Acessibilidade / Reportar erro

Lernaea cyprinacea Linnaeus, 1758 (Cyclopoida: Lernaeidae) in ornamental fish from a commercial fish farm in the state of Pará, Brazilian Amazon

Brazil is on the rise in terms of ornamental fish farming (aquarism) (Brasil, 2019BRASIL, E.M., 2019. Óleos essenciais de Lippia spp. em carpa koi Cyprinus carpio: atividade antiparasitária, hematologia, histologia e desempenho zootécnico. Florianópolis: Universidade Federal de Santa Catarina. Tese de Doutorado em Aquicultura.). Among the most important species cultivated in the country, those of the species Carassius auratus Linnaeus, 1758 (popularly known as goldfish) and Xiphophorus hellerii Heckel, 1848 (known as green swordtail) stand out because of the uniqueness in their color pattern as well as the characteristics of sexual dimorphism (Florindo, 2016FLORINDO, M.C., 2016. Diversidade de parasitos de peixes ornamentais dulcícolas cultivados em Santa Catarina. Florianópolis: Universidade Federal de Santa Catarina. Dissertação de Mestrado em Aquicultura.).

The intensification in the breeding of ornamental fish may favor the loss of balance between the host-parasite environment, resulting in a higher manifestation and transmission of disease (Garcia et al., 2009GARCIA, F., FUGIMOTO, R.Y., MARTINS, M.L. and MORAES, F.R., 2009. Protozoan parasites of Xiphophorus spp. (Poeciliidae) and their relation with water characteristics. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, vol. 61, no. 1, pp. 156-162. https://doi.org/10.1590/S0102-09352009000100022.
https://doi.org/10.1590/S0102-0935200900...
; Martins et al., 2012MARTINS, M.L., MARCHIORI, N., ROUMBEDAKIS, K. and LAMI, F., 2012. Trichodina nobilis Chen, 1963 and Trichodina reticulata Hirschmann et Partsch, 1955 from ornamental freshwater fishes in Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 72, no. 2, pp. 281-286. http://dx.doi.org/10.1590/S1519-69842012000200008. PMid:22735135.
http://dx.doi.org/10.1590/S1519-69842012...
). Among these, stand out those related to macroparasites such as Lernaea cyprinacea Linnaeus, 1758, a copepod crustacean of a cosmopolitan character, which was introduced in Brazil through carp originating from Hungary. The clinical signs involved in parasitism are imbalance, wandering swimming, lethargy, apathy, opacity in the eyes, hemorrhages in the body, cavitation areas on the fins, itching, and consequently, change in behavior (Florindo, 2016FLORINDO, M.C., 2016. Diversidade de parasitos de peixes ornamentais dulcícolas cultivados em Santa Catarina. Florianópolis: Universidade Federal de Santa Catarina. Dissertação de Mestrado em Aquicultura.). The present work report the infestation by L. cyprinacea in ornamental fish of the species X. hellerii and C. auratus from a commercial farm in the state of Pará, Brazilian Amazon.

The animals evaluated in this study come from a commercial property dedicated to the creation of ornamental fish, located in the municipality of Santa Izabel do Pará, a municipality located in the metropolitan mesoregion of the state of Pará, Eastern Amazon, Brazil. In this property, an outbreak of ectoparasitism occurred in fish of the species X. hellerii (green swordtail) and C. auratus (Goldfish) that were kept in mixed cultivation in a 1m3 asbestos tank, which held a total of 50 fish. According to the person responsible for the creation, the outbreak occurred after the acquisition of a male goldfish originating from the municipality of Ananindeua, Pará, Brazil. The animal was introduced in the fish stock of the property that was free of infestation, without respecting a quarantine period. For ectoparasite research, a random sampling of fish from both species was carried out, undergoing individual examinations through visual and physical inspection, biometrics, and sexing. The identification was based on morphology using the dichotomous key for genera and species of post-metamorphic females of the Lernaeidae family in South America, as proposed by Thatcher (2006)THATCHER, V.E., 2006. Amazon fish parasites. 2nd ed. Sofia-Moscow: Pensoft Publishers, 508 p..

A sampling of 40 individuals was carried out, being 28 X. hellerii. The individuals of this species were 12 males and 16 females, and presented a varied color pattern between albino, lyre and common. Through biometrics of this species, it was observed that the analyzed fish had an average total length of 8.53 cm (±2.95; 5.5-11.5 cm). The species C. auratus was composed of 12 specimens, being two females, six males, and four young individuals of unidentified sex. The color pattern corresponded to pearl, oranda and telescope, and its average total length was 8.79 cm (±1.54; 4-15.5 cm).

The parasites had morphological characteristics corresponding to the species L. cyprinacea: head with four large anchors, frequently branched; genital pore near posterior extremity; and fourth legs on hindbody (Figure 1). Regarding the prevalence rate, 75% (30/40) of the fish from both species were infested, from which 59 parasites were recovered (Table 1). The lesions were distributed in the vicinity of the pectoral fins, caudal, in the dorsal and ventral regions of the body, and in one animal, parasitism was observed in the region of the nostrils. The clinical signs of the fish of both species were anorexia, lethargy, and erratic swimming.

Figure 1
Parasitism by Lernaea cyprinacea in fish evaluated in the present study. (A) Carassius auratus fish presenting L. cyprinacea fixed anteriorly to the caudal fin (arrow); (B) Same specimen showing deep skin lesion (arrow) after removing the parasite; (C) Xiphophorus hellerii in prone position, presenting multiple specimens of L. cyprinacea fixed between the spine dorsal and soft dorsal fins; (D) Female L. cyprinacea (scale bar: 1 cm).
Table 1
Parasitic ecology indexes obtained for Lernaea cyprinacea in Carassius auratus and Xiphophorus hellerii from the present work.

The present work presents important data on the infestation by L. cyprinacea in two species of exotic ornamental fish kept in a commercial farm in the state of Pará. Through this work, we highlight the importance of carrying out prophylactic measures to introduce new animals, such as quarantine and other hygienic-sanitary self-control measures to prevent disease outbreaks, like the one described in this research.

Freshwater fish specimens are grown in large proportions in shops spread across the world (Zuanon et al., 2011ZUANON, J.A., SALARO, A.L. and FURUYA, W.M., 2011. Produção e nutrição de peixes ornamentais. Revista Brasileira de Zootecnia, vol. 40, no. 1, pp. 165-174.). Some of the most common ones are those of the species X. hellerii (green swordtail) and C. auratus (goldfish), as evaluated in this work (Zuanon et al., 2011ZUANON, J.A., SALARO, A.L. and FURUYA, W.M., 2011. Produção e nutrição de peixes ornamentais. Revista Brasileira de Zootecnia, vol. 40, no. 1, pp. 165-174.; Florindo, 2016FLORINDO, M.C., 2016. Diversidade de parasitos de peixes ornamentais dulcícolas cultivados em Santa Catarina. Florianópolis: Universidade Federal de Santa Catarina. Dissertação de Mestrado em Aquicultura.). According to Martins et al. (2007)MARTINS, M.L., GARCIA, F., PIAZZA, R.S. and GHIRALDELLI, L., 2007. Camallanus maculatus n. sp. (Nematoda: Camallanidae) in an ornamental fish Xiphophorus maculatus (Osteichthyes: Poeciliidae) cultivated in São Paulo State, Brazil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, vol. 59, no. 5, pp. 1224-1230. http://dx.doi.org/10.1590/S0102-09352007000500019.
http://dx.doi.org/10.1590/S0102-09352007...
, the introduction of ornamental fish imported from several countries culminated in the spread of parasite infections, including Brazil, due to the growing trade in fishkeeping. Therefore, it can be said that the introduction of invasive species through this market has become an increasing risk worldwide (Peeler et al., 2011PEELER, E.J., OIDTMANN, B.C., MIDTLYNG, P.J., MIOSSEC, L. and GOZLAN, R.E., 2011. Non-native aquatic animals introductions have driven disease emergence in Europe. Biological Invasions, vol. 13, no. 6, pp. 1291-1303. http://dx.doi.org/10.1007/s10530-010-9890-9.
http://dx.doi.org/10.1007/s10530-010-989...
; Whittington and Chong, 2007WHITTINGTON, R.J. and CHONG, R., 2007. Global trade in ornamental fish from an Australian perspective: the case for revised import risk analysis and management strategies. Preventive Veterinary Medicine, vol. 81, no. 1-3, pp. 92-116. http://dx.doi.org/10.1016/j.prevetmed.2007.04.007. PMid:17485126.
http://dx.doi.org/10.1016/j.prevetmed.20...
).

The copepod L. cyprinacea parasite is a non-native species that was first cataloged in Brazil in the 1960s, being disseminated from then on to all Brazilian regions (Brasil, 2019BRASIL, E.M., 2019. Óleos essenciais de Lippia spp. em carpa koi Cyprinus carpio: atividade antiparasitária, hematologia, histologia e desempenho zootécnico. Florianópolis: Universidade Federal de Santa Catarina. Tese de Doutorado em Aquicultura.). A study by Assis et al. (2014)ASSIS, D.A.S., CAVALCANTE, S.S. and BRITO, M.F.G., 2014. Aquarium trade as a potential disseminator of non-native invertebrates in Northeastern Brazil. Neotropical Biology and Conservation, vol. 9, no. 2, pp. 115-119., confirmed the presence of Lernaea cyprinacea in four aquarium establishments in Aracaju, northeastern Brazil, including C. auratus and X. hellerii, corroborating the data obtained from the present study. The authors report that measures such as adopting quarantine and not disposing of waste water in common sewage are actions that prevent the spread and establishment of the parasite, including from the point of view of environmental contamination and the possibility of infestation in native species. Other findings of L. cyprinacea in these hosts are also presented in Table 2.

Table 2
Comparative prevalence rate of Lernaea cyprinacea infestation in Carassius auratus and Xiphophorus hellerii.

The contamination that occurs in tanks/aquariums is believed to be due to cross-contamination, such as the insertion of different species in the same environment, management failures like breaking the quarantine period as well as the lack of technification and supervision of trained professionals who adequately guide the producer (Cardoso et al., 2017CARDOSO, P.H.M., COSTA, A.R.D., PESTELLI, M. and BALIAN, S.C., 2017. Relato de caso de parasitismo por Monogenea no peixe ornamental Polypterus palmas no Brasil. Revista de Educação Continuada em Medicina Veterinária e Zootecnia, vol. 15, no. 1, pp. 30-36. http://dx.doi.org/10.36440/recmvz.v15i1.36763.
http://dx.doi.org/10.36440/recmvz.v15i1....
). These problems were also observed in this work, especially in relation to quarantine, which was not established when introducing an animal, resulting in harm to the squad, as reported by Cardoso et al. (2017)CARDOSO, P.H.M., COSTA, A.R.D., PESTELLI, M. and BALIAN, S.C., 2017. Relato de caso de parasitismo por Monogenea no peixe ornamental Polypterus palmas no Brasil. Revista de Educação Continuada em Medicina Veterinária e Zootecnia, vol. 15, no. 1, pp. 30-36. http://dx.doi.org/10.36440/recmvz.v15i1.36763.
http://dx.doi.org/10.36440/recmvz.v15i1....
. These authors emphasize that the isolation of these fish is mandatory, and it is essential to apply it in a period of time necessary for possible manifestation of signs and changes in illnesses, which is also reinforced by the present study.

Tavares-Dias et al. (2011)TAVARES-DIAS, M., NEVES, L.R., SANTOS, E.F., DIAS, M.K.R., MARINHO, R.G.B. and ONO, E.A., 2011. Perulernaea gamitanae (Copepoda: Lernaeidae) parasitizing tambaqui (Colossoma macropomum) (Characidae) and the hybrids tambacu and tambatinga, cultured in Northern Brazil. Colossoma macropomum. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, vol. 63, no. 4, pp. 988-995. http://dx.doi.org/10.1590/S0102-09352011000400026.
http://dx.doi.org/10.1590/S0102-09352011...
stated that diseases caused by parasites of the family Lernaeidae in fish populations have high and rapid capacity for dissemination and proliferation, mainly in captive animals (kept in tanks/aquariums), due to the closed breeding system. The author also states that normally in small fish, it is possible to visualize a more intense infestation by parasites, as was observed in the present study, where the fish presented up to seven parasites adhered to the surface of the body. In a study conducted in São Paulo on the fauna of ectoparasites in several species of ornamental fish, including C. auratus (n = 31) and X. hellerii (n = 8), Cardoso et al. (2019)CARDOSO, P.H.M., COSTA, A.R. and BALIAN, S.C., 2019. Ectoparasitic fauna in freshwater ornamental fish acquired by a wholesaler in the city of São Paulo. Brazilian Journal of Veterinary Research and Animal Science, vol. 55, no. 4, pp. e144086. http://dx.doi.org/10.11606/issn.1678-4456.bjvras.2018.144086.
http://dx.doi.org/10.11606/issn.1678-445...
reported that 80% (215/268) of all fish sampled were infested with parasites, although only 4.5% (10/215) of these were infested with Lernaea spp.. The study showed a low prevalence rate compared to the percentages obtained in this study, in which the prevalence was 75% (30/40).

Fernandes (2003)FERNANDES, G.Q., 2003. Ocorrência de metazoários parasitos de infrapopulações das espécies de peixes Conodon nobilis (Pisces, Haemulidae) (Linnaeus, 1758) e Brycon insignis (Pisces, Characidae) (Steindachner, 1876). Rio de Janeiro: Universidade Estadual do Norte Fluminense. Dissertação de Mestrado em Produção Animal. reported that infestation by Lernaea spp. leads to high mortality rates, reaching up to 100% of a squad, if there is no adequate treatment in a timely manner and also depending on the parasitic intensity. In addition, the consequences revolve around the damage done to the appearance of the fish, due to injuries caused by copepod hooks when adhering to the skin and musculature, as evidenced in the animals of the present study.

The parasitized animals showed a higher frequency of ectoparasite in the dorsal and caudal regions, especially in the fins, findings similar to those previously described by Gallio et al. (2007)GALLIO, M., SILVA, A.S. and MONTEIRO, S.G., 2007. Parasitismo por Lernaea cyprinacea em Astyanax bimaculatus provenientes de um açude no município de Antônio Prado, Rio Grande do Sul. Acta Scientiae Veterinariae, vol. 35, no. 2, pp. 209-212. http://dx.doi.org/10.22456/1679-9216.15973.
http://dx.doi.org/10.22456/1679-9216.159...
. The injuries caused in these regions can evolve into ulcerations and deep injuries, providing secondary infections, according to Cardoso and Balian (2016)CARDOSO, P.H.M. and BALIAN, S.C., 2016. Lymphocystis virus em peixes ornamentais importados para o Brasil. Revista de Educação Continuada em Medicina Veterinária e Zootecnia, vol. 14, no. 1, pp. 6-11. http://dx.doi.org/10.36440/recmvz.v14i1.31030.
http://dx.doi.org/10.36440/recmvz.v14i1....
. Regarding clinical signs, Florindo (2016)FLORINDO, M.C., 2016. Diversidade de parasitos de peixes ornamentais dulcícolas cultivados em Santa Catarina. Florianópolis: Universidade Federal de Santa Catarina. Dissertação de Mestrado em Aquicultura. described that the infested animals show, among other signs, weight loss, anorexia, erratic and lateralized swimming, lethargy, and reduced growth rate. Some of these signs were also observed in the animals in the present study, which had anorexia, lethargy, and erratic swimming.

As described by Cardoso and Balian (2016)CARDOSO, P.H.M. and BALIAN, S.C., 2016. Lymphocystis virus em peixes ornamentais importados para o Brasil. Revista de Educação Continuada em Medicina Veterinária e Zootecnia, vol. 14, no. 1, pp. 6-11. http://dx.doi.org/10.36440/recmvz.v14i1.31030.
http://dx.doi.org/10.36440/recmvz.v14i1....
, and reinforced by the present work, monitoring by veterinarians in these establishments is essential, in order to plan and establish preventive measures, hygienic-sanitary control, and treatment of animals to safeguard the squad's health.

The present study detected a high prevalence of infestation by L. cyprinacea in ornamental fish of the species C. auratus and X. hellerii in a commercial farm in Santa Izabel do Pará, Brazil. The data found reinforce the importance of using quarantine to introduce newly acquired animals, for the prevention of disease outbreaks as the one described in this research.

References

  • ADEL, M., GHASEMPOUR, F., AZIZI, H.R., SHATERI, M.H. and SAFIAN, A.R., 2015. Survey of parasitic fauna of different ornamental freshwater fish species in Iran. Veterinary Research Forum : An International Quarterly Journal, vol. 6, no. 1, pp. 75-78. PMid:25992255.
  • ASSIS, D.A.S., CAVALCANTE, S.S. and BRITO, M.F.G., 2014. Aquarium trade as a potential disseminator of non-native invertebrates in Northeastern Brazil. Neotropical Biology and Conservation, vol. 9, no. 2, pp. 115-119.
  • BRASIL, E.M., 2019. Óleos essenciais de Lippia spp. em carpa koi Cyprinus carpio: atividade antiparasitária, hematologia, histologia e desempenho zootécnico. Florianópolis: Universidade Federal de Santa Catarina. Tese de Doutorado em Aquicultura.
  • CARDOSO, P.H.M. and BALIAN, S.C., 2016. Lymphocystis virus em peixes ornamentais importados para o Brasil. Revista de Educação Continuada em Medicina Veterinária e Zootecnia, vol. 14, no. 1, pp. 6-11. http://dx.doi.org/10.36440/recmvz.v14i1.31030
    » http://dx.doi.org/10.36440/recmvz.v14i1.31030
  • CARDOSO, P.H.M., COSTA, A.R. and BALIAN, S.C., 2019. Ectoparasitic fauna in freshwater ornamental fish acquired by a wholesaler in the city of São Paulo. Brazilian Journal of Veterinary Research and Animal Science, vol. 55, no. 4, pp. e144086. http://dx.doi.org/10.11606/issn.1678-4456.bjvras.2018.144086
    » http://dx.doi.org/10.11606/issn.1678-4456.bjvras.2018.144086
  • CARDOSO, P.H.M., COSTA, A.R.D., PESTELLI, M. and BALIAN, S.C., 2017. Relato de caso de parasitismo por Monogenea no peixe ornamental Polypterus palmas no Brasil. Revista de Educação Continuada em Medicina Veterinária e Zootecnia, vol. 15, no. 1, pp. 30-36. http://dx.doi.org/10.36440/recmvz.v15i1.36763
    » http://dx.doi.org/10.36440/recmvz.v15i1.36763
  • FERNANDES, G.Q., 2003. Ocorrência de metazoários parasitos de infrapopulações das espécies de peixes Conodon nobilis (Pisces, Haemulidae) (Linnaeus, 1758) e Brycon insignis (Pisces, Characidae) (Steindachner, 1876). Rio de Janeiro: Universidade Estadual do Norte Fluminense. Dissertação de Mestrado em Produção Animal.
  • FLORINDO, M.C., 2016. Diversidade de parasitos de peixes ornamentais dulcícolas cultivados em Santa Catarina Florianópolis: Universidade Federal de Santa Catarina. Dissertação de Mestrado em Aquicultura.
  • GALLIO, M., SILVA, A.S. and MONTEIRO, S.G., 2007. Parasitismo por Lernaea cyprinacea em Astyanax bimaculatus provenientes de um açude no município de Antônio Prado, Rio Grande do Sul. Acta Scientiae Veterinariae, vol. 35, no. 2, pp. 209-212. http://dx.doi.org/10.22456/1679-9216.15973
    » http://dx.doi.org/10.22456/1679-9216.15973
  • GARCIA, F., FUGIMOTO, R.Y., MARTINS, M.L. and MORAES, F.R., 2009. Protozoan parasites of Xiphophorus spp. (Poeciliidae) and their relation with water characteristics. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, vol. 61, no. 1, pp. 156-162. https://doi.org/10.1590/S0102-09352009000100022
    » https://doi.org/10.1590/S0102-09352009000100022
  • LAMI, F., 2009. Fauna parasitária de peixes ornamentais comercializados no estado de Santa Catarina, Brasil Florianópolis: Departamento de Aquicultura, Universidade Federal de Santa Catarina, 23 p. Relatório de estágio supervisionado.
  • MARTINS, M.L., GARCIA, F., PIAZZA, R.S. and GHIRALDELLI, L., 2007. Camallanus maculatus n. sp. (Nematoda: Camallanidae) in an ornamental fish Xiphophorus maculatus (Osteichthyes: Poeciliidae) cultivated in São Paulo State, Brazil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, vol. 59, no. 5, pp. 1224-1230. http://dx.doi.org/10.1590/S0102-09352007000500019
    » http://dx.doi.org/10.1590/S0102-09352007000500019
  • MARTINS, M.L., MARCHIORI, N., ROUMBEDAKIS, K. and LAMI, F., 2012. Trichodina nobilis Chen, 1963 and Trichodina reticulata Hirschmann et Partsch, 1955 from ornamental freshwater fishes in Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 72, no. 2, pp. 281-286. http://dx.doi.org/10.1590/S1519-69842012000200008 PMid:22735135.
    » http://dx.doi.org/10.1590/S1519-69842012000200008
  • MIRZAEI, M., 2015. Prevalence and histopathologic study of Lernaea cyprinacea in two species of ornamental fish (Poecilia latipinna and Xiphophorus helleri) in Kerman, south-east Iran. Turkiye Parazitoloji Dergisi, vol. 39, no. 3, pp. 222-226. http://dx.doi.org/10.5152/tpd.2015.3960 PMid:26470930.
    » http://dx.doi.org/10.5152/tpd.2015.3960
  • PEELER, E.J., OIDTMANN, B.C., MIDTLYNG, P.J., MIOSSEC, L. and GOZLAN, R.E., 2011. Non-native aquatic animals introductions have driven disease emergence in Europe. Biological Invasions, vol. 13, no. 6, pp. 1291-1303. http://dx.doi.org/10.1007/s10530-010-9890-9
    » http://dx.doi.org/10.1007/s10530-010-9890-9
  • TAVARES-DIAS, M., NEVES, L.R., SANTOS, E.F., DIAS, M.K.R., MARINHO, R.G.B. and ONO, E.A., 2011. Perulernaea gamitanae (Copepoda: Lernaeidae) parasitizing tambaqui (Colossoma macropomum) (Characidae) and the hybrids tambacu and tambatinga, cultured in Northern Brazil. Colossoma macropomum. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, vol. 63, no. 4, pp. 988-995. http://dx.doi.org/10.1590/S0102-09352011000400026
    » http://dx.doi.org/10.1590/S0102-09352011000400026
  • THATCHER, V.E., 2006. Amazon fish parasites 2nd ed. Sofia-Moscow: Pensoft Publishers, 508 p.
  • THILAKARATNE, I.D.S.I.P., RAJAPAKSHA, G., HEWAKOPARA, A., RAJAPAKSE, R.P.V.J. and FAIZAL, A.C.M., 2003. Parasitic infections in freshwater ornamental fish in Sri Lanka. Diseases of Aquatic Organisms, vol. 54, no. 2, pp. 157-162. http://dx.doi.org/10.3354/dao054157 PMid:12747641.
    » http://dx.doi.org/10.3354/dao054157
  • WHITTINGTON, R.J. and CHONG, R., 2007. Global trade in ornamental fish from an Australian perspective: the case for revised import risk analysis and management strategies. Preventive Veterinary Medicine, vol. 81, no. 1-3, pp. 92-116. http://dx.doi.org/10.1016/j.prevetmed.2007.04.007 PMid:17485126.
    » http://dx.doi.org/10.1016/j.prevetmed.2007.04.007
  • ZUANON, J.A., SALARO, A.L. and FURUYA, W.M., 2011. Produção e nutrição de peixes ornamentais. Revista Brasileira de Zootecnia, vol. 40, no. 1, pp. 165-174.

Publication Dates

  • Publication in this collection
    17 Jan 2022
  • Date of issue
    2024

History

  • Received
    16 July 2021
  • Accepted
    13 Dec 2021
Instituto Internacional de Ecologia R. Bento Carlos, 750, 13560-660 São Carlos SP - Brasil, Tel. e Fax: (55 16) 3362-5400 - São Carlos - SP - Brazil
E-mail: bjb@bjb.com.br