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Aspects of the life cycle of the avian parasite Philornis torquans (Diptera: Muscidae) under laboratory rearing conditions

Published online by Cambridge University Press:  14 March 2018

María José Saravia-Pietropaolo ,
Sofía I. Arce ,
Darío E. Manzoli ,
Martín Quiroga  and
Pablo M. Beldomenico
María José Saravia-Pietropaolo*
Affiliation:
Laboratorio de Ecología de Enfermedades, Instituto de Ciencias Veterinarias del Litoral (ICiVet-Litoral), Universidad Nacional del Litoral (UNL)/Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), R. P. Kreder 2805, 3080, Esperanza, Santa Fe, Argentina
Sofía I. Arce
Affiliation:
Laboratorio de Ecología de Enfermedades, Instituto de Ciencias Veterinarias del Litoral (ICiVet-Litoral), Universidad Nacional del Litoral (UNL)/Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), R. P. Kreder 2805, 3080, Esperanza, Santa Fe, Argentina
Darío E. Manzoli
Affiliation:
Laboratorio de Ecología de Enfermedades, Instituto de Ciencias Veterinarias del Litoral (ICiVet-Litoral), Universidad Nacional del Litoral (UNL)/Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), R. P. Kreder 2805, 3080, Esperanza, Santa Fe, Argentina
Martín Quiroga
Affiliation:
Laboratorio de Ecología de Enfermedades, Instituto de Ciencias Veterinarias del Litoral (ICiVet-Litoral), Universidad Nacional del Litoral (UNL)/Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), R. P. Kreder 2805, 3080, Esperanza, Santa Fe, Argentina Cátedra de Evolución, Facultad de Ciencia y Tecnología, Universidad Autónoma de Entre Ríos, Ruta Provincial 11, Km 10.5, 3100, Oro Verde, Entre Ríos, Argentina
Pablo M. Beldomenico
Affiliation:
Laboratorio de Ecología de Enfermedades, Instituto de Ciencias Veterinarias del Litoral (ICiVet-Litoral), Universidad Nacional del Litoral (UNL)/Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), R. P. Kreder 2805, 3080, Esperanza, Santa Fe, Argentina
*
1Corresponding author: (e-mail: [email protected])
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Abstract

The life cycle of the avian parasitic flies Philornis Meinert (Diptera: Muscidae) is poorly known, limiting the understanding of the ecology of these flies, including interactions with their hosts. We provide data on length and survival of pupal and adult stages and the duration of the pre-oviposition period of Philornis torquans Nielsen. Specimens were collected at larval and pupal stages from infested broods. The pupal stage lasted on average 10.5 days and adults lived up to 100 days in the laboratory. At least 90.2% of larvae pupated and 85.7% of the latter emerged as adults. For individuals collected as larvae, pupal mortality was 3.5 times higher than for those collected as pupae. Females laid from 1–8 clutches in their lifetime and deposited, on average, 41 eggs per female (range: 1–148). Females collected as pupae were larger and had shorter pre-oviposition periods and lifespans than females collected as larvae, but there were no differences in the total eggs laid by these females. This is the first information on reproductive parameters of a subcutaneous species of Philornis, and forms the basis for studies on conditions required for reproduction of this species in captivity.

Type
Physiology, Biochemistry, Development, & Genetics
Information
The Canadian Entomologist , Volume 150 , Issue 3 , June 2018 , pp. 317 - 325
Copyright
© Entomological Society of Canada 2018 

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Footnotes

Subject editor: Kevin Floate

References

Antoniazzi, L., Manzoli, D., Rohrmann, D., Saravia, M., Silvestri, L., and Beldomenico, P. 2011. Climate variability affects the impact of parasitic flies on Argentinean forest birds. Journal of Zoology, 283: 126–134.CrossRefGoogle Scholar
Arendt, W.J. 1985a. Philornis ectoparasitism of pearly-eyed thrashers I. Impact on growth and development of nestlings. The Auk, 102: 270–280.CrossRefGoogle Scholar
Arendt, W.J. 1985b. Philornis ectoparasitism of pearly-eyed thrashers II. Effects on adults and reproduction. The Auk, 102: 281–292.Google Scholar
Arendt, W.J. 2000. Impact of nest predators, competitors, and ectoparasites on pearly-eyed thrashers, with comments on the potential implications for Puerto Rican parrot recovery. Ornitología Neotropical, 11: 13–63.Google Scholar
Aruna Devi, A., Abu Hassan, A., Kumara, T.K., and Che Salmah, M.R. 2011. Life table of Synthesiomyia nudiseta (Van der Wulp) (Diptera: Muscidae) under uncontrolled laboratory environments – a preliminary study. Tropical Biomedicine, 28: 524–530.Google Scholar
Bennett, G.F. and Whitworth, T.L. 1991. Studies on the life history of some species of Protocalliphora (Diptera: Calliphoridae). Canadian Journal of Zoology, 69: 2048–2058.Google Scholar
Bulgarella, M., Quiroga, M.A., Brito Vera, G.A., Dregni, J.S., Cunninghame, F., Mosquera Muñoz, D.A., et al. 2015. Philornis downsi (Diptera: Muscidae), an avian nest parasite invasive to the Galápagos Islands, in mainland Ecuador. Annals of the Entomological Society of America, 108: 242–250.Google Scholar
Causton, C.E., Cunninghame, F., Tapia, W. 2013. Management of the avian parasite Philornis downsi in the Galapagos Islands: a collaborative and strategic action plan. In Galapagos Report 2011–2012. Edited by L.J. Cayot, D. Cruz, and R. Knab. Galapagos National Park Service, Governing Council of Galapagos, Charles Darwin Foundation, and Galapagos Conservancy, Puerto Ayora, Ecuador. Pp. 167–173.Google Scholar
Causton, C.E., Peck, S.B., Sinclair, B.J., Roque-Albelo, L., Hodgson, C.J., and Landry, B. 2006. Alien insects: threats and implications for conservation of Galápagos Islands. Annals of the Entomological Society of America, 99: 121–143.Google Scholar
Couri, M.S. 1999. Myiasis caused by obligatory parasites. Ia. Philornis Meinert (Muscidae). In Myiasis in man and animals in the Neotropical Region. Edited by J.H. Guimarães, and N. Papavero. Plêiade/Fundação de Amparo à Pesquisa do Estado de São Paulo, São Paulo, Brazil. Pp. 51–70.Google Scholar
Couri, M.S., Antoniazzi, L.R., Beldomenico, P., and Quiroga, M. 2009. Argentine Philornis Meinert species (Diptera: Muscidae) with synonymic notes. Zootaxa, 2261: 52–62.Google Scholar
Couri, M.S. and Carvalho, C.J.B. 2003. Systematic relations among Philornis Meinert, Passeromyia Rodhain and Villeneuve and allied genera (Diptera, Muscidae). Brazilian Journal of Biology, 63: 223–232.CrossRefGoogle ScholarPubMed
Couri, M.S., Carvalho, C.J.B., and Löwenberg-Neto, P. 2007. Phylogeny of Philornis Meinert species (Diptera: Muscidae). Zootaxa, 1530: 19–26.Google Scholar
Couri, M.S., Tavares, M.T., and Stenzel, R.R. 2006. Parasitoidism of chalcidid wasps (Hymenoptera, Chalcididae) on Philornis sp. (Diptera, Muscidae). Brazilian Journal of Biology, 66: 553–557.CrossRefGoogle ScholarPubMed
Davies, S., Kattel, R., Bhatia, B., Petherwick, A., and Chapman, T. 2005. The effect of diet, sex and mating status on longevity in Mediterranean fruit flies (Ceratitis capitata), Diptera: Tephritidae. Experimental Gerontology, 40: 784–792.Google Scholar
Delannoy, C.A. and Cruz, A. 1991. Philornis parasitism and nestling survival of the Puerto Rican sharp-shinned hawk. In Bird–parasite interactions: ecology, evolution, and behaviour. Edited by J.E. Loye and M. Zuk. Oxford University Press, Oxford, United Kingdom. Pp. 93–103.Google Scholar
Delvare, G., Heimpel, G.E., Baur, H., Chadee, D.D., Martinez, R., and Knutie, S.A. 2017. Description of Brachymeria philornisae sp. n. (Hymenoptera: Chalcididae), a parasitoid of the bird parasite Philornis trinitensis (Diptera: Muscidae) in Tobago, with a review of the sibling species. Zootaxa, 4242: 34–60.CrossRefGoogle Scholar
Dominguez, M., Reboreda, J.C., and Mahler, B. 2014. Impact of shiny cowbird and botfly parasitism on the reproductive success of the globally endangered yellow cardinal Gubernatrix cristata . Bird Conservation International, 25: 294–305.Google Scholar
Dudaniec, R.Y., Gardner, M.G., and Kleindorfer, S. 2010. Offspring genetic structure reveals mating and nest infestation behaviour of an invasive parasitic fly (Philornis downsi) of Galápagos birds. Biological Invasions, 12: 581–592.Google Scholar
Dudaniec, R.Y. and Kleindorfer, S. 2006. The effects of the parasitic flies Philornis (Diptera, Muscidae) on birds. Emu, 106: 13–20.Google Scholar
Ferrar, P. 1980. Cocoon formation by Muscidae (Diptera). Austral Entomology, 19: 171–174.CrossRefGoogle Scholar
Fessl, B., Couri, M., and Tebbich, S. 2001. Philornis downsi Dodge and Aitken, new to the Galapagos Islands (Diptera, Muscidae). Studia Dipterologica, 8: 317–322.Google Scholar
Fessl, B., Sinclair, B.J., and Kleindorfer, S. 2006. The life cycle of Philornis downsi (Diptera: Muscidae) parasitizing Darwin’s finches and its impacts on nestling survival. Parasitology, 133: 739–747.CrossRefGoogle ScholarPubMed
Fletcher, M.G., Axtell, R.C., and Stinner, R.E. 1990. Longevity and fecundity of Musca domestica (Diptera: Muscidae) as a function of temperature. Journal of Medical Entomology, 27: 922–926.CrossRefGoogle ScholarPubMed
Fraenkel, G. and Bhaskaran, G. 1973. Pupariation and pupation in cyclorrhaphous flies (Diptera): terminology and interpretation. Annals of the Entomological Society of America, 66: 418–422.Google Scholar
Ghoneim, K., Hamadah, K., El-Hela, A., Mohammad, A.H., and Amer, M. 2016. Efficacy of Nigella sativa (Ranunculaceae) extracts on adult performance and phase transition of the desert locust Schistocerca gregaria (Orthoptera: Acrididae). Munis Entomology and Zoology Journal, 11: 287–302.Google Scholar
Guedes, N.M.R., Werneck, M.R., Couri, M.S., and Araújo, F.R. 2000. Filhotes de arara-azul (Anodorhynchus hyacinthinus) com infestação por larvas de Philornis no Pantanal Sul, Brasil. In Ornitologia Brasilera no século XX: incluindo os resumos do VIII Congresso Brasileiro de Ornitologia (Florianópolis, 9 a 14 de julho de 2000). Edited by F.C. Straube, M.M. Argel-de-Oliveira, and J.F. Cândido. Universidade do Sul de Santa Catarina, Sociedade Brasileira de Ornitologia, Curitiba, Brasil. Pp. 331–332.Google Scholar
Haseyama, K.L., Wiegmann, B.M., Almeida, E.A., and de Carvalho, C.J. 2015. Say goodbye to tribes in the new house fly classification: a new molecular phylogenetic analysis and an updated biogeographical narrative for the Muscidae (Diptera). Molecular Phylogenetics and Evolution, 89: 1–12.Google Scholar
Kamal, A.S. 1958. Comparative study of thirteen species of sarcosaprophagous Calliphoridae and Sarcophagidae (Diptera) I. Bionomics. Annals of the Entomological Society of America, 51: 261–271.CrossRefGoogle Scholar
Kaspi, R., Mossinson, S., Drezner, T., Kamensky, B., and Yuval, B. 2002. Effects of larval diet on development rate and reproductive maturation of male and female Mediterranean fruits flies. Physiological Entomology, 27: 29–38.CrossRefGoogle Scholar
Kleindorfer, S. and Dudaniec, R.Y. 2016. Host-parasite ecology, behavior and genetics: a review of the introduced fly parasite Philornis downsi and its Darwin’s finch hosts. BMC Zoology, 1: 1–19.CrossRefGoogle Scholar
Kleindorfer, S., Peters, K.J., Custance, G., Dudaniec, R.Y., and O’Connor, J.A. 2014. Changes in Philornis infestation behavior threaten Darwin’s finch survival. Current Zoology, 60: 542–550.Google Scholar
Lincango, P. and Causton, C.E. 2008. Crianza en cautiverio de Philornis downsi en las Islas Galápagos. Informe interno. Charles Darwin Foundation, Puerto Ayora, Ecuador.Google Scholar
Luckinbill, L.S., Arking, R., Clare, M.J., Cirocco, W.C., and Buck, S.A. 1984. Selection for delayed senescence in Drosophila melanogaster . Evolution, 38: 996–1003.Google Scholar
Maklakov, A.A. and Lummaa, V. 2013. Evolution of sex differences in lifespan and aging: causes and constraints. BioEssays, 35: 717–724.Google Scholar
Manzoli, D., Antoniazzi, L., Saravia, M., Silvestri, L., Rorhmann, D., and Beldomenico, P. 2013. Multi-level determinants of parasitic fly infection in forest passerines. Public Library of Science One, 8: e67104. https://doi.org/10.1371/J.pone.0067104.Google Scholar
Monje, L.D., Quiroga, M., Manzoli, D., Couri, M.S., Silvestri, L., Venzal, J.M., et al. 2013. Sequence analysis of the internal transcribed spacer 2 (ITS2) from Philornis seguyi (García, 1952) and Philornis torquans (Nielsen, 1913) (Diptera: Muscidae). Systematic Parasitology, 86: 43–51.Google Scholar
Nores, A.I. 1995. Botfly ectoparasitism of the brown cacholote and the firewood-gatherer. The Wilson Bulletin, 107: 734–738.Google Scholar
O’Connor, J.A., Robertson, J., and Kleindorfer, S. 2010a. Video analysis of host-parasite interactions in nests of Darwin’s finches. Oryx, 44: 588–594.CrossRefGoogle Scholar
O’Connor, J., Sulloway, F., Robertson, J., and Kleindorfer, S. 2010b. Philornis downsi parasitism is the primary cause of nestling mortality in the critically endangered Darwin’s medium tree finch (Camarhynchus pauper). Biodiversity and Conservation, 19: 853–866.Google Scholar
Partridge, L., Prowse, N., and Pignatelli, P. 1999. Another set of responses and correlated responses to selection on age at reproduction in Drosophila melanogaster. Proceeding of the Royal Society of London B: Biological Sciences, 266: 255–261.Google Scholar
Patitucci, L.D., Quiroga, M., Couri, M.S., and Saravia-Pietropaolo, M.J. 2017. Oviposition in the bird parasitic fly Philornis torquans (Nielsen, 1913) (Diptera: Muscidae) and eggs’ adaptations to dry environments. Zoological Anzeiger, 267: 15–20.Google Scholar
Pinilla, Y.T., Patarroyo, M.A., and Bello, F.J. 2013. Sarconesiopsis magellanica (Diptera: Calliphoridae) life-cycle, reproductive and population parameters using different diets under laboratory conditions. Forensic Science International, 233: 380–386.CrossRefGoogle ScholarPubMed
Quiroga, M.A. and Reboreda, J.C. 2012. Lethal and sublethal effects of botfly (Philornis seguyi) parasitism on house wren (Troglodytes aedon) nestlings. The Condor, 114: 197–202.Google Scholar
Quiroga, M.A. and Reboreda, J.C. 2013. Sexual differences in life history traits of Philornis seguyi (Diptera: Muscidae) parasitizing house wrens (Troglodytes aedon). Annals of the Entomological Society of America, 106: 222–227.Google Scholar
Rabuffetti, F. and Reboreda, J.C. 2007. Early infestations by botflies (Philornis seguyi) survival and nesting success in chalk-browed mockingbirds (Mimus saturninus). The Auk, 124: 898–906.Google Scholar
Ribeiro, P.B., Vianna, E.E.S., Costa, P.R.P, and Scholl, P.J. 1993. Período de vida e capacidade de postura da Dermatobia hominis, em laboratório. Revista Brasileira de Parasitolgia Veterinária, Rio de Janeiro, 2: 29–31.Google Scholar
Salvador, S.A. and Bodrati, A. 2013. Aves víctimas del parasitismo de moscas del género Philornis en Argentina. Nuestras Aves, 58: 16–21.Google Scholar
Segura, L. and Reboreda, J.C. 2011. Botfly parasitism effects on nestling growth and mortality of red-crested cardinals. The Wilson Journal of Ornithology, 123: 107–115.Google Scholar
Skidmore, P. 1985. The biology of the Muscidae of the world. W. Junk Publishers, Dordrecht, The Netherlands.Google Scholar
Spalding, M.G., Mertins, J.W., Walsh, P.B., and Morin, K.C. 2002. Burrowing fly larvae (Philornis porteri) associated with mortality of eastern bluebirds in Florida. Journal of Wildlife Diseases, 38: 776–783.Google Scholar
Teixeira, D.M. 1999. Myasis caused by obligatory parasites. Ib. General observations on the biology of species of the genus Philornis Meinert, 1980 (Diptera, Muscidae). In Myiasis in man and animals in the Neotropical Region. Edited by J.H. Guimaraes and N. Papavero. Plêiade/Fundação de Amparo à Pesquisa do Estado de São Paulo, Sao Paulo, Brazil. Pp. 71–96.Google Scholar
Tirone, G., Parise, P.P., and Avancini, R.M.P. 1996. Ovarian development in Muscina stabulans (Diptera, Muscidae) on differents diets. Revista Brasileira de Entomologia, 40: 105–106.Google Scholar
Tower, J. and Arbeitman, M. 2009. The genetics of gender and life span. Journal of Biology, 8: 1–3.Google Scholar
Ullyett, G.C. 1950. Competition for food and allied phenomena in sheep-blowfly populations. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 234: 77–174.Google Scholar
Wolff, J.N. and Gemmell, N.J. 2013. Mitochondria, maternal inheritance, and asymmetric fitness: why males die younger. BioEssays, 35: 93–99.Google Scholar
Woolaver, L.G., Nichols, R.K., Morton, E.S., and Stutchbury, B.J. 2015. Breeding ecology and predictors of nest success in the critically endangered Ridgway’s hawk Buteo ridgwayi . Bird Conservation International, 25: 385–398.Google Scholar
Zwaan, B., Bijlsma, R., and Hoekstra, R.F. 1995. Direct selection on life span in Drosophila melanogaster . Evolution, 49: 649–659.Google Scholar