ENDOPARASITES OF Gymnotus sp . ( GYMNOTIFORMES : GYMNOTIDAE ) FROM COMMERCIAL BAITFISH FARMING IN PANTANAL BASIN , CENTRAL BRAZIL

This study evaluated the endohelminthic parasites of native baitfish Gymnotus spp. collected from different baitfish farming in the Pantanal basin, State of Mato Grosso do Sul, Central Brazil. From 99 fish collected for parasitological analysis, all of them were found to be parasitized by at least 1 parasite per host. A total of 4504 parasites were collected comprising the following taxa: Digenea, Nematoda, Pentastomida and Acanthocephala. Rondonia rondoni and Goezia sp. as well as Alofia sp. Were registered for the first time in farmed Gymnotus spp. The parasite species diversity in the host is discussed in this study.


INTRODUCTION
Gymnotus spp.commonly known as "swordfish", "banded knifefish", "tuvira", "sarapó" or "ituí", depending on the geographical location, is widely distributed in South America and stands out as an important baitfish commercialized in the Pantanal Sul matogrossense, a region in which they are part of the feeding habit of piscivorous fish like "dourado" (Salminus brasiliensis) and "surubim" (Pseudoplatystoma spp.), and are appreciated by sports fishermen (PEREIRA and RESENDE, 2006) as bait.
Small fish like Gymnotus spp., plays an important ecological role, because the life cycle of the parasites they can act as intermediate and/or paratenic hosts, are food for other fish species and several groups of animals, which are considered definitive hosts (ISAAC et al., 2004).Previous studies have shown high wealth endoparasites (16 species) in Gymnotus spp.collected in natural environments (ISAAC et al., 2004;TAKEMOTO et al., 2009;LUQUE et al., 2011).In considering the rapid development of freshwater aquaculture, studies on endoparasite fauna of farmed fish have not gained special attention nor accompanied the burgeoning of continental fish farming (LIZAMA et al., 2007).
No records were found on endoparasites living in baitfish under farming conditions.Parasitism at a high level can cause fish mortality and consequently, important economic losses to the local population have affected income (ISHIKAWA et al., 2014).A deeper analysis of the maintenance of local or even adult specimens should be performed in order to assess the health of fish being marketed, due to the importance of live bait as a vector of pathogens to piscivorous fish aimed for human consumption.This study evaluated the endohelminthic fauna of Gymnotus spp.collected from different baitfish farmed in the Pantanal Sul matogrossense and presents new data on their diversity and host occurrence under farming conditions.
Fish were transported to the Embrapa Agropecuária Oeste -Aquaculture Laboratory in plastic bags with oxygen.After that, they were euthanized by deep anaesthesia in clove oil solution (150 mg L -1 ) in accordance with procedures approved by the Ethics Committee of Animal Use nº.005/2011-CEUA/UFGD.For parasitological examination, the visceral cavity was opened for macroscopic observation to detect possible parasites.Internal organs as heart, liver, spleen, swim bladder, gonads, stomach, intestines, visceral cavity and muscle was removed and examined in order to collect endoparasites.The parasite specimens were collected, fixed, quantified and stained (EIRAS et al., 2006), for identification according MORAVEC (1998) andTHATCHER (2006).Prevalence, mean intensity and mean abundance of infection were calculated (BUSH et al., 1997).
The parasite community of Gymnotus spp. in this study showed great parasite diversity in which nine species of nematodes, three digeneans, three acanthocephalans and two pentastomids were reported.The species diversity can be assigned to the fish that were collected in nature, which exhibit higher diversity (ISAAC et al., 2004).Therefore, when they were maintained in conditions of captivity, an increase in the parasitic infection contributed to the transmission of parasites.This may also explain the fact that most of the parasites were found in larval stage, indicating an early infection.In addition, the wealth of species could be strongly associated with eating habits (ADRIANO et al., 2012).
Digeneans are endohelminthic parasites with complex life cycle generally involving two hosts.They can be found parasitising several internal organs in definitive hosts (THATCHER, 2006;TAKEMOTO et al., 2009) or as encysted metacercariae (BACHMANN et al., 2007;SANTOS et al., 2012).In the present study, metacercariae of Tylodelphys sp. and Diplostomum sp. were observed in the celomatic cavity and Clinostomum sp. in the muscle.In contrast to what was found here, Clinostomum sp. have related in the gonads and mesentery (ISAAC et al., 2004).This parasite presents wide geographic distribution, a wide amplitude of hosts (CAFFARA et al., 2011) and low host specificity (SERENO-URIBE et al., 2013).
Moreover, human infections were also reported showing its zoonotic potential (CHUNG et al., 1995;SHIRAI et al., 1998;PARK et al., 2009).In a study, analysing the composition of infracommunity structure in Gymnotus spp.from the river, a relationship was observed between the prevalence of Tylodelphys sp. and reproductive period of Gymnotus spp.(ISAAC et al., 2004).It could be inferred that the host susceptibility is strongly related with hormonal and behavioural alterations as a result of stressful conditions in that period.
Larvae of Diplostomum sp. are opportunistic parasites registered in several fish species and amphibians (MACHADO et al., 2005;LOCKE et al., 2010;RELLSTAB et al., 2011).Fish are an important vector for the parasite transmission to the final host.The cercariae emerge from the intermediate host (LOCKE et al., 2010), and the feed habit of Gymnotus spp.including benthic organisms, may have favoured the parasitism by Diplostomum sp. in the host.Although the highest prevalence of infection and damage caused to the host by these mertacercariae are associated with their installation in the eyes (MACHADO et al., 2005), there are reports of the presence of the metacercariae in the gills and adjacent pharyngeal plates (SATO and PAVANELLI, 2004).In this study, the metacercariae were found to be parasitising the celomatic cavity.
The presence of Contracaecum sp. and Brevimulticaecum sp.larvae in the liver and celomatic cavity corroborates some reports (CAMPOS et al., 2009;VENTURA et al., 2016).In the present study, all specimens were Contracaecum larvae of type I, II and III located in the mesentery and liver the gymnotid fish.Similarly, larvae of Contracaecum sp. were also reported in Gymnotus spp.(AZEVEDO et al., 2007;TAKEMOTO et al., 2009).On the other hand, larvae of Brevimulticaecum sp. in fish are scarce.To date, Brevimulticaecum larvae have been reported in the celomatic cavity, hepatic parenchyma, mesentery, skeletal muscle and stomach wall of Gymnotus inaequilabiatus (VIEIRA et al., 2010) and GALINDO et al. (2017) suggest that G. inaequilabiatus acts as a paratenic host to nematodes in the larval stage.
Gymnotus sp. of natural environment the nematodes Capillariinae gen.sp., Contracaecum sp.(types I and II), Eustrongylides sp., Hysterothylacium sp., Procamallanus (P.) peraccuratus, Spiroxys sp.Brevimulticaecum sp., and Ascaridoidea fam.gen.sp. were reported (ISAAC et al., 2004).In a natural environment, R. rondoni has been reported in different river basins, Paraguay, Paraná, Amazonas and São Francisco (COSTA, 1963), parasitizing fish of different families Characidae, Cynodontidae, Doradidae, Heptapteridae, and Pimelodidae (KOHN et al., 2011), R. rondoni is reported for the first time parasitizing Gymnotus sp.In Brazil four species of Goezia sp were described in different species of fish (VIEIRA-MENEZES et al., 2017), but in the genus Gymnotus sp there are no reports of parasitism by this species.Though in the present study the prevalence of Goezia sp infection was low (3.03%), in cases of massive infection, causing gross lesions and high mortality among the fish (VIEIRA-MENEZES et al., 2017).
Apart from the low host specificity of Contracaecum sp.larvae, they also present special importance for public health due to their elevated zoonotic potential (TAKEMOTO et al., 2009).Nevertheless, these results indicate the low possibility of these helminths causing zoonosis as they were found in the liver and visceral cavity.However, Eustrongylides larvae were observed encysted in the muscle and could present a possible cause of human infection.Until the present, nematodes have been related only in Gymnotus spp.from the rivers (ISAAC et al., 2004) and no reports have been found in farmed baitfish Gymnotus.In this study, acanthocephalans were found in larval form encysted in the intestines and stomach.The main factor regulating the prevalence and intensity of infection by acanthocephalans is the predation of the crustaceans as intermediate hosts (AZEVEDO et al., 2007).Similarly, larvae and adult of Quadrigyrus sp. were reported in Gymnotus carapo (ISAAC et al., 2004).On the other hand, Pomphorhynchus sp. was found to parasitise gymnotid fish in Argentina (ARREDONDO and GIL DE PERTIERRA, 2010).Gymnotids were pointed out as an intermediate host for larvae of Quadrigyrus machadoi Fabio, 1983.Obligatory paratenic hosts in the life cycle of acanthocephalans feed on the intermediate host that does not constitute the common item in the diet of definitive host completing the life cycle (EIRAS et al., 2010).The low infection found in this study could be strongly associated with the capture period of the specimens in the environment as the intermediate hosts were found in low amounts in this period, as also observed previously (CAMPOS et al., 2009).Possibly, the helminthic fauna was introduced into fish farming with infected fish captured from the environment.
Pentastomids on their adult stage are normally found to parasitize the lungs of vertebrates mainly reptiles (BRITO et al., 2012;CHRISTOFFERSEN and ASSIS, 2013) and during their larval stage they can be found in freshwater fishes (VARGAS, 1975).Larvae of Sebekia sp. and Leiperia oxycephalum were related in Gymnotus spp.(LUQUE et al., 2013;CHRISTOFFERSEN and ASSIS, 2013) and are generalist parasites in terms of intermediate hosts (REGO and EIRAS, 1989).

CONCLUSION
Gymnotid fish are commonly used as live baitfish for sport fishing of carnivorous and food-appreciated fish but the endoparasitic diversity and definitive hosts in the aquatic ecosystem highlight the importance of these fish as an intermediate host.This study showed that the endoparasitic helminths in bait gymnotid fish are able to survive in fish farming conditions that in this case endured several weeks after capture until marketing.Additionally, this study registers Gymnotus spp.host of Goezia sp. and R. rondoni for the first time.

Table 1 .
Parasitological indices and site of infection of endohelminthic parasites in Gymnotus spp.examined from baitfish farming in the Pantanal basin of Mato Grosso do Sul.