Skip to main content
SpringerLink
Log in

Variation of dipteran ectoparasites (Streblidae) on Anoura geoffroyi Gray, 1838 (Phyllostomidae) in two caves in southeastern Brazil

  • Immunology and Host-Parasite Interactions - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Bats are parasitized by many different arthropods, among which the dipteran families Nycteribiidae and Streblidae are exclusive to bats. Researches that relate the ecology of ectoparasites with their hosts are fundamental for understanding issues related to the interactions between these two groups, in addition to epidemiological aspects of pathogen transmission. The present study evaluated the rate of infestation by dipteran (Streblidae) ectoparasites in two colonies of Anoura geoffroyi associated with caves in the southeastern Brazil. It also evaluated whether parasitological indices differ significantly with regard to host sex and reproductive condition. A total of 1377 bats were captured, of which 84% were parasitized. From these, a total of 5047 streblid bat flies belonging to three species of three genera were collected and identified. The most abundant was Exastinion clovisi (57%), followed by Anastrebla modestini (30%) and Trichobius propinquus (13%). In general, the populations of ectoparasites fluctuated throughout the year, with peaks of abundance during the rainy season. The sex ratios for the species of ectoparasites were close to one, which differs from what is reported in the literature. In addition, there were significant differences in parasitism rates in relation to host sex and reproductive condition. In both populations, ectoparasite infestation of pregnant or lactating females was significantly higher than for non-reproductive females. New studies aimed at assessing whether these higher rates of infestation have any effect on female bat reproduction are needed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Anderson R, Ortencio Filho H (2006) Dípteros ectoparasitas (Diptera, Streblidae) de filostomídeos (Chiroptera, Mammalia) do Parque Municipal no cinturão verde de Cianorte, Paraná, Brasil e sua incidência ao longo das estações do ano. Chiroptera Neotropical 12:238–243

    Google Scholar 

  • Anthony ELP (1988) Age determination in bats. In: Ecological and Behavioral Methods for the Study of Bats. (T. H. Kunz, Ed.). Washington, DC: Smithsonian Institution Press. 47–57.

  • Ascuntar-Osnas O, Montoya-Bustamante S, González-Chávez B (2020) Records of Streblidae (Diptera: Hippoboscoidea) in a tropical dry forest fragment in Colombia. Biota Colombiana 21:16–27. https://doi.org/10.21068/c2020.v21n01a02

    Article  Google Scholar 

  • Azevedo AA, Linardi PM (2002) Streblidae (Diptera of Phyllostomid bats from Minas Gerais, Brasil. Mem Inst Oswaldo Cruz 97:421–422

    Article  Google Scholar 

  • Barbier E, Graciolli G (2016) Community of bat flies (Streblidae and Nycteribiidae) on bats in the Cerrado of Central-West Brazil: hosts, aggregation, prevalence, infestation intensity, and infracommunities. Studies on Neotropical Fauna and Environment 51:176–187

    Article  Google Scholar 

  • Barbier E, Falcão F, Bernard E (2021) Bat-ectoparasitic fly relationships in a seasonally dry tropical forest in Brazil. Parasitol Res 120:3507–3517

    Article  Google Scholar 

  • Bateman MA (1972) The ecology of fruit fly. Annual Review Entomology 17:493–518

    Article  Google Scholar 

  • Bernard E, Machado RB, Aguiar LMS (2011) Discovering the Brazilian bat fauna: a task for two centuries? Mammal Rev 41:23–39

    Article  Google Scholar 

  • Bertola PB, Aires CC, Favorito SE, Graciolli G, Amaku M, Rocha MP (2005) Batflies (Diptera: Streblidae, Nycteribiidae) parasitic on bats (Mammalia: Chiroptera) at Parque Estadual da Cantareira, São Paulo, Brazil: parasitism rates and host-parasite associations. Mem Inst Oswaldo Cruz 100(1):25–32

    Article  Google Scholar 

  • Bonifaz E, Mena JL, Oporto R. (2020). Moscas de murciélagos en algunas localidades de la costa peruana. Revista peruana de biología 27:241–250 (Mayo 2020).  https://doi.org/10.15381/rpb.v27i2.17881

  • Bredt A, Uieda W, Magalhaes ED (1999) Morcegos cavernícolas da região do Distrito Federal, centro-oeste do Brasil (Mammalia, Chiroptera). Revista Brasileira De Zoologia 16:731–770

    Article  Google Scholar 

  • Bueno MET (1992) Geografia da Serra da Piedade. In: Serra da Piedade (Duarte R.H., org.). Belo Horizonte: CEMIG 136

  • Bush AO, Lafferty KD, Lotz JM, Shostaki AWParasitology meets ecology on its own terms: Margolis, et al (1997) Revisited. J Parasitol 83:575–583

    Article  CAS  Google Scholar 

  • Caballero-Martínez LA, Manzano IVR (2009) Hábitos alimentarios de Anoura geoffroyi (Chiroptera: Phyllostomidae) em Ixtapan Del Oro, Estado do México. Acta Zoologia Mexicana 25:161–175

    Google Scholar 

  • Clutton-Brock TH, Albon SD, Quinness FE (1989) Fitness costs of gestation and lactation in wild mammals. Nature 337:260–262

    Article  CAS  Google Scholar 

  • Dick CW, Graciolli G (2018) Checklist of world streblidae (Diptera: Hippoboscoidea). Center for Integrative Research, The Field Museum of Natural History, Chicago, Ill. Available from https://www.researchgate.net/publication/322579074_checklist_of_world_nycteribiidae_diptera_hippoboscoidea. Accessed october 6 june, 2021

  • Dick CW, Miller JA (2010) Streblidae.1249–1260 In: Manual of Central American Diptera (Vol II). Brown BVA, Borkent JM, Cumming DM, Wood NE, Woodley and M. Zumbado (Editors). National Research Council Press, Ottawa

  • Dick CW, Patterson BD (2006) Bat flies - obligate ectoparasites of bats. In S Morand, BR Krasnov, R. Poulin, Micromammals and macroparasites: from evolutionary ecology to management, Springer-Verlag, Tokio 179–194

  • Dittmar K, Morse S, Gruwell M, Mayberry J, DiBlasi E (2011) Spatial and temporal complexities of reproductive behavior and sex ratios: A case from parasitic insects. PLoS ONE 6(5):e19438. https://doi.org/10.1371/journal.pone.0019438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Esbérard CEL, Astúa D, Geise L, Costa LM, Pereira LG (2012) Do young Carollia perspicillata (Chiroptera: Phyllostomidae) present higher infestation rates of Streblidae (Diptera)? Braz J Biol 72:617–621

    Article  Google Scholar 

  • Fritz GN (1983) Biology and ecology of bat flies (Diptera: Streblidae) on bats in the genus Carollia. J Med Entomol 20:1–10

    Article  CAS  Google Scholar 

  • Forrest JRK (2016) Complex responses of insect phenology to climate change. Current Opinion in Insect Science 17:49–54

    Article  Google Scholar 

  • Graciolli G (2021) Streblidae in Catálogo Taxonômico da Fauna do Brasil. PNUD. http://fauna.jbrj.gov.br. Accessed 25 April 2021

  • Graciolli G, Rui AM (2001) Streblidae (Diptera, Hippoboscoidae) em morcegos (Chiroptera, Phillostomidae) no Nordeste do Rio Grande do Sul, Brasil. Iheringia, Série Zoologia, Porto Alegre 90:85–92

    Article  Google Scholar 

  • Graciolli G, Coelho DC (2001) Streblidae (Diptera: Hippoboscoidea) sobre morcegos filostomídeos (Chiroptera: Phyllostomidae) em cavernas do Distrito Federal, Brasil. Revista Brasileira De Zoologia 18:65–970

    Google Scholar 

  • Graciolli G, Carvalho CJB (2001) Moscas ectoparasitas (Diptera, Hippoboscoidea, Nycteribiidae) de morcegos (Mammalia, Chiroptera do Estado do Paraná, Brasil. 1. Basilia, taxonomia e chave pictórica para as espécies. Revista Brasileira de Zoologia 33–49

  • Gribel R, Hay JD (1993) Pollination ecology of Caryocar brasilienses (Caryocaraceae) in central Brazil cerrado vegetation. Jornal of Tropical Ecology 199–211

  • Guerrero R (2019) Streblidae (Diptera:Pupipara) de Venezuela: Sistemática, ecología y evolucíon. Editorial Académica Española 600

  • Hicks O, Burthe SJ, Daunt F, Newell M, Butles A, Ito M, Katsufumi S, Green J (2018) The energetic cost of parasitism in a wild population. Proceedings of the Royal Society b: Biological Sciences 285:1–8. https://doi.org/10.1098/rspb.2018.0489

    Article  Google Scholar 

  • Hofstede HM, Fenton MB (2005) Relationship between roost preferences, ectoparasite density, and grooming behaviours of neotropical bats. Journal of Zoology London 266:333–340

    Article  Google Scholar 

  • Komeno CA, Linhares AX (1999) Batflies parasitic on some phyllostomid bats in Southeastern Brazil: parasitism rates and host-parasite relationships. Mem Inst Oswaldo Cruz 94:151–156

    Article  CAS  Google Scholar 

  • Koppen W (1948) Climatologia: con un studio de los climas de la tierra. México: Fondo de Cultura Economica. 478

  • Kurta A, Bell GP, Nagy KA, Kunz TH (1989) Energetics of pregnancy and lactation in freeranging little brown bats (Myotis lucifugus). Physiological Zoology 62:804–818.Mantilla-Meluk H, Baker RJ (2010) New species of Anoura (Chiroptera: Phyllostomidae) from Colombia, with systematic remarks and notes on the distribution of the A. geoffroyi complex. Occasional Papers of the Museum of Texas Tech University 292:1–19

    Google Scholar 

  • Mantilla-Meluk H, Baker RJ (2010) New species of Anoura (Chiroptera: Phyllostomidae) from Colombia, with systematic remarks and notes on the distribution of the A. geoffroyi complex. Museum of Texas Tech University, pp. 1–24

  • Markus M (2003) Avaliação das áreas de preservação permanente na microbacia do Ribeirão da Casa Branca – Brumadinho. MG. Dissertation, Universidade Federal de Minas Gerais, Belo Horizonte

  • Marshall A (1982) Ecology of insects ectoparasitic on bats. In: Kunz, T. Ecology of bats. New York: Plenum Press 369–401

  • Möller AP (1997) Parasitism and the evolution of host life history. In Host parasite evolution. General principles and avian models (ed. D. H. Clayton & J. Moore), pp. 105 127. New York: Oxford University Press

  • Muchhala N, Jarrín VP (2002) Flower Visitation by Bats in Cloud Forests of Western Ecuador. Biotropica 34:387–395

    Article  Google Scholar 

  • Obdianela MCN, Guanlao PVV, Samaniego EVE, Pornobi KO (2021) Prevalence and Host Specificity of Bat Flies (Streblidae) from Selected Caves in Unisan, Quezon, Philippines. Acta Parasitologica. https://doi.org/10.1007/s11686-021-00373-9

  • Patterson DB, Dick CW, Dittmar K (2007) Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae). J Trop Ecol 23:177–189

    Article  Google Scholar 

  • Peck SB (1974) The Invertebrate Fauna of Tropical American Caves, Part II: Puerto Rico, An Ecological and Zoogeographic Analysis. Biotropica 60:14–31

    Article  Google Scholar 

  • Pessoa SB, Guimarães LR (1936) Notas sobre Streblidae (Diptera), com a descripção de um novo genero e duas novas especies. Anais Fac. Med. Univ. S. Paulo, São Paulo, 12(3):255–267. 1940. Nota sobre streblídeos (Diptera) de morcegos de Mato-Grosso, Brasil. Archos Inst. biol., São Paulo, 11:421–426

  • Postawa T, Szubert-kruszynska AA (2014) Is parasite load dependent on host aggregation size? The case of the greater mouse-eared bat Myotis myotis (Mammalia: Chiroptera) and its parasitic mite Spinturnix myoti (Acari: Gamasida). Parasitol Res 113:1803–1811

    Article  Google Scholar 

  • Poulson TL, White WB (1969) The cave environment. Science 165:971–981

    Article  CAS  Google Scholar 

  • Reis AS (2018) Anoura geoffroyi Gray, 1838: Historia natural de duas colônias associadas a cavernas localizadas no Quadrilátero Ferrífero, Minas Gerais, Brasil Pontifícia Universidade Católica de Minas Gerais, Minas Gerais

  • Reis NR, Peracchi A, Pedro WA, Lima IP (2006) Mamíferos do Brasil. Londrina 1- 437

  • Rui AM, Graciolli G (2005) Moscas ectoparasitas (Diptera, Streblidae) de morcegos (Chiroptera Phyllostomidae) no sul do Brasil: Associações hospedeiro-parasitos e taxas de infestações. Revista Brasileira De Zoologia 22:438–445

    Article  Google Scholar 

  • Souza FCR, Carmo FF (2015) Geossistemas ferruginosos no Brasil. Pp. 47- 76. IN: Carmo FF, Kamino LHY (Org.) Geossistemas Ferruginosos do Brasil: Áreas prioritárias para a conservação da diversidade geológica e biológica, patrimônio cultural e serviços ambientais. Belo Horizonte, 3i Editora

  • StatSoft, Inc. (2004) STATISTICA (data analysis software system), version 7. www.statsoft.com

  • Studier EH, Lysengen VL, O’Farrell MJ (1973) Biology of Myotis thysanodes and M. lucifugus (Chiroptera: Vespertilionidae) - II. Bioenergetics of pregnancy and lactation. Comp Biochem Physiol A Physiol 44:467–471

    Article  CAS  Google Scholar 

  • Torres JM, Urbieta GL, Almeida L, Soares DK, Dos Anjos EA (2019). Ectoparasitic flies (Diptera, Streblidae) of bats (Mammalia, Chiroptera) in a periurban remnant of Cerrado: community composition, prevalence, infestation intensity and specificity. Iheringia, Série Zoologia 109: e2019006

  • Trajano E (1985) Ecologia de populações de morcegos cavernícolas em uma região cárstica do sudeste do Brasil. Revista Brasileira De Zoologia 2:255–320

    Article  Google Scholar 

  • Teixeira ALM, Ferreira RL (2010) Fauna de dípteros parasitas (Diptera: Streblidae) e taxas de infestação em morcegos presentes em cavidades artificiais em Minas Gerais. Chiroptera Neotropical 16:748–754

    Google Scholar 

  • Tschapka M, Dressler S (2002) Chiropterophily: On bat-flowers and flower-bats. Curtis’s Botanical Magazine 19:114–125

    Article  Google Scholar 

  • Whittaker RJ, Jones SH (1994) The Role of Frugivorous Bats and Birds in the Rebuilding of a Tropical Forest Ecosystem, Krakatau, Indonesia. J Biogeogr 21:245–258

    Article  Google Scholar 

  • Urbieta GL, Torres J, Anjos EAC, Carvalho CME, Graciolli G (2018) Parasitism of bat flies (Nycteribiidae and Streblidae) on bats in urban environments: lower prevalence, infracommunities, and specificity. Acta Chiropterologica 20:511–518

    Article  Google Scholar 

  • Vasconcelos PF, Falcão LAD, Graciolli G, Borges MAZ (2016) Parasite-host interactions of bat flies (Diptera: Hippoboscoidea) in brazilian tropical dry forests. Parasitology Research (1987. Print) 115:367–377

  • Wenzel RL (1976) The streblid batflies of Venezuela (Diptera: Streblidae). Young University Science Bulletin, Biological Series 20:1–177

    Google Scholar 

  • Wenzel RL, Tipton VJ, Kiewlicz A (1966) The streblid batflies of Panama (Diptera: Calyptera: Streblidae). In: Wenzel RL, Tipton VJ (eds.) Ectoparasites of Panama. Field Museum of Natural History, Chicago, pp. 405–675

  • Whitaker Junios JO, Ritzi CM, Dick CW (2009) Collecting and preserving ectoparasites for ecological study. In JH Kunz & S Parsons Ecological and Behavioral Methods for the Study of Bats, second edition, John Hopkins University Press, Baltimore 806–827

  • Wolda H (1988) Insect seasonality: why? Annu Rev Ecol Syst 19:1–18

    Article  Google Scholar 

Download references

Acknowledgements

We thank Santuário Nossa Senhora da Piedade and Vale S.A. represented by Gerência de Espeleologia (DIFP) for allowing access to the study areas and for providing logistical support for carrying out the work. We also thank the reviewers for their valuable comments on our manuscript.

Funding

Comitê de Ética da Pontifícia Universidade Católica de Minas Gerais—(CEUA-PUC) and Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) provided grant research authorizations. PUC Minas provided scholarship grant. Fundo de Incentivo à Pesquisa (FIP-2017/387-S1) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq—processo 306216/2018-3) provided funding for the research.

Author information

Authors and Affiliations

  1. Programa de Pós-Graduação em Biologia de Vertebrados, Pontifícia Universidade Católica de Minas Gerais, Belo Horizonte, MG, Brazil

    Aline da Silva Reis & Sônia A. Talamoni

  2. Vale S.A., Gerência de Licenciamento e Espeleologia - Cadeia de Valor de Ferrosos, Nova Lima, Brazil

    Robson de Almeida Zampaulo

  3. Programa de Pós-Graduação em Ecologia e Conservação, Universidade Federal de Mato Grosso do Sul, Campo Grande, Brazil

    Guilherme Douglas Piel Dornelles & Gustavo Graciolli

  4. Instituto de Biociências, Universidade Federal do Mato Grosso do Sul (UFMS), Campo Grande, Brazil

    Gustavo Graciolli

Authors
  1. Aline da Silva Reis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robson de Almeida Zampaulo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guilherme Douglas Piel Dornelles
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gustavo Graciolli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sônia A. Talamoni
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aline da Silva Reis.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Section Editor: Boris R. Krasnov

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 189 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

da Silva Reis, A., de Almeida Zampaulo, R., Dornelles, G.D.P. et al. Variation of dipteran ectoparasites (Streblidae) on Anoura geoffroyi Gray, 1838 (Phyllostomidae) in two caves in southeastern Brazil. Parasitol Res 121, 255–265 (2022). https://doi.org/10.1007/s00436-021-07385-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-021-07385-4

Keywords

Search

Navigation