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Brood parasitic nestlings benefit from unusual host defenses against botfly larvae (Philornis spp.)

  • Cynthia A. UrsinoEmail author
  • M. C. De Mársico
  • J. C. Reboreda
Original Article

Abstract

Brood parasitic birds lay their eggs into the nests of other birds, abandoning parental care of their nestlings to the unsuspecting hosts. Parasite and host nestlings may themselves be parasitized by botfly larvae (Philornis: Muscidae), which burrow under the nestlings’ skin and can seriously affect growth and survival. Here, we provide the first direct evidence that adult baywings (Agelaioides badius), the primary host of the specialist brood parasitic screaming cowbird (Molothrus rufoaxillaris), regularly remove botfly larvae from their own and parasitic nestlings by pulling them out of the nestlings’ skin. This is the only bird species known to remove botfly larvae. By combining nestling cross-fostering with video recording of baywing nests, we show that due to prompt removal, infection with botfly larvae had negligible effects on nestling growth and survival despite high prevalence. Our results provide the first direct observations for larva removal behavior in botfly hosts. Screaming cowbirds may benefit from using baywings as its main host, as larva removal by adult baywings reduces the costs of botfly parasitism.

Significance statement

Infection by botfly larvae of the genus Philornis (Muscidae) causes nestling mortality in many Neotropical birds. Despite the lethal effects, most Philornis hosts studied so far lack specific defenses against these larvae. The grayish baywing (Agelaioides badius), primary host of the brood parasitic screaming cowbird (Molothrus rufoaxillaris), is the only species that, based on indirect evidence, would be able to remove Philornis larvae from infected nestlings. We provide the first direct evidence that adult baywings do indeed remove botfly larvae from their own nestlings as well as from parasitic cowbird nestlings and that this unusual defense may increase the survival of own and screaming cowbird nestlings at infected nests.

Keywords

Philornis sp. Ectoparasitism Brood parasitism Allopreening Heterospecific cleaning Cowbird 

Notes

Acknowledgments

We thank Fundación Elsa Shaw de Pearson for allowing us to conduct this study at Reserva El Destino and Vanina Fiorini, Florencia Lama and Juan Manuel Rojas Ripari for help with the fieldwork. We are grateful to Christina Riehl and two anonymous reviewers for providing valuable comments on the manuscript.

Data availability

The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.

Funding information

CAU is supported by a fellowship from the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). MCDM and JCR are Research Fellows of CONICET. This work was supported by grants to JCR of Agencia Nacional de Promoción Científica y Tecnológica (PICT 2011-0045) and University of Buenos Aires (Ubacyt W808).

Compliance with ethical standards

Conflict of interest

The authors declare they have no conflict of interest.

Ethical approval

Research presented in the manuscript was conducted in accordance with the Argentine law. The study was conducted under permit (202/12) from the local authority (OPDS, Province of Buenos Aires, Argentina). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. As the experimental protocols involving handling of birds were of minimal impact, the University of Buenos Aires committee for animal care and use did not intervene. No nestlings died or were injured during manipulations, and experimental infection had negligible effects on nestling growth and survival.

Supplementary material

265_2019_2751_MOESM1_ESM.mp4 (32.3 mb)
ESM 1 video recordings of Botfly removal by Baywing (MP4 33102 kb)

References

  1. Arendt WJ (1985) Philornis ectoparasitism of pearly- eyed thrashers. I. Impact on growth and development of nestlings Auk 102:270–280Google Scholar
  2. Bush SE, Clayton DH (2018) Anti-parasite behaviour of birds. Phil Trans R Soc B 373:20170196CrossRefGoogle Scholar
  3. Carvalho CJ, Couri MS, Pont AC, Pamplona D, Lopes S (2005) A catalogue of the Muscidae (Diptea) of the neotropical region. Zootaxa 860:1–282CrossRefGoogle Scholar
  4. Clayton DH, Koop JAH, Harbison CW, Moyer BR, Bush SE (2010) How birds combat ectoparasites. Open Ornithol J 3:41–71CrossRefGoogle Scholar
  5. Davies NB (2000) Cuckoos, cowbirds and other cheats. Oxford University Press, OxfordGoogle Scholar
  6. De Mársico MC, Reboreda JC (2008) Differential reproductive success favours strong host preference in a highly specialized brood parasite. Proc R Soc Lond B 275:2499–2506CrossRefGoogle Scholar
  7. De Mársico MC, Reboreda JC (2010) Brood parasitism increases mortality of bay-winged cowbird nests. Condor 112:407–417CrossRefGoogle Scholar
  8. De Mársico MC, Mahler B, Reboreda JC (2010) Reproductive success and nestling growth of the baywing parasitized by screaming and shiny cowbirds. Wilson J Ornithol 122:417–431CrossRefGoogle Scholar
  9. Di Giacomo AG, Reboreda JC (2015) Reproductive success of the specialist brood parasite screaming cowbird in an alternative host, the Chopi Blackbird. Auk 132:16–24CrossRefGoogle Scholar
  10. Dudaniec RY, Kleindorfer S (2006) Effects of the parasitic flies of the genus Philornis (Diptera: Muscidae) on birds. Emu 106:13–20CrossRefGoogle Scholar
  11. Fessl B, Kleindorfer S, Tebbich S (2006) An experimental study on the effects of an introduced parasite in Darwin’s finches. Biol Conserv 127:55–61CrossRefGoogle Scholar
  12. Fraga RM (1984) Bay-winged cowbird (Molothrus badius) remove ectoparasites from their brood parasites, the screaming cowbirds (M. rufoaxillaris). Biotrópica 16:223–226CrossRefGoogle Scholar
  13. Kleindorfer S, Dudaniec RY (2016) Host-parasite ecology, behavior and genetics: a review of the introduced fly parasite Philornis downsi and its Darwin’s finch hosts. BMC Zool 1:1–19CrossRefGoogle Scholar
  14. Knutie SA, Owen JP, McNew SM, Bartlow AW, Arriero E, Herman JM, DiBlasi E, Thompson M, Koop JA, Clayton DH (2016) Galápagos mockingbirds tolerate introduced parasites that affect Darwin’s finches. Ecology 97:940–950PubMedGoogle Scholar
  15. Lanyon S (1992) Interspecific brood parasitism in blackbirds (Icterinae): a phylogenetic perspective. Science 255:77–79CrossRefGoogle Scholar
  16. Lehmann T (1993) Ectoparasites: direct impact on host fitness. Parasitol Today 9:8–13CrossRefGoogle Scholar
  17. McNew SM, Clayton DH (2017) Alien invasion: biology of Philornis flies highlighting Philornis downsi, an introduced parasite of Galápagos birds. Annu Rev Entomol 63:369–387CrossRefGoogle Scholar
  18. Mermoz ME, Fernández GJ (2003) Breeding success of a specialist brood parasite, the Screaming Cowbird, parasitizing an alternative host. Condor 105:63–72CrossRefGoogle Scholar
  19. O’connor JA, Robertson J, Kleindorfer S (2010) Video analysis of host-parasite interactions in nests of Darwins finches. Oryx 44:588–594CrossRefGoogle Scholar
  20. Ortega C (1998) Cowbirds and other brood parasites. The University of Arizona Press, TucsonGoogle Scholar
  21. Peng YS, Fang Y, Xu S, Ge L (1987) The resistance mechanism of the Asian honey bee, Apis cerana Fabr., to an ectoparasitic mite, Varroa jacobsoni Oudemans. J Invertebr Pathol 49:54–60CrossRefGoogle Scholar
  22. Quiroga M, Reboreda JC (2012) Lethal and sublethal effects of botfly (Philornis seguyi) parasitism on House Wren nestlings. Condor 114:197–202CrossRefGoogle Scholar
  23. Rabuffetti FL, Reboreda JC (2007) Early infestation by bot flies (Philornis seguyi) decreases chick survival and nesting success in chalk-browed mockingbirds (Mimus saturninus). Auk 124:898–906CrossRefGoogle Scholar
  24. Segura LN, Reboreda JC (2011) Botfly parasitism effects on nestling growth and mortality of red-crested cardinals. Wilson J Ornithol 123:107–115CrossRefGoogle Scholar
  25. Sorenson MD, Payne RB (2002) Molecular genetics perspectives on avian brood parasitism. Integr Comp Biol 42:388–400CrossRefGoogle Scholar
  26. Thorogood R, Spottiswoode CN, Portugal SJ, Gloag R (2019) The coevolutionary biology of brood parasitism: a call for integration. Phil Trans R Soc B 374:20180190CrossRefGoogle Scholar
  27. Young BE (1993) Effects of the parasitic botfly Philornis carinatus on nestling house wrens, Troglodytes aedon, in Costa Rica. Oecologia 93:256–262CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, IEGEBA-UBA-CONICETUniversidad de Buenos Aires, Pabellón II Ciudad UniversitariaBuenos AiresArgentina

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