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Hippoboscid flies in wild birds rescued at the Sorocaba Zoo, São Paulo, Brazil

[Dípteros hipoboscídeos em aves selvagens resgatadas pelo Zoológico de Sorocaba, São Paulo, Brasil]

RESUMO

Os dípteros hipoboscídeos são parasitos de aves e ocasionalmente de alguns mamíferos, encontrados em todos os biomas brasileiros, com aproximadamente 30 espécies, descritas em 10 gêneros. Durante o período de janeiro de 2021 a junho de 2022, foram coletados hipoboscídeos em exames de rotina de aves das famílas Accipitridae, Ardeidae Cathartidae, Columbidae, Falconidae, Ramphastidae e Strigidae, recebidas ou resgatadas pelo Zoológico de Sorocaba. Os parasitos foram encaminhados para diagnóstico taxonômico no Laboratório de Apoio Diagnóstico de Doenças Parasitárias da Universidade Federal Fluminense (UFF), em Niterói, RJ, onde as seguintes espécies foram identificadas: Icosta americana, Ornithoctona eritrocephala, Pseudolynchia canariensis e Stilbometopa podopostyla. Existem poucas informações na literatura sobre a especificidade parasitária, a relação parasito-hospedeiro e a importância desses ectoparasitos em hospedeiros selvagens.

Palavras-chave:
ectoparasito; Diptera; Hippoboscidae; animais selvagens

Keywords:
Ectoparasite; Diptera; Hippoboscidae; wild animals

Palavras-chave:
ectoparasito; Diptera; Hippoboscidae; animais selvagens

Zoos aquarium and wildlife rescue centers are excellent sources for studies on parasites identification and parasite-host interaction due to the great number and diversity of animals received. Sorocaba Zoo receives and rescues approximately 700 wild animals per year, mainly birds (62%), from Sorocaba Metropolitan Region, which covers 27 municipalities, reaching a total area of 11,611.34km2, that has an intense anthropogenic pressure on environment.

Commonly, many animals arrive in poor health conditions and after proper treatment and quarantine period are released in nature. Although recommended by veterinarians and health authorities, the quarantine period is eventually neglected by some wildlife-maintaining institutions. This procedure must be respected to avoid parasite and other diseases transmission (Fraga et al., 2011FRAGA, M.E.; SILVA MEDEIROS, M.E.; NEVES, D.M. Estudo de Aspergilli durante o período de quarentena de psitacídeos do Centro de Triagem de Animais Silvestres IBAMA, Seropédica, RJ. Braz. J. Vet. Med., v.33, p.68-72, 2011.).

Hippoboscids flies are parasites usually associated with birds of prey (Accipitriformes, Cathartiformes, Falconiformes and Strigiformes) and pigeons (Columbiformes). Although less frequent, in Brazil hippoboscids were also collected on Passeriformes, Piciformes and Galliformes (Moreira et al., 2019MOREIRA, R.F.; FAREZIN, L.D.C.; SOUZA, U.A. et al. Pupipara (Diptera, Hippoboscidae) in wild birds attended at a rehabilitation center in southern Brazil. Rev. Bras. Parasitol. Vet., v.28, p.330-332, 2019., Vélez et al., 2020VÉLEZ, A.; FALCON, J.M.; GUERRA, P.; PADRÓN, P.S. Primer reporte del ectoparásito Ornithoctona erythrocephala (Leach) (Diptera: Hippoboscidae) en Elaenia albiceps (Orbigny y Lafresnaye) (Passeriformes: Tyrannidae), en el sur del Ecuador. Rev. Chil. Entomol., v.46, p.545-552, 2020.; Gomes et al., 2021GOMES, L.R.P.; FRATONI, R.D.O.; DE LA TORRE, G.M. et al. Stilbometopa podopostyla (Speiser) (Diptera: Hippoboscidae): first larva description, new record in Paraná state (Brazil) and new host record. Stud. Neotrop. Faun. Environ., v.56, p.78-82, 2021.), corroborating other studies (Murgas et al., 2014MURGAS, A.S.; CHONG, O.G.L.; MILLER, M.J. Hippoboscidae (Insecta: Diptera) ectoparásitos en aves de Panamá, claves de identificación, hospederos y distribución. Scient., v.24, p.49-68, 2014.; Barino et al. 2021BARINO, G.T.M.; DIAS, R.J.P.; GRACIOLLI, G. Hippoboscid flies (Diptera: Hippoboscidae) on birds of prey in the Atlantic Forest, Minas Gerais, Brazil. Rev. Bras. Parasitol. Vet., v.30, p.1- 6, 2021.; Graciolli, Bispo, 2005GRACIOLLI, G.; BISPO, A.A. Hippoboscidae (Diptera) ectoparasitos sobre seis espécies de corujas (Strigiformes) no estado do Paraná, Sul do Brasil. Rev. Bras. Ornitol., v.13, p.181-182, 2005.; Graciolli and Oak, 2003; Liébana et al., 2011LIÉBANA, M.S.; SANTILLÁN, M.A.; CICCHINO, A.C. et al. Ectoparasites In free-ranging american kestrels in Argentina: Implications for the transmission of viral diseases. J. Rap. Res., v.45, p.335-341, 2011.).

The objective of this study was to determine the occurrence and identification of hippoboscid flies in wild avian species. The hippoboscids were collected during triage examination of birds received or rescued at Sorocaba Zoo, São Paulo state, in Brazil.

MATERIAL AND METHODS

From January/2021 to June/2022, 597 birds were received and rescued at Sorocaba Zoo and 2.34% (14/597) had ectoparasites. The avian hosts were identified using external morphological characteristics, according to the Brazilian Committee of Ornithological Records (Pacheco et al., 2021PACHECO, J.P.; SILVEIRA, L.F.; ALEIXO, A. et al. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee - second editions. Ornithology Research, v. 29, p. 94-105, 2021.).

Hippoboscid flies collected during clinical examinations were stored in 70° GL alcohol and sent to the Laboratory of Diagnostic Support in Parasitic Diseases of the Fluminense Federal University (UFF), in labeled vials, informing the scientific and common names of the hosts, place and date of collection. At the laboratory, the fly species identification was made by microscopic analysis of morphological characteristics, using the keys proposed by Graciolli and Carvalho (2003GRACIOLLI, G.; CARVALHO, C.J.B. Hippoboscidae (Diptera, Hippoboscoidea) no Estado do Paraná, Brasil: chaves de identificação, hospedeiros e distribuição geográfica. Rev. Bras. Zool., v.20, p.667-674, 2003.).

RESULTS

The specimens of hippoboscids examined were diagnosed as to the following species: Icosta american, Ornithoctona erythrocephala, Pseudolynchia canariensis and Stilbometopa podopostyla (Fig. 1). The avian host species belonged to the families Accipitridae, Ardeidae, Cathartidae, Columbidae, Falconidae, Ramphastidae and Strigidae. (Table 1).

Figure 1
Adult specimens of hippoboscids flies collected from wild birds at Sorocaba Zoo: a) Icosta american, b) Pseudolynchia canariensis, c) Stilbometopa podopostyla and d) Ornithoctona erythrocephala (bar = 2 mm).

Table 1
Relationship between host bird species and hippoboscids flies collected in clinical examinations at Sorocaba Zoo, from January 2021 to June 2022

DISCUSSION

Members of the family Hippoboscidae are mandatory hematophagous parasites, developing an important role in the transmission of pathogens to their hosts, besides causing anemia due to severe blood spoliation. According to Leite et al. (2013LEITE, Y.F.C.; PINHEIRO, R.T.; BRAGA, E.M. Prevalência de hemosporideos em três localidades do Estado do Tocantins, Brasil. Ornithol. v.6, p.1-13, 2013.), parasitism by hippoboscids can affect the temporal and spatial dynamics of natural populations in avian communities. They can also act as vectors of West Nile fever virus for birds, compromising reproduction, causing immune depression, opportunistic infections, and death (Farajollah et al., 2005; Gancz et al., 2004GANCZ, A.Y.; BARKER, I.K.; LINDSAY, R. et al. West Nile virus outbreak in north American owls, Ontario, 2002. Emerg. Infect. Dis., v.10, p.2135, 2004.).

In Brazil, hippoboscids are often found in Columbiformes, especially in domestic pigeons. In this host species, parasitosis can cause irritation due to hematophagy, beside the possibility of hematozoan transmission, such as Haemoproteus columbae (Gredilha et al., 2008GREDILHA, R.; BALTHAZAR, D.A.; SPADETTI, A.L. et al. Pseudolynchia canariensis (Diptera: Hippoboscidae) em Buteogallus aequinoctialis (Ciconiiformes: Accipitridae) no estado do Rio de Janeiro, Brasil. Rev. Bras. Parasitol. Vet., v.17, p.110-112, 2008.; Marcelino et al., 2009MARCELINO, V.J.F.C.; ARCOVERDE, A.R.; DAEMON, E. Aspectos da associação forética dos ácaros Myialges spp. (Astigmata: Epidermoptidae) e Ornitocheyletia hallae Volgin (Prostigmata: Cheyletidae) com a mosca Pseudolynchia canariensis (Macquart)(Diptera: Hippoboscidae). Neotrop. Entomol., v.38, p.578-581, 2009.). In this study, parasitized birds were not evaluated for the presence of hematozoa.

In agreement with a previous study conducted in 155 birds of prey received in a rescue center in Minas Gerais, Brazil, the parasitism by Ornithoctona erytrocephala and Icosta americana reposted. (Barino et al., 2021BARINO, G.T.M.; DIAS, R.J.P.; GRACIOLLI, G. Hippoboscid flies (Diptera: Hippoboscidae) on birds of prey in the Atlantic Forest, Minas Gerais, Brazil. Rev. Bras. Parasitol. Vet., v.30, p.1- 6, 2021.).

Studies conducted by Vaz and Teixeira (2016) and Moreira et al. (2019MOREIRA, R.F.; FAREZIN, L.D.C.; SOUZA, U.A. et al. Pupipara (Diptera, Hippoboscidae) in wild birds attended at a rehabilitation center in southern Brazil. Rev. Bras. Parasitol. Vet., v.28, p.330-332, 2019.) reported parasitism by Ornithoctona erytrocephala and Icosta americana in avian, occurring in the Brazilian South and Southeast regions, respectively.

Parasitism by Stilbometopa sp. may be common in species of Columbidae. According to Adriano and Cordeiro (2001ADRIANO, E.A.; CORDEIRO, N.S. Prevalência e intensidade de Haemoproteus columbae em três espécies de pombas silvestres do Brasil. Mem Inst Oswaldo Cruz, v.96, p.175-178, 2001.) Stilbometopa sp. can be found in wild doves (Zenaida auriculata) with a prevalence of 13.8% (46/331). In this study, only one specimen of eared dove was examined, positive for this parasitism.

Studies of this nature contribute to the knowledge of the parasitic fauna of wild animals while they allow establishing the areas of occurrence and geographic distribution of ectoparasites.

CONCLUSION

Most of the birds received at the Sorocaba Zoo presented ectoparasites, demonstrating how important it is to search for these organisms during the physical examination and quarantine. This care and identification are very important because these ectoparasites can be responsible for diseases.

Studies on hippoboscids parasitizing wild animals are still scarce in Brazil. The diagnosis and research aiming to the identification of the wild avian host range for hippoboscids may be of help for the determination of risks associated to the parasitic exploitation and hemoparasitism. The knowledge regarding the host occurrence for hippoboscids may help in determining the biosecurity and strategies for prevention. The biology of hippoboscids was not investigated.

REFERENCES

  • ADRIANO, E.A.; CORDEIRO, N.S. Prevalência e intensidade de Haemoproteus columbae em três espécies de pombas silvestres do Brasil. Mem Inst Oswaldo Cruz, v.96, p.175-178, 2001.
  • BARINO, G.T.M.; DIAS, R.J.P.; GRACIOLLI, G. Hippoboscid flies (Diptera: Hippoboscidae) on birds of prey in the Atlantic Forest, Minas Gerais, Brazil. Rev. Bras. Parasitol. Vet., v.30, p.1- 6, 2021.
  • FARAJOLLAHI, A.; CRANS, W.J.; NICKERSON, D. et al. Detection of West Nile Virus RNA from the louse fly Icosta americana (Diptera: Hippoboscidae), J. Am. Mosq. Contr. Assoc., v.21, p.154, 474-476, 2005.
  • FRAGA, M.E.; SILVA MEDEIROS, M.E.; NEVES, D.M. Estudo de Aspergilli durante o período de quarentena de psitacídeos do Centro de Triagem de Animais Silvestres IBAMA, Seropédica, RJ. Braz. J. Vet. Med., v.33, p.68-72, 2011.
  • GANCZ, A.Y.; BARKER, I.K.; LINDSAY, R. et al. West Nile virus outbreak in north American owls, Ontario, 2002. Emerg. Infect. Dis., v.10, p.2135, 2004.
  • GRACIOLLI, G.; BISPO, A.A. Hippoboscidae (Diptera) ectoparasitos sobre seis espécies de corujas (Strigiformes) no estado do Paraná, Sul do Brasil. Rev. Bras. Ornitol., v.13, p.181-182, 2005.
  • GRACIOLLI, G.; CARVALHO, C.J.B. Hippoboscidae (Diptera, Hippoboscoidea) no Estado do Paraná, Brasil: chaves de identificação, hospedeiros e distribuição geográfica. Rev. Bras. Zool., v.20, p.667-674, 2003.
  • GREDILHA, R.; BALTHAZAR, D.A.; SPADETTI, A.L. et al. Pseudolynchia canariensis (Diptera: Hippoboscidae) em Buteogallus aequinoctialis (Ciconiiformes: Accipitridae) no estado do Rio de Janeiro, Brasil. Rev. Bras. Parasitol. Vet., v.17, p.110-112, 2008.
  • GOMES, L.R.P.; FRATONI, R.D.O.; DE LA TORRE, G.M. et al. Stilbometopa podopostyla (Speiser) (Diptera: Hippoboscidae): first larva description, new record in Paraná state (Brazil) and new host record. Stud. Neotrop. Faun. Environ., v.56, p.78-82, 2021.
  • LEITE, Y.F.C.; PINHEIRO, R.T.; BRAGA, E.M. Prevalência de hemosporideos em três localidades do Estado do Tocantins, Brasil. Ornithol. v.6, p.1-13, 2013.
  • LIÉBANA, M.S.; SANTILLÁN, M.A.; CICCHINO, A.C. et al. Ectoparasites In free-ranging american kestrels in Argentina: Implications for the transmission of viral diseases. J. Rap. Res., v.45, p.335-341, 2011.
  • MARCELINO, V.J.F.C.; ARCOVERDE, A.R.; DAEMON, E. Aspectos da associação forética dos ácaros Myialges spp. (Astigmata: Epidermoptidae) e Ornitocheyletia hallae Volgin (Prostigmata: Cheyletidae) com a mosca Pseudolynchia canariensis (Macquart)(Diptera: Hippoboscidae). Neotrop. Entomol., v.38, p.578-581, 2009.
  • MOREIRA, R.F.; FAREZIN, L.D.C.; SOUZA, U.A. et al. Pupipara (Diptera, Hippoboscidae) in wild birds attended at a rehabilitation center in southern Brazil. Rev. Bras. Parasitol. Vet., v.28, p.330-332, 2019.
  • MURGAS, A.S.; CHONG, O.G.L.; MILLER, M.J. Hippoboscidae (Insecta: Diptera) ectoparásitos en aves de Panamá, claves de identificación, hospederos y distribución. Scient., v.24, p.49-68, 2014.
  • PACHECO, J.P.; SILVEIRA, L.F.; ALEIXO, A. et al. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee - second editions. Ornithology Research, v. 29, p. 94-105, 2021.
  • VÉLEZ, A.; FALCON, J.M.; GUERRA, P.; PADRÓN, P.S. Primer reporte del ectoparásito Ornithoctona erythrocephala (Leach) (Diptera: Hippoboscidae) en Elaenia albiceps (Orbigny y Lafresnaye) (Passeriformes: Tyrannidae), en el sur del Ecuador. Rev. Chil. Entomol., v.46, p.545-552, 2020.

Publication Dates

  • Publication in this collection
    13 Nov 2023
  • Date of issue
    Nov-Dec 2023

History

  • Received
    15 Aug 2022
  • Accepted
    06 July 2023
Universidade Federal de Minas Gerais, Escola de Veterinária Caixa Postal 567, 30123-970 Belo Horizonte MG - Brazil, Tel.: (55 31) 3409-2041, Tel.: (55 31) 3409-2042 - Belo Horizonte - MG - Brazil
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