Pupipara (Diptera, Hippoboscidae) in wild birds attended at a rehabilitation center in southern Brazil

Pupíparas (Diptera, Hippoboscidae) em Aves Silvestres Atendidas em Centro de Reabilitação no Sul do Brasil

Renata Fagundes Moreira Laura de Campos Farezin Ugo Araújo Souza Bruna Zafalon da Silva Derek Blaese Amorim Aline Girotto-Soares Lívia Eichenberg Surita Marcelo Meller Alievi Gustavo Graciolli João Fabio Soares About the authors

Abstract

The hippoboscids are cosmopolitan permanent obligate hematophagous ectoparasites of birds, domestic and wild mammals and, occasionally, humans. Some species may act as vectors or hosts of etiological pathogenic agents. The aims of this study were to report on the first cases of Hippoboscidae in Crax blumenbachii and Parabuteo unicinctus; to provide new reports from Brazil on Tyto furcata and Asio stygius parasitized by Icosta americana; to report on individuals of Bubo virginianus, Falco sparverius and Accipiter striatus parasitized by genera Ornithoctona; and to provide new reports on parasitism of O. erythrocephala in the state of Rio Grande do Sul. The birds of prey and C. blumenbachii were attended at a rehabilitation center in Porto Alegre and at a veterinary hospital in Cruz Alta. These new records demonstrate the huge gap that exists regarding studies on avian ectoparasites and highlight potential vectors of hemoparasites for the bird species studied.

Keywords:
Hematophagous ectoparasites; flies; birds of prey; cracids; hippoboscidae; Southern Brazil

Resumo

Os hipoboboscídeos são ectoparasitos hematófagos obrigatórios, permanentes e cosmopolitas de aves, mamíferos domésticos e silvestres e, ocasionalmente, humanos. Algumas espécies podem atuar como vetores ou hospedeiros de agentes patogênicos etiológicos. Os objetivos deste estudo foram relatar os primeiros casos de Hippoboscidae em Crax blumenbachii e Parabuteo unicinctus; fornecer novo relato do Brasil sobre Tyto furcata e Asio stygius parasitados por Icosta americana; relatar indivíduos de Bubo virginianus, Falco sparverius e Accipiter striatus parasitados pelo gênero Ornithoctona; e fornecer novos relatos sobre parasitismo de O. erythrocephala no estado do Rio Grande do Sul. As aves de rapina e C. blumenbachii foram atendidas em um centro de reabilitação em Porto Alegre e em um hospital veterinário em Cruz Alta. Esses novos registros demonstram a enorme lacuna que existe em relação aos estudos sobre ectoparasitas aviários e destacam potenciais vetores de hemoparasitos para as espécies de aves estudadas.

Palavras-chave:
Ectoparasitos hematófagos; moscas; aves de rapina; cracídeos; hippoboscidae; Sul do Brasil

Introduction

Hippoboscid flies are cosmopolitan permanent obligate hematophagous ectoparasites of birds, domestic and wild mammals and, occasionally, humans (RODHAIN, 2015Rodhain F. Insects as vectors: systematics and biology. Rev Sci Tech 2015; 34(1): 83-96, 67-82. PMid:26470450.). The females of these flies do not lay eggs, but grow larvae internally; when fully developed, the larvae are released and pupated immediately (HUTSON, 1971Hutson AM. New species of the Ornithomya biloba-group and records of other Hippoboscidae (Diptera) from Africa. Syst Entomol 1971; 40(2): 139-148.). Some species may act as vectors or hosts of etiological agents such as bacteria, helminths and protozoa. Among these, Pseudolynchia canariensis is frequently found in pigeons, causing damage to these birds, and is the only known vector of Haemoproteus columbae (SERRA-FREIRE & MELLO, 2006Serra-Freire NM, Mello RP. Entomologia & acarologia na medicina veterinária. Rio de Janeiro: LF Livros; 2006.; RAHOLA et al., 2011Rahola N, Goodman SM, Robert V. The Hippoboscidae (Insecta: Diptera) from Madagascar, with new records from the “Parc National de Midongy Befotaka”. Parasite 2011; 18(2): 127-140. http://dx.doi.org/10.1051/parasite/2011182127. PMid:21678788.
http://dx.doi.org/10.1051/parasite/20111...
; RODHAIN, 2015Rodhain F. Insects as vectors: systematics and biology. Rev Sci Tech 2015; 34(1): 83-96, 67-82. PMid:26470450.).

Farajollahi et al. (2005)Farajollahi A, Crans WJ, Nickerson D, Bryant P, Wolf B, Glaser A, et al. Detection of West Nile virus RNA from the louse fly Icosta americana (Diptera: Hippoboscidae). J Am Mosq Control Assoc 2005; 21(4): 474-476. http://dx.doi.org/10.2987/8756-971X(2006)21[474:DOWNVR]2.0.CO;2. PMid:16506578.
http://dx.doi.org/10.2987/8756-971X(2006...
detected RNA of the West Nile virus in specimens of Icosta americana that were parasitizing birds of prey. The Rickettsia raoultii has been detected molecularly in Melophagus ovinus (LIU et al., 2016Liu D, Wang YZ, Zhang H, Liu ZQ, Wureli HZ, Wang SW, et al. First report of Rickettsia raoultii and R. slovaca in Melophagus ovinus, the sheep ked. Parasit Vectors 2016; 9(600): 1-6. http://dx.doi.org/10.1186/s13071-016-1885-7. PMid:27884170.
http://dx.doi.org/10.1186/s13071-016-188...
), although Rickettsiae do not have any significant impact on birds.

Parabuteo unicinctus, Falco sparverius, Bubo virginianus, Tyto furcata, Asio stygius, Rupornis magnirostris, Caracara plancus and Accipiter striatus are predatory birds with strong presence in Latin America. They balance biodiversity by controlling the populations of rodents, lizards, snakes and bats. Crax blumenbachii is endemic to the Atlantic Forest of southeastern Brazil, but destruction of the biome and hunting have led to significant decline in this species, which is now endangered (STRAHL et al., 1995Strahl S, Ellis S, Byers O, Plasse C, Crax S. Conservation assessment and management plan for neotropical guans, curassows and chachalacas. Houston: CBSG; 1995.; BIRDLIFE INTERNATIONAL, 2016BirdLife International. The IUCN Red List of Threatened Species: Species factsheet: Crax blumenbachii [online]. Cambridge: BirdLife International; 2016 [cited 2018 jul 18]. Available from: http://www.birdlife.org.
http://www.birdlife.org...
).

The aims of this study were to report on the first cases of Hippoboscidae in C. blumenbachii and P. unicinctus; to provide new reports from Brazil on T. furcata and A. stygius parasitized by I. americana; to report on individuals of B. virginianus, F. sparverius and A. striatus parasitized by genera Ornithoctona; and to provide new reports on the distribution and parasitism of O. erythrocephala in the state of Rio Grande do Sul.

Material and Methods

The birds evaluated here were received for veterinary medical care at the Conservation and Rehabilitation Center for Wild Animals (PRESERVAS) of the Federal University of Rio Grande do Sul (UFRGS), in Porto Alegre, except for a specimen of T. furcata, which was attended at the Veterinary Hospital of Cruz Alta, between August 2015 and August 2018. Any ectoparasites that were observed on these birds were removed from them, preserved in 70% ethanol and sent for identification. The parasites were identified using the keys published by Hutson (1984)Hutson AM. Diptera: Keds, flat-flies and bat-flies (Hippoboscidae and Nycteribiidae). Londres: Royal Entomological Society; 1984. (Handbooks for the identification of British insects; vol. 10). and Graciolli & Carvalho (2003)Graciolli G, Carvalho CJB. Hippoboscidae (Diptera, Hippoboscoidea) no Estado do Paraná, Brasil: chaves de identificação, hospedeiros e distribuição geográfica. Rev Bras Zool 2003; 20(4): 667-674. http://dx.doi.org/10.1590/S0101-81752003000400019.
http://dx.doi.org/10.1590/S0101-81752003...
, and species were photographed as exemplified in Figure 1.

Figure 1
Specimens identified of Hippoboscidae. A = Icosta Americana; B = Ornithoctona erythrocephala.

Results

In total, 12 species of Hippoboscidae were identified on nine birds. These birds were all free-living, with the exception of one individual of C. blumenbachii, which was kept in captivity. The results, places of origin and living conditions (free-living or in captivity) of these birds are presented in Table 1.

Table 1
Places of origin of the hosts and numbers of flies found.

Discussion

From a bibliographical survey that we conducted, this is the first report of parasitism by Hippoboscidae in C. blumenbachii and P. unicinctus. These birds were parasitized by O. erythrocephala. In cracids, Vaz & Teixeira (2016)Vaz FF, Teixeira VN. New records of three hippoboscid species on newly captured birds from nature in Paraná, Brazil. Rev Bras Parasitol Vet 2016; 25(4): 501-503. http://dx.doi.org/10.1590/s1984-29612016056. PMid:27737369.
http://dx.doi.org/10.1590/s1984-29612016...
observed O. erythrocephala parasitizing Penelope obscura in the state of Paraná, Brazil. Also in Brazil, the genus Ornithoctona was found in birds of prey in the states of Mato Grosso, São Paulo, Paraná, Santa Catarina and Rio Grande do Sul. Two females of O. erythrocephala were observed parasitizing Milvago chimango in the southern part of Rio Grande do Sul (LAMBRECHT et al., 2015Lambrecht FM, Serra-Freire NM, Farias NAR. Milvago chimango (Vieillot, 1816) (Aves: Falconidae) novo hospedeiro para Ornithoctona erythrocephala (Leach, 1817) (Diptera: Hippoboscidae) no município do Rio Grande, Rio Grande do Sul, Brasil. Rev Uniabeu 2015; 8(18): 257-261.).

Gregor et al. (1973)Gregor F, Černý V, De La Cruz J. On the avian Hippoboscidae (Diptera) of Cuba. Folia Parasitol (Praha) 1973; 20(2): 183-187. PMid:4770811. found that F. sparverius was parasitized by O. erythrocephala in Cuba and cited a report by Maa (1969)Maa TC. A revised checklist and concise host index of Hippoboscidae (Diptera). Pac Insects Monog 1969; 20: 261-299., who had found that it was parasitized by Ornithoctona sp., Ornithoica sp., Ornithophila metallica, Ornithophila gestroi, Ornithomya sp. and Phthona modesta. However, the present study is the first report from Brazil.

Vaz & Teixeira (2016)Vaz FF, Teixeira VN. New records of three hippoboscid species on newly captured birds from nature in Paraná, Brazil. Rev Bras Parasitol Vet 2016; 25(4): 501-503. http://dx.doi.org/10.1590/s1984-29612016056. PMid:27737369.
http://dx.doi.org/10.1590/s1984-29612016...
observed O. erythrocephala parasitizing newly captured free-living individuals of the species R. magnirostris and C. plancus in Paraná. However, the present study provides a new record of this parasitism in Rio Grande do Sul. Mueller et al. (1969)Mueller NS, Mueller HC, Berger DD. Host records and phenology of louse-flies on Wisconsin birds. Wisconsin Academy of Sciences. Arts and Letters 1969; 57: 189-207. reported O. erythrocephala in B. virginianus and A. striatus in Wisconsin, USA. The genus Ornithoctona in B. virginianus and A. striatus was observed in the present study for the first time in Brazil.

Icosta is the largest genus of the family Hipposcidae, with about 65 species (KEIRANS, 1975Keirans JE. A review of the phoretic relationship between Mallophaga (Phthiraptera: Insecta) and Hippoboscidae (Diptera: Insecta). J Med Entomol 1975; 12(1): 71-76. http://dx.doi.org/10.1093/jmedent/12.1.71. PMid:1099206.
http://dx.doi.org/10.1093/jmedent/12.1.7...
). It has already been discovered in Paraná and Santa Catarina. I. americana and I. rufiventris have been reported from the owls Megascops atricapilla, M. sanctaecatarinae, M. choliba, Athene cunicularia, Ciccaba virgata, Otus choliba and Strix hylophila in Brazil (GRACIOLLI & CARVALHO, 2003Graciolli G, Carvalho CJB. Hippoboscidae (Diptera, Hippoboscoidea) no Estado do Paraná, Brasil: chaves de identificação, hospedeiros e distribuição geográfica. Rev Bras Zool 2003; 20(4): 667-674. http://dx.doi.org/10.1590/S0101-81752003000400019.
http://dx.doi.org/10.1590/S0101-81752003...
; GRACIOLLI & BISPO, 2005Graciolli G, Bispo AA. Hippoboscidae (Diptera) ectoparasitos sobre seis espécies de corujas (Strigiformes) no estado do Paraná, Sul do Brasil. Rev Bras Ornitol 2005; 13(2): 181-182.). The I. rufiventris and Ornithoica vicina complete their life cycle in owls (MAA, 1969Maa TC. A revised checklist and concise host index of Hippoboscidae (Diptera). Pac Insects Monog 1969; 20: 261-299.). The present study provides the first records of Icosta americana in T. furcata and A. stygius in Brazil.

Thus, this is the first report of parasitism by Hippoboscidae in C. blumenbachii and P. unicinctus. This report also describes new occurrences of the genera Ornithoctona and Icosta parasitizing birds of prey in Rio Grande do Sul and some other parts of Brazil.

Knowledge of the ectoparasite fauna in wild birds is of paramount importance, especially among birds threatened with extinction, because these pupipara have vector potential. In these birds, hemoparasites may be harmful to the population balance and may be especially pathogenic towards birds that are under stress through captivity.

Acknowledgements

This work was supported by the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq) and by the Coordination Office for Improvement of Higher-Education Personnel (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, CAPES).

References

  • BirdLife International. The IUCN Red List of Threatened Species: Species factsheet: Crax blumenbachii [online]. Cambridge: BirdLife International; 2016 [cited 2018 jul 18]. Available from: http://www.birdlife.org
    » http://www.birdlife.org
  • Farajollahi A, Crans WJ, Nickerson D, Bryant P, Wolf B, Glaser A, et al. Detection of West Nile virus RNA from the louse fly Icosta americana (Diptera: Hippoboscidae). J Am Mosq Control Assoc 2005; 21(4): 474-476. http://dx.doi.org/10.2987/8756-971X(2006)21[474:DOWNVR]2.0.CO;2 PMid:16506578.
    » http://dx.doi.org/10.2987/8756-971X(2006)21[474:DOWNVR]2.0.CO;2
  • Graciolli G, Bispo AA. Hippoboscidae (Diptera) ectoparasitos sobre seis espécies de corujas (Strigiformes) no estado do Paraná, Sul do Brasil. Rev Bras Ornitol 2005; 13(2): 181-182.
  • Graciolli G, Carvalho CJB. Hippoboscidae (Diptera, Hippoboscoidea) no Estado do Paraná, Brasil: chaves de identificação, hospedeiros e distribuição geográfica. Rev Bras Zool 2003; 20(4): 667-674. http://dx.doi.org/10.1590/S0101-81752003000400019
    » http://dx.doi.org/10.1590/S0101-81752003000400019
  • Gregor F, Černý V, De La Cruz J. On the avian Hippoboscidae (Diptera) of Cuba. Folia Parasitol (Praha) 1973; 20(2): 183-187. PMid:4770811.
  • Hutson AM. Diptera: Keds, flat-flies and bat-flies (Hippoboscidae and Nycteribiidae). Londres: Royal Entomological Society; 1984. (Handbooks for the identification of British insects; vol. 10).
  • Hutson AM. New species of the Ornithomya biloba-group and records of other Hippoboscidae (Diptera) from Africa. Syst Entomol 1971; 40(2): 139-148.
  • Keirans JE. A review of the phoretic relationship between Mallophaga (Phthiraptera: Insecta) and Hippoboscidae (Diptera: Insecta). J Med Entomol 1975; 12(1): 71-76. http://dx.doi.org/10.1093/jmedent/12.1.71 PMid:1099206.
    » http://dx.doi.org/10.1093/jmedent/12.1.71
  • Lambrecht FM, Serra-Freire NM, Farias NAR. Milvago chimango (Vieillot, 1816) (Aves: Falconidae) novo hospedeiro para Ornithoctona erythrocephala (Leach, 1817) (Diptera: Hippoboscidae) no município do Rio Grande, Rio Grande do Sul, Brasil. Rev Uniabeu 2015; 8(18): 257-261.
  • Liu D, Wang YZ, Zhang H, Liu ZQ, Wureli HZ, Wang SW, et al. First report of Rickettsia raoultii and R. slovaca in Melophagus ovinus, the sheep ked. Parasit Vectors 2016; 9(600): 1-6. http://dx.doi.org/10.1186/s13071-016-1885-7 PMid:27884170.
    » http://dx.doi.org/10.1186/s13071-016-1885-7
  • Maa TC. A revised checklist and concise host index of Hippoboscidae (Diptera). Pac Insects Monog 1969; 20: 261-299.
  • Mueller NS, Mueller HC, Berger DD. Host records and phenology of louse-flies on Wisconsin birds. Wisconsin Academy of Sciences. Arts and Letters 1969; 57: 189-207.
  • Rahola N, Goodman SM, Robert V. The Hippoboscidae (Insecta: Diptera) from Madagascar, with new records from the “Parc National de Midongy Befotaka”. Parasite 2011; 18(2): 127-140. http://dx.doi.org/10.1051/parasite/2011182127 PMid:21678788.
    » http://dx.doi.org/10.1051/parasite/2011182127
  • Rodhain F. Insects as vectors: systematics and biology. Rev Sci Tech 2015; 34(1): 83-96, 67-82. PMid:26470450.
  • Serra-Freire NM, Mello RP. Entomologia & acarologia na medicina veterinária Rio de Janeiro: LF Livros; 2006.
  • Strahl S, Ellis S, Byers O, Plasse C, Crax S. Conservation assessment and management plan for neotropical guans, curassows and chachalacas. Houston: CBSG; 1995.
  • Vaz FF, Teixeira VN. New records of three hippoboscid species on newly captured birds from nature in Paraná, Brazil. Rev Bras Parasitol Vet 2016; 25(4): 501-503. http://dx.doi.org/10.1590/s1984-29612016056 PMid:27737369.
    » http://dx.doi.org/10.1590/s1984-29612016056

Publication Dates

  • Publication in this collection
    30 May 2019
  • Date of issue
    Apr-Jun 2019

History

  • Received
    03 Oct 2018
  • Accepted
    18 Jan 2019
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