREIRA et al., 2009). In contrast, they were lower (prevalence= 60.0% and mean intensity= 3.8) than the rates of infection described by VITAL et al. (2011) for the carnivorous fish P. nattereri from Lake Piranha in the State of Amazonas. These differences may due to the different host species, environment and distinct lifestyles. The main pathogenic effects of digeneans infections in fish hosts occur from metacercariae. In general, metacercariae tends to be less host-specific than adult digeneans and can affect fish growth and survival, as well as being a source of infection to definitive hosts and other piscivorous vertebrates. Many metacercarie enter the host fish by active invasion of the cercariae, and the transmission success depends on the cercariae behavior (THATCHER, 2006; BULLARD; OVERSTREET, 2008). Thus, distribution of metacercariae within the host can be affected by parasite behavior as well as by host behavior and habitat (THATCHER, 2006; BULLARD; OVERSTREET, 2008; TAVARES- DIAS et al., 2011). Therefore, the metacercariae can infect various fish organs, including the gills, causing moderate to severe hyperplasia of the primary gill lamellae, forming cysts surrounded with multiple cellular reactions, including mononuclear inflammatory cells (BULLARD; OVERSTREET, 2008; EISSA et al., 2011). In addition, a massive and widespread infection by these metacercariae, particularly in little fish, can cause intensive inflammatory response and mortality (BULLARD; OVERSTREET, 2008; EIRAS et al., 2010). For this study, the levels of infection by Posthodiplostomum sp. metacercariae in the gills of A. ocellatus from Preto River were lower than those reported by Tavares-Dias et al. (2011) for this same host from Pracuúba Lake also in the state of Amapá. In Brazil, only metacercariae of Posthodiplostomum macrocotyle have been identified in the hosts Mugil liza, Geophagus brasiliensis and Trachelyopterus striatulus from Guandu River (AZEVEDO et al., 2010). High prevalence and intensity of Posthodiplostomum sp. metacercariae indicates abundance of fish-eating bird in the area, which are definitive hosts, besides favorable conditions for the first intermediate host, a snail, the most common cause of the infections on the gills of A. ocellatus (TAVARES-DIAS et al., 2011). Furthermore, these results corroborate the fact that the fish lifestyle has great importance on the levels of infection by digeneans species. The host-parasite relationship has been a useful tool for understanding the ecological relationships between parasites and their hosts (SILVA et al., 2011; VITAL et al., 2011; GUIDELLI et al., 2011). The body size (weight and length) and the hosts’ condition factor can be used for this purpose. In this study, there was no correlation between the intensity of parasites and size of any of the host species. Similar results have also been described by Azevedo et al. (2007) for A. ocellatus. In this study, the lack of correlation between the body size and parasitic intensity might be due to its behavior and physiology. In contrast, the total length was negatively correlated with the abundance of digenean Saccocoelioides nanii and the prevalence of the metacestode for Prochilodus argenteus (MONTEIRO et al., 2009). POULIN; LEUNG (2011) stated that any relationship between host fish body size and the intensity of helminth parasites using it as intermediate host should be negative, because large hosts are unlikely to serve as prey. Therefore, the host fish size is not one of the factors promoting local diversification of helminth parasite species. The condition factor is a good indicator of fish well-being and can be used to evaluate the effects of parasitism on the hosts’ health (SILVA et al., 2011; GUIDELLI et al., 2011). However, the relative condition factor is indicator of health that also reflects recent nutritional conditions (GUIDELLI et al., 2011) and physiological status. In A. ocellatus of this study, the Kn was negatively influenced by the intensity of helminthes G. asota, Posthodiplostomum sp. (metacercarie), P. inopinatus and Contracaecum sp. (larvae), which indicates that these parasites were pathogenic to the host. However, the intensity of G. aruanae did not influence the Kn in O. bicirrhosum. In contrast, a positive correlation between the intensity of monogenoideans and Kn was reported for O. niger from Coari Lake (SILVA et al., 2011) and Pygocentrus nattereri from Piranha Lake (VITAL et al., 2011), both in the state of Amazonas. However, hosts are not affected by parasites when there is balance in the parasite–host relationship. Negative effects of endoparasites on the hosts Kn 552 Parasitic infections... TAVARES-DIAS, M.; SOUSA, T. J. S. M.; NEVES, L. R. Biosci. J., Uberlândia, v. 30, n. 2, p. 546-555, Mar./Apr. 2014 are more prominent in infections by larvae (GUIDELLI et al., 2011), as occurred in A. ocellatus of this study. Furthermore, overall the response of hosts to parasites varies according to type and stress intensity caused by parasites, as well as their life- cycle and time of exposure. In conclusion, our results showed that the helminth parasites had negative effect on body conditions of A. ocellatus from Preto River in State of Amapá. Given the poor fauna of endoparasites of O. bicirrhosum is somewhat intriguing, thus needing further studies. This study lists Preto River as a new locality for Contracaecum sp., Posthodiplostomum sp. and P. inopinatus. ACKNOWLEDGEMENTS The present work was developed according to the principles adopted by COBEA (Brazilian College of Animal Experiments). M. Tavares-Dias was supported by a Research fellowship from CNPq (Conselho Nacional de Pesquisa e Desenvolvimento Tecnológico, Brazil). RESUMO: O presente estudo avaliou a fauna parasitária de Osteoglossum bicirrhosum da Amazônia central (Brasil) e Astronotus ocellatus da Amazônia oriental (Brasil) de ambiente natural, e também a relação parasito-hospedeiro. 87,5% dos O. bicirrhosum estavam parasitados por Gonocleithrum aruanae (Monogenoidea) e A. ocellatus (92,8%) estavam parasitados por Ichthyophthirius multifiliis (Ciliophora), Gussevia asota (Monogenoidea), metacercárias de Posthodiplostomum sp. (Diplostomidae), adultos de Procamallanus inopinatus e larvas de Contracaecum sp. (Anisakidae). Em O. bicirrhosum os níveis de infecção por Gonocleithrum aruanae foram elevados, enquanto em A. ocellatus os maiores níveis de infecção foram causados por helmintos ectoparasitos como G. asota, e endoparasitos como Posthodiplostomum sp., Procamallanus inopinatus e Contracaecum sp. Em A. ocellatus houve significativa (p>0,05) correlação negativa entre a intensidade de helmintos e fator de condição relativa (Kn), indicando os parasitos foram patogênicos para os hospedeiros. A fauna parasitária de O. bicirrhosum foi reduzida, enquanto a de A. ocellatus foi constituída por espécies de helmintos, incluindo formas larvais desses parasitas. Tais diferenças na fauna de parasites de ambos os peixes onívoros pode ser devido a sua história de vida, bem como a fatores ambientais e biológicos. PALAVRAS-CHAVE: Fator de condição. Helmintos. Parasitos. Peixes de água doce. REFERENCES ABDALLAH, V. D.; AZEVEDO, R. K.; LUQUE, J. L. Notes on the morphology of two species of Gussevia Kohn e Paperna (Monogenea: Dactylogyridae) parasit on Astronotus ocellatus (Agassiz) (Perciformes: Cichlidae) from Brazil. Pan-American Journal of Aquatic Sciences, Natal, v. 3, p. 101-104, 2008. AGUDELO-ZAMORA, H. D.; LÓPEZ-MACIAS, J. N.; SÁNCHEZ-PÁEZ, C. L. 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