Lacerda, José Dantas Araújo ¹ ; Pacheco, Henri Castro ² ; Souza, Magno Chagas ³ ; Xavier, Nasly Cristianna Gonçalves ⁴ ; da Cruz, Wilton Pires ⁵ and Hernandes, Fabio Akashi ⁶

¹University Campus of Parauapebas, Universidade Federal Rural da Amazônia (UFRA), Via de acesso para a UFRA, Rodovia PA 275, Km 08, Zona Rural, mailbox 3017, zip code 68515-000, Parauapebas City, Pará, Brazil.
²University Campus of Parauapebas, Universidade Federal Rural da Amazônia (UFRA), Via de acesso para a UFRA, Rodovia PA 275, Km 08, Zona Rural, mailbox 3017, zip code 68515-000, Parauapebas City, Pará, Brazil.
³University Campus of Parauapebas, Universidade Federal Rural da Amazônia (UFRA), Via de acesso para a UFRA, Rodovia PA 275, Km 08, Zona Rural, mailbox 3017, zip code 68515-000, Parauapebas City, Pará, Brazil.
⁴University Campus of Parauapebas, Universidade Federal Rural da Amazônia (UFRA), Via de acesso para a UFRA, Rodovia PA 275, Km 08, Zona Rural, mailbox 3017, zip code 68515-000, Parauapebas City, Pará, Brazil.
⁵University Campus of Parauapebas, Universidade Federal Rural da Amazônia (UFRA), Via de acesso para a UFRA, Rodovia PA 275, Km 08, Zona Rural, mailbox 3017, zip code 68515-000, Parauapebas City, Pará, Brazil.
⁶✉ Departamento de Ecologia e Zoologia, CCB/ECZ, Trindade, Universidade Federal de Santa Catarina, 88040-970 – Florianópolis, SC, Brazil.

2023 - Volume: 63 Issue: 4 pages: 1219-1224

Short note

Keywords

Abstract

Introduction

In addition to the prominent role of Brazil as one of the leading producers and exporters of chicken meat in large-scale facilities (Aquino 2021; Uzundumlu & Dilli 2023), the practice of raising chickens in small rural areas for subsistence is widespread across all regions of the country, particularly among low-income populations. Referred to as domestic poultry (''galinha caipira'' in Brazilian Portuguese) (Feitosa Jr. et al. 2020), these rustic chickens are commonly bred in urban areas of rural towns. However, this situation can contribute not only to the spread of ectoparasites but also to the dissemination of other significant disease-causing agents. The chickens are often allowed to roam freely and come into close contact with other domestic and wild birds (Arends 1997; Cunha et al. 2020).

Feather mites (Acariformes: Astigmata) are a substantial group of ectoparasitic arthropods permanently and exclusively associated with birds. They encompass over 2500 species, classified into 34 families and two superfamilies: Analgoidea and Pterolichoidea (Gaud & Atyeo 1996; Proctor 2003; Klimov & OConnor 2008; Mullen and OConnor 2019). A number of feather mite families from both the Analgoidea and Pterolichoidea have been documented in association with chickens worldwide. Mironov (2013) listed nine families of analgoidean mites, which representatives reside on the feathers, skin, in the quill cavities and respiratory tract of chickens, and of two families of pterolichoidean mites living on the feathers and in the quills.

In the family Pterolichidae, two species have been documented in association with domestic chickens, Pterolichus obtusus Robin, 1868 and Epistomolichus reticulatus Mironov, Pérez et Palma, 2009; the former worldwide (e.g. Kaschula & Stephan 1947; Gaud 1965; Manuel & Siores 1967; Rosen et al. 1985; Corpuz-Raros 1993; Sangvaranond 1993, 1994, 2003; Alekseev 1998; Wang & Fan 2010; Jankovska et al. 2012; Lakyat et al. 2022) and the latter from Galápagos Islands (Mironov et al. 2009). In the New World, P. obtusus has been reported in various countries, including the USA (Hirst 1922), Cuba (Černý 1970; Rodríguez et al. 2016; Santana & Pineda 2019), Costa Rica (Hernandez-Divers et al. 2008, Hernandez et al. 2013), Argentina (Roveda & Boero 1962), Peru (García et al. 2021), and Brazil (Hipólito & Freitas 1943; Oba et al. 1978).

In the present paper, we report the presence of P. obtusus on rustic chickens in two regions of Brazil, marking a significant rediscovery of this mite after a gap of 45 years since its last reported occurrence in the country.

Materials and methods

The mites reported herein came from small backyard chicken houses of two Brazilian administrative regions: 1) North: Marabá and Parauapebas, Pará State; 2) Southeast: Pains, district of São Lourenço, Minas Gerais State. In the case of the rustic chickens from Parauapebas, it was noticed that they appeared uncomfortable, and hardly gained weight – it was later shown that their wing feathers were full of parasitic mites. In the chickens from Marabá, the presence of mites was also observed. In the latter, the breeding conditions were more technical, with chickens resulted from cross breeds between rustic and Indian giant breed, in addition to being fed with a balanced diet, regularly vaccinated and dewormed – in these, the number of mites observed was visibly lower and there was no evidence of mite-related stress in the chickens.

Feather samples were sent inside dry bags to the Laboratory of Entomology of the Universidade Federal Rural da Amazônia, Campus of Parauapebas, and to the Acarology laboratory of the Universidade Federal de Santa Catarina, Florianópolis, for evaluation. The mite samples were collected from the feathers using a stereomicroscope. The mites specimens were mounted on slides using Hoyer's medium (Krantz & Walter 2009) and identified using light microscope based on the appropriate taxonomic literature (e.g. Atyeo & Gaud 1992; Gaud & Atyeo 1996; Mironov et al. 2010). Voucher specimens are deposited at the Acari Collection of the Department of Ecology and Zoology, Universidade Federal de Santa Catarina (ECZ-UFSC).

Results and discussion

All examined mite specimens were identified as Pterolichus obtusus Robin, 1877 (Pterolichidae) (Fig. 1). Three species are currently included in the genus Pterolichus: P. obtusus, P. lithodorus Gaud, 1965, and P. stenochaetus Gaud, 1965, the latter two species described from African francolins (Francolinus spp., Galliformes, Phasianidae, Gallini). The main diagnostic characters of this genus were outlined by Mironov et al. (2010, table I), and include: in both sexes, dorsal setae h1 absent; in males, legs III and IV subequal in thickness, subapical claw on tarsus IV absent, both setae d and e on tarsus IV filiform; and in females, dorsal setae d2 and e1 inserted on the main hysteronotal shield.

Material examined. From Gallus gallus domesticus (L.): 6♂♂, 6♀♀, 1n, Marabá (5°12′26.75″S; 49°02′46.14″ W), Pará State, 02.V.2022; 4♂♂, 9♀♀, Parauapebas (6°04′39.50″S; 49°51′43.57″W), Pará State, 04.V.2022, M.N.P. Cruz coll.; 16♂♂, 15♀♀, 1n, W.P. Cruz coll.; 15♂♂, 8♀♀, Pains (20°19′19.40″S; 45°42′43.97″W), district of São Lourenço, Minas Gerais State, 8.II.2014, L.F.O. Bernardi coll.

Pterolichus obtusus was previously reported in Brazil only twice: once in Minas Gerais state (no specific locality mentioned, Hipólito & Freitas 1943) and once in Mogi das Cruzes, São Paulo State, from industrial flocks of laying hens (Oba et al. 1978). This current record represents a notable rediscovery of the species, as its last known occurrence in this country dates back 45 years.

Among feather mites known to cause injury to farmed chickens globally, the most significant species include P. obtusus (Pterolichoidea: Pterolichidae), Megninia spp. (Analgoidea: Analgidae), and Allopsoroptoides galli Mironov (Analgoidea: Psoroptoididae) (Gaud et al. 1985; Mironov 2013). These species can cause dermatitis, leading to reduced performance and significant economic losses in poultry (D'Souza et al. 2001; Mullen & OConnor 2019). The observed symptoms in the chickens from Parauapebas are consistent with those previously reported in chickens infested with P. obtusus, such as bird restlessness, weight loss, reduced egg production and irregular molting patterns (Alekseev 1998). However, without a comprehensive systematic study under controlled conditions, it is not possible to definitively correlate these symptoms with the presence of these mites.

The current findings reveal that P. obtusus is more widely distributed in Brazil than previously suggested from the limited literature sources (Hipólito & Freitas 1943; Oba et al. 1978). We reveal that this species has persisted in the country despite the development of industrial rearing of chickens in large facilities, where young chicks are isolated from parental contact. This system impedes the primary mode of feather mite transmission between individuals – the vertical transmission (Doña et al. 2017). As demonstrated, small rural and backyard farms facilitate intergenerational contact between adult chickens and young chicks, maintaining populations of P. obtusus and other feather mites associated with chickens. Consequently, these farms can serve as ongoing sources of mite infestation for chickens and other poultry in the region.

The importance of Brazil as a major producer and exporter of chicken meat (Aquino 2021; Uzundumlu & Dilli 2023) underlines the significance of the present findings. By identifying the presence of these mites on chickens in Brazil, this brief communication provides valuable information for the development of animal health programs and policies aimed at controlling mite infestations. Additionally, it provides essential support for decision-making processes related to research funding dedicated to studying the impact of P. obtusus in both domestic and wild fowl populations, thus contributing to the advancement of aviculture in the country. Understanding the specific locations where these mites are prevalent enables the implementation of targeted measures to control their spread and prevent outbreaks and transfers between aviaries.

Acknowledgements

To the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the scholarships to the first and second authors and the Universidade Federal Rural da Amazônia for providing the necessary tools for this study; To Leopoldo O.F. Bernardi, for sending feather samples from Minas Gerais state.

Declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing Interests

The authors declare no competing interests.

Author contributions

All authors contributed to the elaboration of this study.

Funding

This study was not funded.

Availability of data and materials

Data is available from the authors upon reasonable request.

References

1. Alekseev A.N. 1998. Ticks and mites as permanent and temporary bird ectoparasites, vectors and disseminators of pathogens. Bulletin of the Scandinavian Society for Parasitology, 8(2): 1-8.
2. Aquino C. 2021. Poultry and Products Annual. Global Agricultural Information Network. Report Number: BR2021-0033. https://usdabrazil.org.br/wp-content/uploads/2021/09/Poultryand-Products-Annual_Brasilia_Brazil_09-01-2021-1.pdf
3. Arends J.J. 1997. External parasites and poultry pests. In: Calnek B.W., Barnes H.J., Beard C.W., McDougald L.R., Saif Y.M. eds. Diseases of Poultry. Ames, Iowa, USA: Iowa State University Press, 785-813.
4. Atyeo W.T., Gaud J. 1992. The identity of Pterolichus obtusus Robin, 1877 with descriptions of new genera and species of feather mites (Acarina, Pterolichidae) from the Galliformes (Aves). Acarologia, 33: 193-206. https://www1.montpellier.inrae.fr/CBGP/acarologia/article.php?id=2389
5. Černý V. 1970. Cerny Feather Mites (Sarcoptiformes, Analgoidea) of Domestic Fowl in Cuba. Folia Parasitologica, 17: 233-238.
6. Corpuz-Raros L.A. 1993. A checklist of Philippines mites and ticks (Acari) associated with vertebrates and their nests. Asia Life Sciences, 2(2): 177-200.
7. Cunha L.M., Rezende L.C., Oliveira T.M.D., Teixeira C.M., Santos A.K.R.D., Martins N.R.D.S., Lara L.J., Oliveira P.R. 2020. Validação de questionário para levantamentos de ocorrência e fatores de risco de ectoparasitos para avicultura. Conexão Ciência, 15:48-58. https://doi.org/10.24862/cco.v15i1.1100
8. Doña J., Potti J., Hera I., Blanco G., Frías O., Jovani R. 2017. Vertical transmission in feather mites: insights into its adaptive value. Ecological Entomology, 42: 492-499. https://doi.org/10.1111/een.12408
9. D'Souza P.E., Jagannath M.S., Murthy K.M.S. 2001. Feather mite infestation in a broiler breeder farm. VetRecord, 149: 777. https://doi.org/10.1136/vr.149.25.777-a
10. Feitosa Jr. A.B., Bezerra N.P.C., Bezerra D.C., Fonseca L.S., Negreiros R.C.A., Rios D.P., Coimbra V.C.S. 2020. Influenza aviária: vigilância ativa em criações avícolas de subsistência no entorno do Sítio de aves migratórias de Panaquatira, Maranhão, Brasil. Brazilian Journal of Development, 6: 17773-17782. https://doi.org/10.34117/bjdv6n4-085
11. García D.R., Ferrer Y.G., Valdés Fraga L., Mendoza O.C., Navarrete M.G., Rodríguez M.V. 2021. Evaluation of alpha-cypermethrin for the control of mites in laying hens under laboratory conditions. Revista de Investigaciones Veterinarias del Perú, 32(3): e20404. https://doi.org/10.15381/rivep.v32i3.20404
12. Gaud J. 1965. Acariens Sarcoptiformes plumicoles (Analgoidea) Parasites sur les oiseaux Galliformes d'Afrique. Annales du Musée Royal de l′Afrique Centrale, Série 8, Sciences zoologiques, 136: 1-77.
13. Gaud J., Atyeo W.T. 1996. Feather mites of the World (Acarina, Astigmata): the supraspecific taxa. Annales du Musée Royal de l′Afrique Centrale. Sciences Zoologiques, 277, 1-193 (Pt. 1, text) + 1-436 (Pt. 2, illustrations).
14. Gaud J., Atyeo W.T., Barré N. 1985. Les acariens du genre Megninia (Analgidae) parasites de Gallus gallus. Acarologia, 26: 171-182. https://www1.montpellier.inrae.fr/CBGP/acarologia/article.php?id=2673
15. Hernandez-Divers S.M., Villegas P., Jimenez C., Hernandez-Divers S.J., Garcia M., Riblet S.M., Carroll C.R., OConnor B.M., Webb J.L., Yabsley M.J., Williams S.M., Sanchez S. 2008. Backyard Chicken Flocks Pose a Disease Risk for Neotropic Birds in Costa Rica. Avian Diseases, 52: 558-566. https://doi.org/10.1637/8298-032808-Reg.1
16. Hernandez S.M., Peters V.E., Weygandt P.L., Jimenez C., Villegas P., OConnor B., Yabsley M.J., Garcia M., Riblet S.M., Carroll C.R. 2013. Do Shade-Grown Coffee Plantations Pose a Disease Risk for Wild Birds? Eco Health, 10: 145-158. https://doi.org/10.1007/s10393-013-0837-3
17. Hipólito O., Freitas M.G. 1943. Notas Ornitopatológicas (Observações sôbre alguns acarinos parasitos de Gallus gallus domesticus em Minas Gerais). Anais do II Congresso Brasileiro de Veterinária, 6: 81-82.
18. Hirst S. 1922. Mites Injurious to Domestic Animals, with an Appendix on the Acarine Disease of Hive Bees. Economic series (British Museum (Natural History)), no. 13. https://doi.org/10.5962/bhl.title.57139
19. Jankovska I., Bejcek V., Langrova I., Válek P., Vadlejch J., Čadková Z. 2012. Black grouse in Czech Republic and its parasites. Helminthologia, 49: 78-81. https://doi.org/10.2478/s11687-012-0016-z
20. Kaschula V.R., Stephan S.A.R. 1947. Mites, hitherto unrecorded in South Africa, collected in Natal from fowls, pigeons, turkeys, Guinea-fowls, wild birds and rabbits. Onderstepoort Journal of Veterinary Science and Animal Industry, 22(1): 51-75.
21. Klimov P., OConnor B.M. 2008. Origin and higher-level relationships of psoroptidian mites (Acari: Astigmata: Psoroptidia): Evidence from three nuclear genes. Molecular Phylogenetics and Evolution, 47(3): 1135-1156. https://doi.org/10.1016/j.ympev.2007.12.025
22. Krantz G.W., Walter D.E. 2009. A manual of Acarology. 3rd ed. Lubbock (TX): Texas Tech University Press; 807 pp.
23. Lakyat A., Pumnuan J., Thipmanee K. 2022. Ectoparasite species attacking chicken in eastern area of Bangkok, Thailand. International Journal of Agricultural Technology, 18(4): 1619-1632. http://www.ijat-aatsea.com/past_v18_n4.html
24. Manuel M.F., Siores F. 1967. Pterolichus obtusus Robin, 1868, a common feather mite of chickens in the Philippines. The Indian Veterinary Journal, 44: 1032-1035.
25. Mironov S.V. 2013. Allopsoroptoides galli n. g., n. sp., a new genus and species of feather mites (Acari: Analgoidea: Psoroptoididae) causing mange in commercially raised domestic chicken in Brazil. Systematic Parasitology, 85: 201-212. https://doi.org/10.1007/s11230-013-9422-y
26. Mironov S.V., Pérez T.M., Palma R. 2009. A new genus and species of feather mite of the family Pterolichidae (Astigmata: Pterolichidae) from Gallus gallus (Aves: Phasianidae) from the Galápagos Islands. Acarina, 17: 89-100.
27. Mironov S.V., Skirnisson K., Thorarinsdottir S.T., Nielsen O.K. 2010. Feather mites (Astigmata: Psoroptidia) parasitising the rock ptarmigan Lagopus muta (Montin) (Aves: Galliformes) in Iceland. Systematic Parasitology, 75: 187-206. https://doi.org/10.1007/s11230-009-9219-1
28. Mullen G.R., OConnor B.M. 2019. Mites (Acari). In: Mullen GR, Durden LA (ed) Medical and veterinary entomology, 3rd edn. Elsevier, Academic Press, pp 533-602. https://doi.org/10.1016/B978-0-12-814043-7.00026-1
29. Oba M.S.P., Pereira M.C., Schumaker T.T.S. 1978. Pterolichus obtusus Robin, 1868 (Acariformes: Dermoglyphidae) em Gallus gallus domesticus no Estado de São Paulo, Brasil. O Biológico, 44: 145-148.
30. Pedroso L., Hernandes F.A. 2016. New records of feather mites (Acariformes: Astigmata) from non-passerine birds (Aves) in Brazil. Check List 12: 1-25. https://doi.org/10.15560/12.6.2000
31. Proctor H.C. 2003. Feather mites (Acari: Astigmata): Ecology, behavior, and evolution. Annual Review of Entomology, 48: 185-209. https://doi.org/10.1146/annurev.ento.48.091801.112725
32. Rodríguez D., Larramendy R., Varona E., Colás M., Oscar R., Villa J.R., Morales Y., Cobas I., Rebollar R. 2016. Comportamiento de los parásitos externos en aves (Gallus gallus) de diferentes líneas puras. Revista Cubana de Ciencia Avícola, 39.2 (2015): 5-12.
33. Rosen S., Hadani A., Shoham D. 1985: Parasitic mites (Acarina: Arachnoïdea) in wild birds trapped in poultry farms in Israel. I: Species of mites and their hosts Acarologia, 26(1): 79-85. https://www1.montpellier.inrae.fr/CBGP/acarologia/article.php?id=2684
34. Roveda R.J., Boero J.J. 1962. Acaros de las plumas. Revista de la Facultad de Agronomia y Veterinaria. Buenos Aires, 51(2): 53-76.
35. Sangvaranond A. 1993. Studies on prevalence and outbreak of ectoparasites in native chickens in central part of Thailand. Kasetsart Journal - Natural Sciences, Thailand, 27: 194-203.
36. Sangvaranond A. 1994. Ectoparasites of Bantams in the Central Region of Thailand. Agriculture and Natural Resources 28(1). Bangkok, Thailand: 58-65. https://li01.tci-thaijo.org/index.php/anres/article/view/241376
37. Sangvaranond A. 2003. Ectoparasites of Domesticated Chickens in Thailand. Kasetsart Veterinarians, 13: 42-54.
38. Santana P.E.T., Pineda N.C. 2019. Actualización de la lista de Ácaros (Arachnida: Acari) de Cuba. Revista Ibérica de Aracnología, 34: 102-118.
39. Wang Z.-Y., Fan Q.-H. 2010. Psoroptidia (Acari: Astigmatina) of China: a review of research progress. Zoosymposia 4: 260-271. In: Zhang Z.-Q., Hong X.-Y., Fan Q.-H. (eds) Xin Jie-Liu Centenary: Progress in Chinese Acarology. Zoosymposia, 4: 1-345. https://doi.org/10.11646/zoosymposia.4.1.16
40. Uzundumlu A.S., Dilli M. 2023. Estimating Chicken Meat Productions of Leader Countries for 2019-2025 Years. Ciência Rural, Santa Maria, v.53:2, e20210477. https://doi.org/10.1590/0103-8478cr20210477

instructions