Introduction

Isópodes Cymothoidae Leach, 1818, has parasitic habits (Brusca, Coelho, & Taiti, 2001) and its morphological structures are prehensile pereopods provided by long claws, strong and curved, buccal pieces highly modified for parasitic life (Thatcher, 2006). After living the marsupium, the cymothoid juveniles are ready to attach and feed on small fishes (Leonardos & Trilles, 2003).

The family Cymothoidae harbor more than sixty genera and one of them is Braga Schiöedte and Meinert, 1881, with six species, which was firstly proposed to harbor parasitic isopods of freshwater fish from South America. According to Thatcher (2006), specimens of the genus can be found in tongue and operculum cavity of the hosts, they have symmetric body, cephalon little immersed in pereonite 1, all seven pairs of pereopods prehensile and provided with stout claw-like dactyls and pleotelson usually wider than long.

In Brazil, these parasites were reported on the following hosts: B. amapaensis in the mouth of Acestrorhynchus microlepis from Amapá (Thatcher, 1996; Eiras, Takemoto, & Pavanelli, 2010), B. patagonica in the gills of Hoplias malabaricus from Macapá (Alcântara & Tavares-Dias, 2015), B. nasuta in the mouth of Hypostomus sp. from Amazonas, Bahia and São Paulo (Thatcher, 2006), B. cichlae in Cynopotamus humeralis, Cichla ocellaris and C. temensis from São Paulo, Minas Gerais, Pará and Amazonas (Thatcher, 2006), B. fluviatilis in unidentified catfish (Thatcher, 2006).

Arapaima gigas Schinz, 1822, commonly known as pirarucu or arapaima, is considered one of the biggest freshwater fish reaching approximately 200 Kg and 2.5 m long (Ono, Roubach, & Pereira-Filho, 2003; Saint-Paul, 1986). Fish distributed in the Amazon basin, A. gigas has been target of commercial fisheries in the Amazon River and its tributaries, as well as in the flooded areas, i. e., igapós, causing damage to the natural stocks (Imbiriba, 2001). Due to easy handling, rapid growth and weight gain, the excellent survival rate of fingerlings, good acceptability of extruded diet, its tolerance to stocking density, aerial breathing, good acceptance of its meat and high value in the market, this species has been produced in commercial fish farm, as an alternative to predatory fishery (Imbiriba, 2001; Ono, Halverson, & Kubitza, 2004; Pereira-Filho et al., 2003). Nevertheless, high stocking density and inadequate fish handling are responsible for stress, imbalance in the host-parasite-environment relationship provoking a portal of entry to diseases and economic losses (Martins, 2004; Lemos, Rodrigues, & Lopes, 2006).

This study identified the isopods from the fingerlings of pirarucu cultured in earthen ponds from a fish farm located in the Amazon region, Pará State.

Material and methods

Fingerlings were collected from a commercial fish farm in the in the city of Parauapebas, Pará State (05o 59’S, 49o 53’W) between May and August 2016 (Figure 1). Fingerlings were from earthen ponds with abundant vegetation on the edges. Fish were collected from two spawnings (Figure 2) that occurred in two earthen ponds with 1,680 m3 (12 x 70 x 2 m), harvested from a couple weighing 90 kg each. Reproduction is natural with spontaneous spawning inside the ponds where the fingerlings are captured at the age of 20 days.

Figure 1.

Commercial fish farm located in the Amazon region, Pará State.

Figure 2.

Fingerlings of pirarucu, Arapaima gigas, collected from a commercial fish farm located in the Amazon region, Pará State. A- fish with approximately 10 g transferred to nursery, B- presence of ectoparasites on the body surface, C-lateral view of the parasite attached on the fish body.

A total of 3,625 of pirarucu with approximately 10 g were transferred to nursery for feeding training and observation. During feeding training, the fingerlings were carefully observed in relation to the presence of ectoparasites on the body surface. The parasites were collected, fixed and processed according to Eiras, Takemoto, and Pavanelli (2006). The specimens were measured (total length and width) and dissected to observe the anatomic pieces after cleared with phenol. Antenna, antennula, maxilla, maxillule, maxilliped, pereon, pleon, pereopods, pleopods, pleotelson and uropods were mounted between a depressed slide and a coverslip for observation and measurement in a Leica EZ4HD stereomicroscope (Thatcher, Oliveira, & Garcia, 2009). The vouchers were deposited at the Aquatic Organisms Health Laboratory of the Universidade Federal de Santa Catarina (CCA, UFSC) Aquaculture Department, Florianópolis, Santa Catarina, Brazil (AQUOS-ISO-1). The marsupium was carefully opened from a female specimen to observe the eggs. Identification was according to Lemos de Castro (1959), Thatcher (1995, 1997, 2006), Thatcher et al. (2009). Parasitological descriptors such as prevalence, mean intensity and mean abundance followed the Bush, Lafferty, Lotz, and Shostak (1997) recommendation.

Results

Macroscopic observation revealed the presence of a total of eleven specimens (seven females and four males) of the isopod Braga nasuta from the ventral region close to pectoral fin and anus, collected from parasitized fingerlings (Figure 3). Males were 14.06 ± 2.3 mm long by 6.46 ± 1.2 mm wide and females 23.0 ± 2.8 mm long by 13.0 ± 1.4 mm wide. The prevalence was 0.303%, intensity 1.000 ± 0.000 and mean abundance 0.003±0.055. In just one female 26 mancas were found comprising the stage I of development.

Figure 3.

Braga nasuta specimen from cultured Arapaima gigas. A-ventral view, B-dorsal view, C-lateral view of the parasite attached on the fish body.

Discussion

In relation to site of attachment, species of the genus Braga commonly attach to the operculum cavity, gills or wounds opened on the fish body (Lemos de Castro, 1959; Thatcher, 2006). Dias, Neves, Marinho, and Tavares-Dias (2015) have observed B. patagonica on the dorsal region of C. macropomum causing loss of scales and tegument culminating in an inflammatory process. In contrast to that reported by Dias et al. (2015), in the present study the parasites did prefer the ventral region of the host or close to pectoral fin and anus. No mortality was found due to the parasitic infestation. The prevalence rate was low and parasitized hosts showed weight loss, hemorrhages and inflammatory reaction on the attachment site.

Members of the Cymothoidae Family could cause loss of blood, reduced gill filaments and prejudiced respiratory efficiency (Carvalho, Arruda, & Del-Claro, 2004), besides reduced growth. This parasitism results in ulcerative lesions that opens a portal of entry for secondary infections by bacteria, fungi and viruses (Leonardos & Trilles, 2003; Hirano et al., 2006; Martins, 2004).

Some of these alterations previously reported were found in the present study in pirarucu fingerlings parasitized by B. nasuta. As for example, in the attachment region epithelial perforations and hemorrhages, weight loss and deepening of the ventral region of the host were clearly observed. However, only the histopathological and hematological analysis could confirm the pathogenic action.

Apart from the variations that occur in different fish stages like habit, parasitological indices herein observed were too low and were similar to that reported in tambaqui Colossoma macropomum parasitized by Braga patagonica (2.5% prevalence, intensity 1.0±0.2 and mean abundance 0.03) by Dias et al. (2015). Brandão et al. (2013) observed Braga cigarra from the buccal cavity of Galeocharax knerii captured from the Rivers Veados at 7.7% prevalence, Paranapanema at 31.7% prevalence and Taquari at 5.7% prevalence in Southeast Brazil. In fact, it is difficult to estimate the real prevalence of the parasites in fish due to fishery procedures that use net, leading the fish to escape from the capture, possibly allowing detachment of the parasite, which will search for a new host (Brandão et al., 2013). This event can also explain the low parasitic indices of B. nasuta found in cultured pirarucu in this study. Tavares-Dias, Araújo, Barros, and Viana (2014) were the first authors to register B. patagonica in cultured C. macropomum with 30% prevalence. They argued that the parasites had reached the ponds by the alien fish like traira Hoplias malabaricus, curimatã Curimata cyprinoides and red tail Acestrorhynchus falcatus) from the supplied water once the parasites were also found on those fish. These fish invaded the ponds of C. macropomum from the channels of water supply and by the presence of the parasites could be strongly considered as vectors of B. patagonica (Tavares-Dias et al., 2014). This fact was confirmed by Tavares-Dias et al. (2014) when analyzed alien fish parasitized by B. patagonica present in the channels of water supply for C. macropomum culture.

This situation could be occurred in this study, in which they were fed not only by ration but also by tilapia and curimatã fingerlings, even not having registers of B. nasuta in these species that serve as food to pirarucu. The most important prophylactic measure should be the parasitological examination to make sure if these fish used as food could be act as vector of parasites. Additionally, extending this analysis to other fish species could also reveal if B. nasuta is host-parasite specific or not.

The presence of cymothoid crustaceans in the natural environment was related by Vieira (2006) in a biological inventory of crustaceans from the basin of Sucuriju River, Lake region in the State of Amapá. The authors collected Braga cf. fluviatilis and Braga cf. patagonica from the aquatic and marginal vegetation in the wetland forest. This finding indicates that this parasite can be found in the vegetation increasing the possibility for fish parasitism as normally observed the abundant vegetation on the edges of pirarucu ponds.

Isopods of fish present not only biological importance but also economic one once in high infestations they can provoke significant losses in cultured fish (Eiras et al., 2010; Tavares-Dias, Dias-Júnior, Florentino, Silva, & Cunha, 2015). Cymothoids present morphological structures well adapted to parasitic life that damage the fish tissue. In fish farms, the best management practices to reduce the possibility of high infestations of parasites must be implemented to avoid secondary infections. It is also recommended to verify the water source that supply the ponds, realize adequate prophylactic fish handling, control the amount and quality of feeding, avoid the entrance of vectors and keep the water quality within the normal values for the species. This study presents the first report of the ectoparasite B. nasuta in farmed pirarucu.

Acknowledgements

The authors thank the Conselho Nacional (CNPq) for financial support to M.L. Martins (CNPq 305869-2014-0).

References

Alcântara, N. M., & Tavares-Dias, M. (2015). Structure of the parasites communities in two Erythrinidae fish from Amazon River system (Brazil). Revista Brasileira de Parasitologia Veterinária, 24(2), 183-190.

Brandão, H., Toledo, G. M., Wunderlich, A. C., Ramos, I. P., Carvalho, E. D., & Silva, R. J. (2013). Occurrence of Braga cigarra (Cymothoidae) parasitizing Galeocharax knerii (Characidae) from affluents of Jurumirim reservoir, Brazil. Revista Brasileira de Parasitologia Veterinária, 22(2), 292-296.

Brusca, R. C., Coelho, V., & Taiti, S. (2001). A Guide to the Coastal Isopods of California. Tree of Life Web Project. Retrieved from http://tolweb.org/notes/?note_id=3004

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

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

Dias, M. K. R., Neves, L. R., Marinho, R. G. B., & Tavares-Dias, M. (2015). Parasitic infections in tambaqui from eight fish farms in Northern Brazil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 67(4), 1070-1076.

Eiras, J. C., Takemoto, R. M., & Pavanelli, G. C. (2010). Diversidade dos parasitos de peixes de água doce do Brasil. Maringá, PR: Clichetec.

Eiras, J. C., Takemoto, R. M., & Pavanelli, G. C. (2006). Métodos de estudo e técnicas laboratoriais em parasitologia de peixes. Maringá, PR: UEM.

Hirano, L. Q. L., Bosso, A. C. S., Vieira, L. G., Brito, F. M. M., Pereira, H. C., Silva Júnior, L. M., ... Santos, A. L. Q. (2006). Análise qualitativa e quantitativa de ectoparasitas de Pygocentrus nattereri Kner, 1860 (Characiformes: Characidae) da bacia do rio Araguaia, GO. 19ª RAIB Biológico, 68, 238-360.

Imbiriba, E. P. (2001). Potencial de criação de pirarucu, Arapaima gigas, em cativeiro. Acta Amazonica, 31(2), 299-316.

Lemos de Castro, A. (1959). Sobre as espécies sul-americanas do gênero Braga Schioedte et Meinert, 1881 (Isopoda: Cymothoidae). Rio de Janeiro, RJ: Arquivo do Museu Nacional.

Lemos, J. B., Rodrigues, M. E. B., & Lopes, J. P. (2006). Diagnóstico de ectoparasitas e bactérias em tilápias (Oreochromis niloticus) cultivadas na região de Paulo Afonso, Bahia. Brazilian Journal of Fish Engineering, 1(1), 75-90.

Leonardos, I., & Trilles, J.-P. (2003). Host-parasite relationships: occurrence and effect of the parasitic isopod Mothocya epimerica on sand smelt Atherina boyeri in the Mesolongi and Etolikon Lagoons (W. Greece). Diseases of Aquatic Organisms, 54(3), 243-251.

Martins, M. L. (2004). Cuidados Básicos e Alternativas no Tratamento de Enfermidades de Peixes na Aquicultura Brasileira. In M. J. T. Ranzani-Paiva, R. M. Takemoto, & M. de Los A. P. Lizama, (Eds). Sanidade de Organismos Aquáticos (p. 355-368). São Paulo, SP: Editora Varela.

Ono, E. A., Halverson, M. R., & Kubitza, F. (2004). Pirarucu, o gigante esquecido. Panorama de Aquicultura, 14(81), 14-25.

Ono, E. A., Roubach, R., & Pereira-Filho, M. (2003). Pirarucu production: Advances in Central Amazon, Brazil. Global Aquaculture Advocate, 6, 44-46.

Pereira-Filho, M., Cavero, B. A. S., Roubach, R., Ituassú, D. R., Gandra, A. L., & Crescêncio, R. (2003). Cultivo do Pirarucu (Arapaima gigas) em viveiro escavado. Acta Amazonica, 33(4), 715-718.

Saint-Paul, U. (1986). Potential for aquaculture of south American freshwater fishes; a rewiew. Aquaculture, 54(3), 205-240.

Tavares-Dias, M., Araújo, C. S. O., Barros, M. S., & Viana, G. M. (2014). New hosts and distribution records of Braga patagonica, a parasite cymothoidae of fishes from the Amazon. Brazilian Journal of Aquatic Science and Technology, 18(1), 91-97.

Tavares-Dias, M., Dias-Júnior, 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.

Thatcher, V. E. (2006). Amazon fish parasites. Sofia, Moscow: Pensoft Publishers.

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

Thatcher, V. E. (1996). Braga amapaensis n. sp. (Isopoda, Cymothoidae), a mouth cavity parasite of the Amazonian fish, Acestrorhynchus guyanensis Menezes. Amazoniana, 14(1/2), 121-129.

Thatcher, V. E. (1997). Mouthpart morphology of six freshwater species of Cymothoidae from Amazonian fish compared to that of three marine forms, with the proposal of Artystonenae subfam nov. Amazoniana, 14(3), 311-322.

Thatcher, V. E., Oliveira, A. A. N., & Garcia, A. M. (2009). Braga cigarra comb. nov. for Philostomella cigarra (Crustacea: Isopoda: Cymothoidae) with a redescription of the species based on specimens from Galeocharax kneri, a freshwater fish of Minas Gerais State, Brazil. Zoologia, 26(1), 155-160.

Vieira, I. M. (2006). Inventário biológico da carcinofauna das áreas Sucuriju e região dos Lagos, Amapá. In S. V. Costa Neto (Ed.), Inventário biológico das áreas do Sucuruju e região dos Lagos no Amapá: Relatório Final Probio (p. 143-155). Macapá, AP: IEPA.

Author notes

nunes.mdnunes@gmail.com