28, Bull. Eur. Ass. Fish Pathol., 33(1) 2013

NOTE Parasitic infections in juveniles of Prochilodus nigricans ”Ž™ȱ’—ȱŠȱœŽ–’Ȭ’—Ž—œ’ŸŽȱ꜑ȱ farm in the Peruvian Amazon

P. D. Mathews1*, J. P. D. Mathews2ȱŠ—ȱǯȱǯȱ œ–’Û˜3

1*USP-University of São Paulo, Institute of Biomedical Sciences, Department of Š›Šœ’˜•˜¢ǰȱŖśśŖŞȬşŖŖȱ¨˜ȱŠž•˜ǰȱǰȱ›Š£’•Dzȱ2 National Institute of Amazonian ŽœŽŠ›Œ‘ǰȱŽ™Š›–Ž—ȱ˜ȱŒ˜•˜¢ǰȱŜşŖŜŖȬŖŖŗȱŠ—Šžœǰȱ›Š£’•Dzȱ3 Research Institute of the Peruvian Amazon, Department of Aquatic Ecosystems, 265556, Iquitos, Peru.

Abstract The boquichico Prochilodus nigricans represents a socio-economically important species in the Amazon basin and semi-intensive and intensive production for human consumption has emerged in the •Šœȱ¢ŽŠ›œǯȱ‘›ŽŽȱœ™ŽŒ’Žœȱ˜ȱ™Š›Šœ’Žœȱ Ž›ŽȱŒ˜••ŽŒŽȱŠ—ȱ’Ž—’ꮍDZ Rhinonastes pseudocapsaloideum, Trichodina sp. and Lecithobotrioides elongates. R. pseudocapsaloideum was the most prevalent species (100%) with highest mean intensity and mean abundance (168.5).

Fishes of the genus Prochilodus are among the species is of high economic importance with a most conspicuous, abundant, and widespread promising potential for intensive and extensive freshwater species living in South American aquaculture. Despite the importance of boqui- ›’ŸŽ›œȱ̘ ’—ȱ˜ȱ‘Žȱ•Š—’ŒȱŒŽŠ—ȱǻ’ŸŠœž—Š›ȱ Œ‘’Œ˜ȱŠœȱŠȱŸŠ•žŠ‹•Žȱ˜˜ȱ꜑ȱŠ—ȱŠȱŽœ’›Š‹•Žȱ ŽȱŠ•ǯǰȱŘŖŖŗǼǯȱ‘ŽœŽȱ꜑Žœȱ’—‘Š‹’ȱŠȱ ’ŽȱŸŠ›’Ž¢ȱ ŠšžŠ›’ž–ȱœ™ŽŒ’Žœǰȱ•’Ĵ•Žȱ‘Šœȱ‹ŽŽ—ȱ™ž‹•’œ‘Žȱ˜—ȱ of aquatic ecosystems. P. nigricans, known as bo- its diseases. quichico or curimata, is a species with migratory behavior, which synchronizes its movements Therefore, with the gradual increase of intensive ’‘ȱ ŠŽ›ȱ•ŽŸŽ•ȱ̞ŒžŠ’˜—œǯȱ ȱ’œȱ˜ž—ȱ’—ȱ Š—ȱœŽ–’Ȭ’—Ž—œ’ŸŽȱ꜑ȱŠ›–’—ȱ’—ȱ‘ŽȱŽ›žŸ’Š—ȱ several Amazonian landscape biotypes, such as Amazon, there is a need for constant monitoring ȃŸ¤›£ŽŠȄȱǻ̘˜™•Š’—ȱ’—ž—ŠŽȱ‹¢ȱ ‘’Žȱ ŠŽ›ȱ ˜ȱ‘Žȱ꜑ȱ˜›ȱ‘Žȱ’Š—˜œ’œȱŠ—ȱ’–Ž•¢ȱŒ˜—›˜•ȱ ›’ŸŽ›œǼȱŠ—ȱȃ’Š™àȄȱǻ̘˜™•Š’—ȱ’—ž—ŠŽȱ‹¢ȱ of the parasites. black water rivers) forests, streams and rapids (Lopera-Barreto et al., 2008). P. nigricans can Between August and September 2011, corre- ›ŽŠŒ‘ȱž™ȱ˜ȱŚśȱŒ–ȱ’—ȱ•Ž—‘ǰȱ Ž’‘’—ȱřȱ”ȱ sponding to the relative dry season, 50 individ- ǻŠœ›˜ȱŠ—ȱŠ›’ǰȱŘŖŖŚǼǯȱ˜›Ž˜ŸŽ›ǰȱ‘’œȱ꜑ȱ uals of P. nigricans were collected with drag nets

* Corresponding author’s e-mail: [email protected] Bull. Eur. Ass. Fish Pathol., 33(1) 2013, 29

›˜–ȱŠȱœŽ–’Ȭ’—Ž—œ’ŸŽȱ꜑ȱŠ›–ǰȱ•˜ŒŠŽȱŠȱřŘŞȱ–ȱ structures. Whole mount preparations were above sea level in the northeast of Loreto State made by means of the phenol balsam method ǻŽ›žǼǰȱŠȱ•Š’žŽȱřǚȱŚŞȂȱŚŞǯşȂȂȱȱŠ—ȱ•˜—’žŽȱ ŠŒŒ˜›’—ȱ˜ȱ‘ŠŒ‘Ž›ȱǻŗşşŗǼǯȱ‘Žȱ’Ž—’ęŒŠ’˜—ȱ ŝřǚȱŗşȂȱŗŞȂȂȱǯȱ‘ŽȱŠ›ŽŠȱ‘ŠœȱŠ—ȱŠŸŽ›ŠŽȱŠ——žŠ•ȱ of the parasites was based on the methodol- temperature of 28.6°C and relative humidity ogy of Kritsky et al. (1988), Thatcher (1999) of 85%. and Thatcher (2006). The prevalence, mean intensity and mean abundance of the parasites ‘ŽȱŠ›–Žȱ꜑ȱ Ž›ŽȱŽȱ ’ŒŽȱŠ’•¢ȱ ’‘ȱŽ¡- Ž›ŽȱŒŠ•Œž•ŠŽȱŠŒŒ˜›’—ȱ˜ȱžœ‘ȱŽȱŠ•ǯȱǻŗşşŝǼǯ truded diet containing 25% crude protein and ŘǯŜȱŒŠ•Ȧ”ȱ˜ȱ’Žœ’‹•ŽȱŽ—Ž›¢ǯȱ‘Žȱ–ŽŠ—ȱ The necropsy of juveniles of P. nigricans from •Ž—‘ȱǻƹǼȱ˜ȱ‘ŽȱśŖȱœŠ–™•Žȱ꜑ȱ ŠœȱŘřǯśȱƹȱ a semi-intensive farm in the Peruvian Amazon ŖǯŚȱŒ–ȱŠ—ȱ‘Žȱ–ŽŠ—ȱ Ž’‘ȱǻƹǼȱ ŠœȱŘŘŖǯŝȱƹȱ evidenced the occurrence of the monogene- ŗśǯŚȱǯȱ˜••˜ ’—ȱœŠ–™•’—ǰȱ‘Žȱ꜑ȱ Ž›Žȱ”’••Žȱ an Rhinonastes pseudocapsaloideum in the gill by cerebral puncture and placed individually ꕊ–Ž—œȱŠ—ȱ‘Žȱ—ŠœŠ•ȱŒŠŸ’¢ǰȱ‘Žȱ›Ž–Š˜Žȱ ’—ȱŒ˜—Š’—Ž›œǯȱ ’••œȱ Ž›Žȱ™•ŠŒŽȱ’—ȱꗐŽ›ȱ‹˜ •œȱ Lecithobotrioides elongatus in the intestine and Š—ȱŒ˜ŸŽ›Žȱ ’‘ȱŠȱŗDZŚŖŖŖȱ˜›–Š•’—ȱœ˜•ž’˜—ǯȱ the ciliate Trichodina sp. in the skin. R. pseudo- Ў›ȱ˜—ŽȬ‘Š•ȱ‘˜ž›ǰȱ‘Žȱ’••œȱ Ž›ŽȱŠ’ŠŽȱ’—ȱ capsaloideum was found in all the 50 examined this liquid and then removed from the bowl. ꜑ȱ ‘’•ŽȱTrichodina sp. and L. elongatus were Ž•–’—‘Žœȱ Ž›ŽȱŠ••˜ Žȱ˜ȱœŽĴ•Žȱ˜—ȱ‘Žȱ‹˜Ĵ˜–ȱ found in 30 (60%) and 1 (2%) host specimens, and were subsequently collected with the aid of respectively (Table 1). Šȱœ–Š••ȱ™’™ŽĴŽȱž—Ž›ȱŠȱ’œœŽŒ’—ȱ–’Œ›˜œŒ˜™Žȱ (Nikon SM-30). The counting of protozoa of Several studies report the parasitism of neo- ‘Žȱœ”’—ȱœŒ›Š™’—œȱ˜ȱŽŠŒ‘ȱ꜑ȱ Šœȱ™Ž›˜›–Žȱ tropical characids by monogeneans and cili- using MacMaster chamber under light micros- ates belonging to the genera Rhinonastes and copy and estimated by evaluating the number Trichodina. These parasites groups were also ˜ȱ™Š›Šœ’ŽœȦꎕǯȱ‘Žȱ—ŠœŠ•ȱ˜œœŠŽȱ˜ȱ꜑ȱ Ž›Žȱ ›Ž™˜›Žȱ’—ȱ˜‘Ž›ȱ꜑ȱœ™ŽŒ’ŽœȱŒž•’ŸŠŽȱ’—ȱŽ›žȱ Šœ‘Žȱ ’‘ȱ˜›–Š•’—ȱŗDZŚŖŖŖǰȱŠ—ȱ‘Žȱ•’šž’ȱ (Iannacone and Luque, 1991; Mathews et al., was analyzed under a stereomicroscope. For ŘŖŖŝDzȱ’—’œȱŽȱŠ•ǯǰȱŘŖŖŝǼǯȱ parasitological exams of their stomachs and intestines, the organs were removed and placed Parasites that have a direct life cycle, such as in Petri dishes and then examined. For identi- monogeneans and protozoan, are more fre- ꌊ’˜—ȱ‘Žȱ–˜—˜Ž—ŽŠ—œǰȱ™Ž›–Š—Ž—ȱœ•’Žœȱ quently found in lentic environments and this were prepared with total parasites assembly ac- type of environment favors the transmission of cording to Thatcher (2006). For the observation these parasites. Adult parasites can be found of sclerotized structures, monogeneans were ’—ȱ’••œǰȱœ”’—ǰȱꗍœȱŠ—ȱ—ŠœŠ•ȱŒŠŸ’¢ǰȱ ‘Ž›Žȱ ę¡Žȱ’—ȱŠȱœ˜•ž’˜—ȱ˜ȱŠ––˜—’ž–ȱ™’Œ›ŠŽȱ•¢Œ- ‘Ž¢ȱ•Š¢ȱŽœȱŠ—ȱ’Žȱœ˜˜—ȱŠĞŽ› Š›œǯȱœȱ erine and mounted in Canada balsam according ŽŸŽ•˜™ȱ’›ŽŒ•¢ȱ˜—ȱ‘Žȱ‘˜œǰȱŠ—ȱŠĞŽ›ȱ‘ŠŒ‘- ˜ȱŠ•–‹Ž›ȱǻŗşŝŖǼǯȱ‘Ž›ȱœ™ŽŒ’–Ž—œȱ Ž›Žȱ ’—ǰȱ’ŸŽȱ›’œŽȱ˜ȱ•Š›ŸŠŽȱ‘Šȱœ ’–ȱž—’•ȱꗍ’—ȱ mounted unstained in Gray and Wess’ medium new host where they mature sexually (Thoney and Gomori’s trichrome to visualize internal and Hargis, 1991; Flores-Crespo and Flores, 30, Bull. Eur. Ass. Fish Pathol., 33(1) 2013

Table 1. ›ŽŸŠ•Ž—ŒŽȱǻǼǰȱ–ŽŠ—ȱ’—Ž—œ’¢ȱǻ DzȱƹȱŠ—Š›ȱŽŸ’Š’˜—ǼȱŠ—ȱ–ŽŠ—ȱŠ‹ž—Š—ŒŽȱǻDzȱƹȱŠ—Š›ȱ Deviation) of parasites collected from juveniles of Prochilodus nigricans cultivated in the Peruvian Amazon.

Parasites P(%) MI MA Site of infection Rhinonastes pseudocapsaloideum 100.0 ŗŜśǯŞȱƹȱŗǯřş ŗŜśǯŞȱƹȱŗǯŚŗ ’••œȦ—ŠœŠ•ȱŒŠŸ’¢ Trichodina sp. 60.0 ŗřŞǯŘȱƹȱŖǯŗŝ şśǯŞȱƹȱŖǯŘŖ Skin Lecithobotrioides elongatus 2.0 ŗşǯśȱƹȱŖǯŗŘ Śǯş ƹȱŖǯŗŜ Intestine

ŘŖŖřǼǯȱ‘’œȱŽ¡™•Š’—ȱ ‘¢ȱ™Š›Šœ’Žœȱꗍȱ›ŽŠŽ›ȱ in the Peruvian Amazon. Massive infestations opportunities for development and reproduc- by R. pseudocapsaloideum may explain why the tion in lentic environments and overpopulated ꜑ȱœ˜™™ŽȱŽŽ’—ǰȱŠ—ȱ˜ŸŽ›ȱŠȱŽ ȱŠ¢œǰȱŽŠŒ‘ȱ ꜑ȱŠ›–ȱ™˜—œǯȱ —ȱ›Ž’˜—œȱ ’‘ȱ›˜™’ŒŠ•ȱŠ—ȱ ꜑ȱœžŒŒŽœœ’ŸŽ•¢ȱ‹ŽŠ—ȱ˜ȱœ‘˜ ȱœ’—œȱ˜ȱ•Ž‘Š›- semi-tropical climate, the life cycle of ectopar- gy, colour loss, anorexia and mild hyperpnea asites can be completed in less than one day occasionally leading to mortality. and thus proliferate explosively (Flores-Cres- po and Flores, 2003). The climate in the Peru- R. pseudocapsaloideum was described by Kritsky vian Amazon is tropical humid with annual et al. (1988) from the nasal cavity of P. nigricans temperature average of 28.6°C and relative collected from Janauaca Lake near Manaus, humidity of 85%. In the earthen ponds where Amazonas, Brazil. Furthermore, Lizana et al. ‘Žȱ꜑ȱ Ž›ŽȱŒ˜••ŽŒŽǰȱ‘Žȱ ŠŽ›ȱŒ’›Œž•Š’˜—ȱ ǻŘŖŖśǼȱ’Ž—’ꮍȱœ™ŽŒ’–Ž—œȱ˜ R. pseudocapsa- is almost negligible or non-existent and the loideum in nasal cavity of Prochilodus lineatus ꜑ȱŽ—œ’¢ȱ’œȱ‘’‘ǯȱ‘’œȱŠŸ˜›ȱ›Š—œ–’œœ’˜—ȱ˜ȱ “žŸŽ—’•Žȱ˜ȱ‘Žȱž™™Ž›ȱŠ›Š—¤ȱ’ŸŽ›ȱ̘˜™•Š’—ǰȱ ectoparasites (Flores-Crespo and Flores, 2003; ›Š£’•ǰȱŒ˜—ę›–’—ȱ‘Žȱ˜ŒŒž››Ž—ŒŽȱ˜ȱ‘’œȱœ™ŽŒ’Žœȱ Cable et al., 2002), and may explain the elevated of parasite in the genus Prochilodus. prevalence and abundance of monogenean and ›’Œ‘˜’—’œȱŠ–˜—ȱ‘Žȱ꜑Žœǯ Lizana et al. (2005) reported a prevalence of ŚřǯŜƖȱŠ—ȱŠȱ–ŽŠ—ȱŠ‹ž—Š—ŒŽȱ˜ȱŗǯřȱ˜›ȱR. Among the various groups of helminthes which pseudocapsaloideum in wild P. lineatus collected ™Š›Šœ’Žȱ›Žœ‘ ŠŽ›ȱ꜑Žœǰȱ–Š—¢ȱ–˜—˜Ž—ŽŠ—ȱ from Paraná River, Brazil. In addition, Kritsky et species cause considerable economic losses al. (1988) reported a 15 % prevalence of mono- ’—ȱ ꜑ȱ Š›–’—ȱ ’—ȱ ’쎛Ž—ȱ ›Ž’˜—œȱ ˜ȱ ‘Žȱ geneans in P. nigricans but without giving other world (Marcogliese et al., 2001). Three species parasitic indexes. The much higher prevalence of Monogenoidea are known to parasite the and mean intensity of R. pseudocapsaloideum in genus Prochilodus in the Amazonas River Basin, P. nigricans in our study can be explained by R. pseudocapsaloideum, Anacanthoroides mizel- the unfavorable environmental conditions and lei, Tereancistrum ornatus (Kritsky et al., 1988; ‘’‘ȱ꜑ȱŽ—œ’’Žœȱ’—ȱ‘Žȱ꜑ȱŠ›–ǯȱ Thatcher, 2006). In our study R. pseudocapsaloi- deumȱ’œȱ›Ž™˜›Žȱ˜›ȱ‘Žȱꛜȱ’–Žȱ’—ȱ“žŸŽ—’•Žœȱ˜ȱ —ȱ‘Žȱ™›ŽœŽ—ȱœž¢ȱ Žȱ›Ž™˜›ȱ˜›ȱ‘Žȱꛜȱ boquichico (P. nigiricans) in farmed conditions time parasitic infections in farmed P. nigricans Bull. Eur. Ass. Fish Pathol., 33(1) 2013, 31

turushuqui oxidoras niger en la Amazonía farms in the Peruvian Amazon. There was a peruana. Boletín de Lima 13ǰȱŚřȬŚŝǯ high prevalence and abundance of the mono- Kritsky DC, Thatcher VE and Boeger WA genean R. pseudocapsaloideum. The results of this (1988). Neotropical Monogenea. 13. study and studies addressing various aspects Rhinonastes pseudocapsaloideum n. gen., n. sp. of parasites in other species cultivated in the (Dactylogyridae, Ancyrocephalinae), a nasal same region (Mathews et al., 2011; Alcantara parasite of curimatá, Prochilodus nigricans Agassiz (Cypriniformes, Prochilodontidae), ŽȱŠ•ǯǰȱŘŖŖŞǼȱŒ˜—ę›–ȱ‘Žȱ—ŽŒŽœœ’¢ȱ˜ȱŒ˜—œŠ—ȱ in Brazil. Journal of Parasitology 74, 695-698. –˜—’˜›’—ȱ˜ȱ꜑ǰȱœŽŽ”’—ȱ‘Žȱ’Š—˜œ’œȱŠ—ȱ Lizama MAP, Takemoto RM, and Pavanelli timely control of infestations by monogeneans, ȱǻŘŖŖśǼǯȱ —ĚžŽ—ŒŽȱ˜ȱ‘˜œȱœŽ¡ȱŠ—ȱŠŽȱ ’—ȱ˜›Ž›ȱ˜ȱ›ŽžŒŽȱ꜑ȱ–˜›Š•’¢ǯ on infracommunites of metazoan parasites of Prochilodus lineatus (Valenciennes, 1836) References (Prochilodontidae) of the upper Paranà Alcantara FB, Chu-Koo FW, Rodriguez L, River Floodplain, Brazil. Parasite, 12, 299- Chavez C, Burney A, Barbaran T, Tello S and řŖŚǯȱ žÛŽ£ȱ ȱǻ2008). First report of parasitism of Lopera-Barreto NM, Ribeiro RP, Vargas L, Brachyplatistoma tigrimun by Argulus pestifer Povh JA, Gomes P C, Mangolin CA, Boso in Aquaculture. Folia Amazonica 17, 99-102. ȱŠ—ȱ žŠ•ŠȱȱǻŘŖŖŞǼǯȱŠ›ŠŒŽ›’£Š³¨˜ȱ žœ‘ȱǰȱŠěŽ›¢ȱ ǰȱ˜œȱ ȱŠ—ȱ‘˜œŠ”ȱ genética de estoques de Prochilodus lineatus ȱǻŗşşŝǼǯȱŠ›Šœ’˜•˜¢ȱ–ŽŽœȱŽŒ˜•˜¢ȱ˜—ȱ Valenciennes, 1836) (Characiformes:Proc its own terms: Margolis et al. revisited. hilodontidae), utilizados em programas Journal of Parasitology 83ǰȱśŝśȬśŞřǯ de repovoamento: importância para a Œ˜—œŽ›ŸŠ³¨˜ȱŠȱ’Œ’˜Šž—ŠȱŽȱ˜ȱŽŒ˜œœ’œŽ–Šǯȱ Š‹•ŽȱǰȱŒ˜Ĵȱǰȱ’—œ•Ž¢ȱȱŠ—ȱ Š››’œȱȱ Bioscience Journal 24, 86-93. (2002). Behavior favoring transmission in the viviparous monogenean Gyrodactylus Š•–‹Ž›ȱ ȱǻŗşŝŖǼǯȱ‘ŽȱŽ¡Œ›Ž˜›¢ȱœ¢œŽ–œȱ turnbulli. Journal of Parasitology 1ǰȱŗŞřȬŗŞŚǯ and the marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda, Šœ›˜ȱȱŠ—ȱŠ›’ȱȱǻŘŖŖŚǼǯȱŽ›’’Ÿ˜›Žœȱ Monogenea). Arkiv för Zoologi 2, 1-23. of the South American Fish Family Prochilodontidae (Teleostei: Ostariophysi: Marcogliese DJ, Ball M and Lankester MW Characiformes): A Phylogenetic and ǻŘŖŖŗǼǯȱ˜Ž—’Š•ȱ’–™ŠŒœȱ˜ȱŒ•ŽŠ›ŒžĴ’—ȱ˜—ȱ Revisionary study. Smithsonian Contributions parasites of minnows in small boreal lakes. to Zoology 622, 83-89. Folia Parasitologica 48ǰȱŘŜşȬŘŝŚǯȱ Dinis VN, Mathews DP, Chu-Koo FW, Tello MS Mathews DP, Chu–Koo FW, Tello MS, Malta Š—ȱ œ–’Û˜ȱȱǻŘŖŖŝǼǯȱŠž—Šȱ™Š›Šœ’Š›’Šȱ ǰȱŠ›Ž••ŠȱȱŠ—ȱ ˜–ŽœȱȱǻŘŖŖŝǼǯȱ de juveniles de arahuana, Osteoglossum Fauna ectoparasitaria en alevinos de paiche bicirrhosum (Vandelli, 1829) cultivado en Arapaima gigas (Shinz, 1822) cultivados en el el Centro de Investigaciones de Quistocoha, centro de Investigaciones de Quistococha, Loreto, Perú. Folia Amazonica 16, 29-33. Loreto, Perú. Folia Amazonica 16ǰȱŘřȬŘŝǯ Flores-Crespo J and Flores RC (2003). Š‘Ž œȱǰȱŠ‘Ž œȱ ǰȱŽŠȱ ȱŠ—ȱ œ–’Û˜ȱ ˜—˜Ž—ŽŠ—ȱ™Š›Šœ’Žœȱ’—ȱŽ¡’ŒŠ—ȱ꜑DZȱŠȱ OR (2011). Massive infestation by Perulernaea recapitulation. Técnica Pecuaria México 41, gamitanae (Crustacea: Cyclopoida: ŗŝśȬŗşŘǯ Lernaidae) in juvenile gamitana, cultured in the Peruvian Amazon. Veterinaria México Iannacone J and Luque JL (1991). Monogeneos 42ǰȱśşȬŜŚǯ parásitos del paiche, Arapaima gigas y del Sivasundar A, Bermingham E and Orti G (2001). 32, Bull. Eur. Ass. Fish Pathol., 33(1) 2013

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