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Haliotrema aurigae (Yamaguti, 1968) Plaisance, Bouamer & Morand, 2004, in ornamental reef fish imported into Brazil

Haliotrema aurigae (Yamaguti, 1968) Plaisance, Bouamer & Morand, 2004, em peixe ornamental de recife importado para o Brasil

Abstract

More than 1.450 marine fish species are commercialized as ornamental fish and approximately 90% of these are wild-caught. Rainford's butterflyfish, Chaetodon rainfordi (McCulloch, 1923), is endemic to the western Pacific. This fish species belongs to one of the main ornamental fish families imported into Brazil. Haliotrema is a genus of the family Dactylogyridae. Species of this genus have very interesting host associations and geographic distributions. The aim of this study was to report on occurrences of exotic Haliotrema aurigae in diseased Rainford butterflyfish that were imported to Brazil. One Rainford’s butterflyfish with suspected parasitic disease was euthanized and subjected to skin and gill scraping. The parasite specimens were mounted on semi-permanent slides with Hoyer’s solution for morphological analysis of sclerotized structures. The hard-sclerotized structures of these specimens were compared and were identified as those of Haliotrema aurigae (Yamaguti, 1968). These results emphasize the importance of implementation of correct control measures at the country’s borders, to avoid the introduction of exotic parasites. In addition, it can be emphasized that the easy adaptation of this parasite to new environments is a concern for ornamental fish farmers.

Keywords:
Aquatic health; parasitic disease; exotic parasite

Resumo

Mais de 1.450 espécies de peixes marinhos são comercializados como peixes ornamentais e, aproximadamente, 90% são extraídos na natureza. O peixe borboleta Rainford, Chaetodon rainfordi (McCulloch, 1923), é endêmico no Pacífico Ocidental. Esta espécie de peixe pertence a uma das principais famílias importadas para o Brasil. Haliotrema é um gênero da família Dactylogyridae. Espécies desse gênero têm associação com hospedeiros e distribuição geográfica. O objetivo deste estudo é relatar a ocorrência de Haliotrema aurigae exótico, em peixes-borboleta doentes, que foram importados para o Brasil. Um peixe-borboleta Rainford, suspeito de estar infectado com doença parasitária, foi eutanasiado e submetido à raspagem de pele e brânquias. As amostras foram montadas em lâminas semipermanentes com Hoyer, para análise morfológica de estruturas esclerotizadas. A morfologia e as estruturas esclerotizadas duras das amostras foram comparadas e identificadas como Haliotrema aurigae (Yamaguti, 1968). Esses resultados enfatizam a importância da implementação de medidas de controle pós-fronteira para evitar a introdução de parasitas exóticos no país. Além disso, pode-se enfatizar que a fácil adaptação do parasita a um novo ambiente é uma preocupação para os pscicultores ornamentais.

Palavras-chave:
Saúde aquática; doença parasitária; parasita exótico

With the growth of fishkeeping in Brazil, trading imported ornamental fish has gained importance over the years. In 2014, the aquarium market had a turnover of more than 18 million dollars, putting the country among the eight largest exporters in the world (Dey, 2016Dey VK. The global trade in ornamental fish [online]. Kuala Lumpur: Infofish International; 2016 [cited 2019 Sept 1]. Available from: https://www.bassleer.com/ornamentalfishexporters/wp-content/uploads/sites/3/2016/12/GLOBAL-TRADE-IN-ORNAMENTAL-FISH.pdf
https://www.bassleer.com/ornamentalfishe...
). Fifteen percent of these exported fish were marine fish. Although keeping marine fish is expensive, the demand for these fish has grown through new technologies that have arisen to facilitate the maintenance of saltwater aquariums. However, exporting and importing of ornamental fish can lead to invasion of exotic species and may pose risks to local biodiversity (Lymbery et al., 2014Lymbery AJ, Morine M, Kanani HG, Beatty SJ, Morgan DL. Co-invaders: the effects of alien parasites on native hosts. Int J Parasitol Parasites Wildl 2014; 3(2): 171-177. http://dx.doi.org/10.1016/j.ijppaw.2014.04.002. PMid:25180161.
http://dx.doi.org/10.1016/j.ijppaw.2014....
). The ornamental fish trade is characterized by aggregation of fish species from several countries. More than 1.450 marine fish species are commercialized as ornamental fish and approximately 90% of these are caught from the wild environment. Thus, many pathogenic agents may be transferred with the translocated fish, thus leading to outbreaks of diseases (Whittington & Chong, 2007Whittington RJ, Chong R. Global trade in ornamental fish from an Australian perspective: the case for revised import risk analysis and management strategies. Prev Vet Med 2007; 81(1-3): 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 family Chaetodontidae comprises 131 species of marine fish, which preferentially inhabit the coral reefs of the Pacific Ocean (Tiralongo et al., 2018Tiralongo F, Lipari R, Mancini E. A new exotic fish for the Mediterranean Sea: Chaetodon auriga Forsskål, 1775 (Perciformes: Chaetodontidae). Mediterr Mar Sci 2018; 19(3): 491-493. http://dx.doi.org/10.12681/mms.16929.
http://dx.doi.org/10.12681/mms.16929...
). Known as butterflyfish, these fish species are characterized by their bright colors and, hence, are highly coveted by aquarists around the world (Affonso & Galetti., 2007Affonso PRAM, Galetti PM Jr. Genetic diversity of three ornamental reef fishes (Families Pomacanthidae and Chaetodontidae) from Brazilian coast. Braz J Biol 2007;67(4 Suppl): 925-933. http://dx.doi.org/10.1590/S1519-69842007000500017. PMid:18278361.
http://dx.doi.org/10.1590/S1519-69842007...
).

Rainford's butterflyfish, Chaetodon rainfordi (McCulloch, 1923), is an endemic species from the Western Pacific. Its natural range is limited to the Great Barrier Reef of Australia and coastal areas adjacent to Lord Howe Island. These fish feed on algae and small benthic invertebrates (Froese & Pauly, 2019Froese R, Pauly D. FishBase [online]. 2019 [cited 2019 Aug 1]. Available from: https://www.fishbase.se/summary/12023
https://www.fishbase.se/summary/12023...
) and belong to one of the main ornamental families imported into Brazil and the rest of the world (Gasparini et al., 2005Gasparini JL, Floeter SR, Ferreira CEL, Sazima I. Marine ornamental trade in Brazil. Biodivers Conserv 2005; 14(12): 2883-2899. http://dx.doi.org/10.1007/s10531-004-0222-1.
http://dx.doi.org/10.1007/s10531-004-022...
; Lawton et al., 2013Lawton RJ, Pratchett MS, Delbeek JC. Harvesting of butterflyfishes for aquarium and artisanal fisheries. In: Pratchett MS, Berumen ML, Kapoor BG, editors. Biology of butterflyfishes. 1st ed. Boca Raton: CRC Press; 2013. p. 269-291. http://dx.doi.org/10.1201/b15458-12.
http://dx.doi.org/10.1201/b15458-12...
).

Monogeneans are parasites in the phylum Platyhelminthes that are normally found in fish species and lower invertebrates. Among the 13 families of monogeneans, four are frequently pathogenic to fish: Gyrodactylidae, Dactylogyridae, Ancyrocephalidae and Capsalidae (Reed et al., 2012Reed P, Francis-Floyd R, Klinger R, Petty D. Monogenean parasites of fish [online]. Gainesville: University of Florida; 2012 [cited 2019 Aug 1]. Available from: https://edis.ifas.ufl.edu/fa033
https://edis.ifas.ufl.edu/fa033...
). Species of the genus Haliotrema Johnston and Tiegs 1922; (Monogenea: Ancyrocephalinae) have very interesting host associations and geographic distributions. They are reputed to be highly host-specific and are found exclusively on marine percomorph fish in tropical and subtropical waters, associated with coral reef environments (Klassen, 1994Klassen GJ. Phylogeny of Haliotrema Species (Monogenea: Ancyrocephalidae) from Boxfishes (Tetraodontiformes: Ostraciidae): Are Haliotrema Species from Boxfishes Monophyletic? J Parasitol 1994; 80(4): 596-610. http://dx.doi.org/10.2307/3283198. PMid:8064528.
http://dx.doi.org/10.2307/3283198...
).

The present study report on occurrences of exotic Haliotrema aurigae in diseased Rainford's butterflyfish (C. rainfordi) that were imported. These parasites may have been introduced together with their hosts into Brazil. The importance of implementation of correct control measures at the country’s borders, in order to avoid the introduction of exotic parasites, is emphasized.

Six Rainford’s butterflyfish (C. rainfordi) were imported from Australia on November 22, 2018. These fish were quarantined for 8 days; they showed no clinical signs of infection and were then released for commercialization.

They were transferred into a water recirculation system with a usable volume of 5.000 L, in which they joined other fish belonging to the company that imported them. These fish were fed three times a day with commercial feed (Tetra® marine flakes and granules, Germany) until they stopped eating, i.e. until they reached satiety. The water quality parameters were measured daily and were maintained as follows: temperature, 26 °C; salinity, 29 g L-1; dissolved oxygen, 5 mg L‒1; alkalinity, 160 mg L-1; pH, 8.2; and total ammonia concentration, < 0.1 mg L‒1.

These butterflyfish specimens were then released into a reef aquarium without displaying any clinical signs. However, six days after the release, a veterinary technician working for the retailer observed that one of them exhibited behavioral changes such as flashing, darkening (Figure 1), prostration and low mobility. This fish was dying, and infection with some form of parasitic disease was suspected. It was anesthetized with eugenol (75 mg L-1) (Roubach et al., 2005Roubach R, Gomes LC, Leão Fonseca FA, Val AL. Eugenol as an efficacious anaesthetic for tambaqui, Colossoma macropomum (Cuvier). Aquacult Res 2005; 36(11): 1056-1061. http://dx.doi.org/10.1111/j.1365-2109.2005.01319.x.
http://dx.doi.org/10.1111/j.1365-2109.20...
) and euthanized by sectioning the spine (Noga, 2010Noga EJ. Fish disease: diagnosis and treatment. 2nd ed. Iowa: Willey-Blackwell; 2010. http://dx.doi.org/10.1002/9781118786758.
http://dx.doi.org/10.1002/9781118786758...
), and was then subjected to skin and gill scraping.

Figure 1
Rainford's butterflyfish (Chaetodon rainfordi) parasitized by Haliotrema aurigae.

The gills were removed from the fish specimen and monogenean parasites were collected manually using sterilized forceps. The parasite specimens were then mounted on semi-permanent slides with Hoyer’s solution for morphological analysis of sclerotized structures (Kritsky et al., 1995Kritsky DC, Boeger WA, Popazoglo F. Neotropical Monogenoidea. 22: variation in Scleroductus species (Gyrodactylidea, Gyrodactylidae) from siluriform fishes of southeastern Brazil. J Helminthol Soc Wash 1995; 62(1): 53-56.). Photomicrographs were obtained using a differential interference contrast (DIC) microscope (Zeiss Axio Imager A2). The morphology and the hard-sclerotized structures of the specimens were compared with the descriptions given by Plaisance et al. (2004)Plaisance L, Bouamer S, Morand S. Description and redescription of Haliotrema species (Monogenoidea: Poloyonchoinea: Dactylogyridae) parazitising butterflyfishes (Teleostei: Chaetodontidae) in the Indo-West Pacific Ocean. Parasitol Res 2004; 93(1): 598-604. http://dx.doi.org/10.1007/s00436-004-1094-8. PMid:15103553.
http://dx.doi.org/10.1007/s00436-004-109...
.

The specimens of monogeneans that were collected from the gills (Figure 2A) of this specimen of Rainford's butterflyfish (C. rainfordi) were identified as Haliotrema aurigae (Yamaguti, 1968). A male copulatory complex was the determinant structure in this differentiation; characterized by a trapezoidal base and an elongated accessory structure, with apparent filaments at its posterior extremity (Figure 2B). In addition, in the haptor, a transverse marking on the appendix, in the medial portion of the dorsal anchor, was observed (Figure 2C). Both of these characteristics were concordant with the description provided by Plaisance et al. (2004)Plaisance L, Bouamer S, Morand S. Description and redescription of Haliotrema species (Monogenoidea: Poloyonchoinea: Dactylogyridae) parazitising butterflyfishes (Teleostei: Chaetodontidae) in the Indo-West Pacific Ocean. Parasitol Res 2004; 93(1): 598-604. http://dx.doi.org/10.1007/s00436-004-1094-8. PMid:15103553.
http://dx.doi.org/10.1007/s00436-004-109...
.

Figure 2
Photomicrographs of Haliotrema aurigae collected from Chaetodon rainfordi imported from Australia: (A) scale bar = 5 µm; (B) male copulatory organ (scale bar = 2 µm); (C) haptor (scale bar = 5 µm).

Previously described in the genus Pseudohaliotrema, the species was considered by Plaisance et al. (2004)Plaisance L, Bouamer S, Morand S. Description and redescription of Haliotrema species (Monogenoidea: Poloyonchoinea: Dactylogyridae) parazitising butterflyfishes (Teleostei: Chaetodontidae) in the Indo-West Pacific Ocean. Parasitol Res 2004; 93(1): 598-604. http://dx.doi.org/10.1007/s00436-004-1094-8. PMid:15103553.
http://dx.doi.org/10.1007/s00436-004-109...
as belonging to Haliotrema. In our study, we observed important characteristics relating to the sclerotized structures of monogenean parasites of Rainford's butterflyfish, which had not been collected in Brazil until now. Furthermore, these parasites were assigned to the genus Haliotrema Johnston and Tiegs, 1922. The specimens presented a straight or slightly curved penis, a trapezoidal base to the male copulatory complex and a simple filamentary accessory piece, among other morphological specifications.

Until now, the distribution of H. aurigae had been reported to be limited to the southern Pacific Ocean, on the outskirts of islands with coral reefs, preferentially parasitizing the family Chaetodontidae (Mizelle & Kritsky, 1969Mizelle JD, Kritsky DC. Studies on monogenetic trematodes. XL. New species from marine and freshwater fishes. Am Midl Nat 1969; 82(2): 417-428. http://dx.doi.org/10.2307/2423787.
http://dx.doi.org/10.2307/2423787...
; Plaisance & Kritsky, 2004Plaisance L, Kritsky DC. Dactylogyrids (Platyhelminthes: Monogenoidea) parasitizing butterfly fishes (Teleostei: Chaetodontidae) from the coral reefs of Palau, Moorea, Wallis, New Caledonia and Australia: species of Euryhaliotrematoides n. gen. and Aliatrema n, gen. J Parasitol 2004; 90(2): 328-341. http://dx.doi.org/10.1645/GE-3257. PMid:15165056.
http://dx.doi.org/10.1645/GE-3257...
; Plaisance et al., 2004Plaisance L, Bouamer S, Morand S. Description and redescription of Haliotrema species (Monogenoidea: Poloyonchoinea: Dactylogyridae) parazitising butterflyfishes (Teleostei: Chaetodontidae) in the Indo-West Pacific Ocean. Parasitol Res 2004; 93(1): 598-604. http://dx.doi.org/10.1007/s00436-004-1094-8. PMid:15103553.
http://dx.doi.org/10.1007/s00436-004-109...
). There are 131 recognized species of Haliotrema, and H. aurigae had previously been reported in Rainford's butterflyfish only once, by Reverter et al. (2016)Reverter M, Cutmore SC, Bray R, Cribb TH, Sasal P. Gill monogenean communities (Platyhelminthes, Monogenea, Dactylogyridae) of butterflyfishes from tropical Indo-West Pacific Islands. Parasitology 2016; 143(12): 1580-1591. http://dx.doi.org/10.1017/S0031182016001463. PMid:27573880.
http://dx.doi.org/10.1017/S0031182016001...
on the Indo-Pacific coast. The occurrence in Brazil in the present study is reported. These findings provide important information that can be used by aquarists in treating this parasitic infection of ornamental fish under confined conditions.

Parasite control measures are not implemented by importers after the fish have crossed the Brazilian border because of the lack of epidemiological data on fish diseases and asymptomatic carriers. This increases the risk of diseases in native fish and subsequent economic loss. There is a need for importers of ornamental fish to implement biosecurity measures at their facilities to prevent the introduction and dissemination of diseases caused by parasites such as monogenean worms. The quarantine period for fish in Brazil is only seven days (Brasil, 2019Brasil. Ministério da Agricultura Pecuária e Abastecimento. Sistema de Consulta à Legislação (SISLEGIS), versão 1.0 [online]. Brasília; 2019 [cited 2020 Sept 1]. Available from: http://sistemasweb.agricultura.gov.br/sislegis/action/detalhaAto.do?method=gravarAtoPDF&tipo=INM&numeroAto=00000004&seqAto=000&valorAno=2019&orgao=GM/MAPA&codTipo=&desItem=&desItemFim=
http://sistemasweb.agricultura.gov.br/si...
), which is not sufficient in most cases to detect or eliminate etiological agent(s) (Whittington & Chong, 2007Whittington RJ, Chong R. Global trade in ornamental fish from an Australian perspective: the case for revised import risk analysis and management strategies. Prev Vet Med 2007; 81(1-3): 92-116. http://dx.doi.org/10.1016/j.prevetmed.2007.04.007. PMid:17485126.
http://dx.doi.org/10.1016/j.prevetmed.20...
).

Considering the losses caused by monogeneans in fish and the transborder potential of Haliotrema sp., it is necessary not only to optimize management practices but also to implement biosecurity measures that enable rapid and accurate diagnosis. This will help minimize the risk of economic losses and introduction of new diseases in this country. In this report, we detected gill infestation by monogeneans in the ornamental reef fish, Rainford’s butterflyfish. This finding emphasizes the importance of implementation of correct control measures by importers at the country’s border, in order to avoid the introduction of exotic parasite species into this country. It is important to emphasize that parasites that have specific host associations and geographic distributions were able to survive in the new aquarium without a coral reef environment in Brazil.

Acknowledgements

We thank the National Council for Scientific and Technological Development (CNPq) for the research grant for M.L. Martins (CNPq # 306635/2018-6); for the sabbatical fellowship for P.H.M. Cardoso (CAPES 1808006); and William E. Furtado (AQUOS, UFSC) for the parasite photos. This study was funded in part by the Coordination Office for Improvement of Higher-Education Personnel (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, CAPES), under finance code 001.

  • How to cite: Cardoso PHM, Balian SC, Soares HS, Furtado W, Martins ML. Haliotrema aurigae (Yamaguti, 1968) Plaisance, Bouamer & Morand, 2004, in ornamental reef fish imported into Brazil. Braz J Vet Parasitol 2020; 29(3): e001620. https://doi.org/10.1590/S1984-29612020033

References

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    » http://dx.doi.org/10.1590/S1519-69842007000500017
  • Brasil. Ministério da Agricultura Pecuária e Abastecimento. Sistema de Consulta à Legislação (SISLEGIS), versão 1.0 [online]. Brasília; 2019 [cited 2020 Sept 1]. Available from: http://sistemasweb.agricultura.gov.br/sislegis/action/detalhaAto.do?method=gravarAtoPDF&tipo=INM&numeroAto=00000004&seqAto=000&valorAno=2019&orgao=GM/MAPA&codTipo=&desItem=&desItemFim=
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    » https://www.bassleer.com/ornamentalfishexporters/wp-content/uploads/sites/3/2016/12/GLOBAL-TRADE-IN-ORNAMENTAL-FISH.pdf
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    » http://dx.doi.org/10.1007/s10531-004-0222-1
  • Klassen GJ. Phylogeny of Haliotrema Species (Monogenea: Ancyrocephalidae) from Boxfishes (Tetraodontiformes: Ostraciidae): Are Haliotrema Species from Boxfishes Monophyletic? J Parasitol 1994; 80(4): 596-610. http://dx.doi.org/10.2307/3283198 PMid:8064528.
    » http://dx.doi.org/10.2307/3283198
  • Kritsky DC, Boeger WA, Popazoglo F. Neotropical Monogenoidea. 22: variation in Scleroductus species (Gyrodactylidea, Gyrodactylidae) from siluriform fishes of southeastern Brazil. J Helminthol Soc Wash 1995; 62(1): 53-56.
  • Lawton RJ, Pratchett MS, Delbeek JC. Harvesting of butterflyfishes for aquarium and artisanal fisheries. In: Pratchett MS, Berumen ML, Kapoor BG, editors. Biology of butterflyfishes 1st ed. Boca Raton: CRC Press; 2013. p. 269-291. http://dx.doi.org/10.1201/b15458-12
    » http://dx.doi.org/10.1201/b15458-12
  • Lymbery AJ, Morine M, Kanani HG, Beatty SJ, Morgan DL. Co-invaders: the effects of alien parasites on native hosts. Int J Parasitol Parasites Wildl 2014; 3(2): 171-177. http://dx.doi.org/10.1016/j.ijppaw.2014.04.002 PMid:25180161.
    » http://dx.doi.org/10.1016/j.ijppaw.2014.04.002
  • Mizelle JD, Kritsky DC. Studies on monogenetic trematodes. XL. New species from marine and freshwater fishes. Am Midl Nat 1969; 82(2): 417-428. http://dx.doi.org/10.2307/2423787
    » http://dx.doi.org/10.2307/2423787
  • Noga EJ. Fish disease: diagnosis and treatment 2nd ed. Iowa: Willey-Blackwell; 2010. http://dx.doi.org/10.1002/9781118786758
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  • Plaisance L, Bouamer S, Morand S. Description and redescription of Haliotrema species (Monogenoidea: Poloyonchoinea: Dactylogyridae) parazitising butterflyfishes (Teleostei: Chaetodontidae) in the Indo-West Pacific Ocean. Parasitol Res 2004; 93(1): 598-604. http://dx.doi.org/10.1007/s00436-004-1094-8 PMid:15103553.
    » http://dx.doi.org/10.1007/s00436-004-1094-8
  • Plaisance L, Kritsky DC. Dactylogyrids (Platyhelminthes: Monogenoidea) parasitizing butterfly fishes (Teleostei: Chaetodontidae) from the coral reefs of Palau, Moorea, Wallis, New Caledonia and Australia: species of Euryhaliotrematoides n. gen. and Aliatrema n, gen. J Parasitol 2004; 90(2): 328-341. http://dx.doi.org/10.1645/GE-3257 PMid:15165056.
    » http://dx.doi.org/10.1645/GE-3257
  • Reed P, Francis-Floyd R, Klinger R, Petty D. Monogenean parasites of fish [online]. Gainesville: University of Florida; 2012 [cited 2019 Aug 1]. Available from: https://edis.ifas.ufl.edu/fa033
    » https://edis.ifas.ufl.edu/fa033
  • Reverter M, Cutmore SC, Bray R, Cribb TH, Sasal P. Gill monogenean communities (Platyhelminthes, Monogenea, Dactylogyridae) of butterflyfishes from tropical Indo-West Pacific Islands. Parasitology 2016; 143(12): 1580-1591. http://dx.doi.org/10.1017/S0031182016001463 PMid:27573880.
    » http://dx.doi.org/10.1017/S0031182016001463
  • Roubach R, Gomes LC, Leão Fonseca FA, Val AL. Eugenol as an efficacious anaesthetic for tambaqui, Colossoma macropomum (Cuvier). Aquacult Res 2005; 36(11): 1056-1061. http://dx.doi.org/10.1111/j.1365-2109.2005.01319.x
    » http://dx.doi.org/10.1111/j.1365-2109.2005.01319.x
  • Tiralongo F, Lipari R, Mancini E. A new exotic fish for the Mediterranean Sea: Chaetodon auriga Forsskål, 1775 (Perciformes: Chaetodontidae). Mediterr Mar Sci 2018; 19(3): 491-493. http://dx.doi.org/10.12681/mms.16929
    » http://dx.doi.org/10.12681/mms.16929
  • Whittington RJ, Chong R. Global trade in ornamental fish from an Australian perspective: the case for revised import risk analysis and management strategies. Prev Vet Med 2007; 81(1-3): 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

Publication Dates

  • Publication in this collection
    06 July 2020
  • Date of issue
    2020

History

  • Received
    28 Jan 2020
  • Accepted
    22 Apr 2020
Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
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