Open Access
How to translate text using browser tools
1 December 2004 Effects of Protocalliphora Parasites on Nestling Food Composition in Corsican Blue Tits Parus caeruleus: Consequences for Nestling Performance
Jerzy Bańbura, Philippe Perret, Jacques Blondel, Donald W. Thomas, Mireille Cartan-Son, Marcel M. Lambrechts
Author Affiliations +

The influence of a parasite (larvae of Protocalliphora, Diptera: Calliphoridae) on an avian host (Blue Tit) was studied in 1994–1997 as part of a long-term research project on a population of Blue Tits inhabiting nest boxes on the island of Corsica. The Blue Tit broods were heavily infested with Protocalliphora larvae. The abundance of caterpillars as a key food type for the tits was monitored. A random sample of 16 nests was experimentally subjected to an anti-parasite heat treatment, which resulted in a marked decline in the numbers of Protocalliphora larvae. Untreated nests, with high numbers of parasites, were regarded as control nests. Under the anti-parasite treatment, Blue Tit nestlings were fed less frequently than the control nestlings (8 v. 11 food items per hour per nestling). Significant changes in the diet composition occurred, with parasite-free nestlings being consistently fed with fewer caterpillars. An average parasitised nestling was supplied by its parents with 2.6 caterpillars more than an average parasite-free chick. This suggests that in the highly parasitised control nests, the parent tits made an effort to compensate for the detrimental effects caused by Protocalliphora larvae. Feeding rate and food composition were shown to influence chick condition and survival in the nest. In spite of these facts, the nestlings in parasitised nests developed less rapidly and had lower survival rates than in the anti-parasitically heat-treated nests. The parasitic Protocalliphora larvae have a double effect on their avian host: they adversely affect nestling performance, and they compel adult tits to work harder in order to at least partially compensate for that influence.



K. Allander 1998. The effects of an ectoparasite on reproductive success in the great tit: a 3-year experimental study. Can. J. Zool. 76: 19–25. Google Scholar


J. Bańbura , J. Blondel , H. de Wilde-Lambrechts , M.J. Galan , M. Maistre 1994. Nestling diet variation an insular Mediterranean population of Blue Tits Parus caeruleus: effects of years, territories and individuals. Oecologia 100: 413–20. Google Scholar


J. Bańbura , M. M. Lambrechts , J. Blondel , P. Perret , M. Cartan-Son 1999. Food handling time of Blue Tit chicks: constraints and adaptation to different prey types. J. Avian Biol. 30: 263–270. Google Scholar


J. Bańbura , P. Perret , J. Blondel , A. Sauvages , M.-J. Galan , M. M. Lambrechts 2001. Sex differences in parental care in a Corsican Blue Tit Parus caeruleus population. Ardea 89: 517–526. Google Scholar


J. Blondel 1985. Breeding strategies of the Blue Tit and Coal Tit (Parus) in mainland and island Mediterranean habitats: a comparison. J. Anim. Ecol. 54: 531–556. Google Scholar


J. Blondel , A. Dervieux , M. Maistre , P. Perret 1991. Feeding ecology and life history variation of the Blue Tit in Mediterranean deciduous and sclerophyllous habitats. Oecologia 88: 9–14. Google Scholar


J. Blondel , P. Dias , M. Maistre , P. Perret 1993. Habitat heterogeneity and life history variation of Mediterranean Blue Tits (Parus caeruleus). Auk 110: 511–520. Google Scholar


J. Blondel , P. Dias , M. Maistre , P. Perret , S. Hurtrez-Boussès , M. M. Lambrechts 1998. Is small clutch size of a Corsican blue tit population optimal? Oecologia 117: 80–89. Google Scholar


J. Blondel , P. Dias , P. Perret , M. Maistre , M. M. Lambrechts 1999. Selection-based biodiversity at a small spatial scale in a low-dispersing insular bird. Science 285: 1399–1402. Google Scholar


J. Blondel , R. Pradel , J.-D. Lebreton 1992. Low fecundity insular blue tits do not survive better as adults than high fecundity mainland ones. J. Anim. Ecol. 61: 205–213. Google Scholar


Z. Bouslama , Y. Chabi , M. M. Lambrechts 2001. Chicks resist high parasite intensities in an Algerian population of blue tit. Ecoscience 8: 320–324. Google Scholar


Z. Bouslama , M. M. Lambrechts , N. Ziane , R. Djenidi , Y. Chabi 2002. The effect of nest ectoparasites on parental provisioning in a North-African population of the Blue Tit Parus caeruleus.Ibis 144: 73–78. Google Scholar


P. Christe , H. Richner , A. Opplinger 1996a. Of great tits and fleas: sleep baby sleep… Anim. Behav. 52: 1087–1092. Google Scholar


P. Christe , H. Richner , A. Opplinger 1996b. Begging, food provisioning, and nestling competition in great tits infested with parasites. Behav. Ecol. 7: 127–131. Google Scholar


D. H. Clayton , J. Moore (eds). 1997. Host-parasite evolution — general principles and avian models. Oxford Univ. Press. Google Scholar


C. Combes 2001. Parasitism. The ecology and evolution of intimate interactions. Chicago Univ. Press. Google Scholar


M. J. Crawley 1993. GLIM for Ecologists. Blackwells, Oxford. Google Scholar


A. Draber-Mońko 2004. [Calliphoridae Blowflies (Insecta: Diptera)]. Fundacja Natura Optima Dux, Warszawa. Google Scholar


R. Dufva , K. Allander 1996. Variable effects of the Hen Flea Ceratophyllus gallinae on the breeding success of the Great Tit Parus major in relation to weather conditions. Ibis 138: 772–777. Google Scholar


C. S. Gold , D. L. Dahlsten 1983. Effects of parasitic flies (Protocalliphora ssp.) on nestlings of mountain and chestnut-backed chickadees. Wilson Bull. 95: 560–572. Google Scholar


F. Grieco 1999. Prey selection in Blue Tits Parus caeruleus as a response to food levels. Acta Ornithol. 34: 199–203. Google Scholar


F. Grieco 2002. Time constraint on food choice in provisioning blue tits, Parus caeruleus: the relationship between feeding rate and prey size. Anim. Behav. 64: 517–526. Google Scholar


S. Hurtrez-Bousses , J. Blondel , P. Perret , J. Fabreguettes , F. Renaud 1998. Chick parasitism by blowflies affects feeding rates in a Mediterranean population of Blue Tits. Ecol. Lett. 1: 17–20. Google Scholar


S. Hurtrez-Boussès , J. Blondel , P. Perret , F. Renaud 1997a. Relationship between intensity of blowfly infestation and reproductive success in a Corsican population of Blue Tits. J. Avian Biol. 28: 267–270. Google Scholar


S. Hurtrez-Boussès , M. de Garine-Wichatitsky , P. Perret , J. Blondel , F. Renaud 1999. Variations in prevalence and intensity of blow fly infestations in an insular Mediterranean population of blue tits. Can. J. Zool. 77: 337–341. Google Scholar


S. Hurtrez-Boussès , P. Perret , F. Renaud , J. Blondel 1997b. High blowfly parasitic loads affect breeding success in a Mediterranean population of Blue Tits. Oecologia 112: 514–517. Google Scholar


S. Hurtrez-Boussès , F. Renaud , J. Blondel , P. Perret , M.-J. Galan 2000. Effects of ectoparasites of young on parents' behaviour in a Mediterranean population of Blue Tits. J. Avian Biol. 31: 266–269. Google Scholar


F. C. James , C. E. McCulloch 1990. Multivariate analysis in ecology and systematics: panacea or Pandora's box. Ann. Rev. Ecol. Syst. 21: 129–166. Google Scholar


L. S. Johnson , D. J. Albrecht 1993. Effects of haematophagous ectoparasites on nestling house wrens, Troglodytes aedon: who pays the cost of parasitism? Oikos 6: 255–262. Google Scholar


A. H. Kędra , A. G Kruszewicz , T. D. Mazgajski , E. Modlińska 1996. The effects of the presence of fleas in nestboxes on fledglings of pied flycatchers and great tits. Acta Parasitol. 41: 211–213. Google Scholar


L. Lafuma , M. M. Lambrechts , M. Raymond 2001. Aromatic plants in bird nests as a protection against blood-sucking flying insects? Behav. Proc. 56: 113–120. Google Scholar


M. M. Lambrechts , Santos A. Dos 2001. Aromatic herbs in Corsican blue tit nests: The “Potpourri” hypothesis. Acta Oecol. 21: 175–178. Google Scholar


J. E. Loye , M. Zuk (eds). 1991. Bird-parasite interactions — ecology, evolution, and behaviour. Oxford Univ. Press. Google Scholar


T. D. Mazgajski , A. H. Kędra 1997. Are nestlings of hole-nesting birds affected by ectoparasites? A review. Wiadomości Parazytologiczne 43: 347–355. Google Scholar


T. D. Mazgajski , A. H. Kędra , E. Modlinska , J. Samborski 1997. Fleas Siphonaptera influence the condition of Starling Sturnus vulgaris nestlings. Acta Ornithol. 32: 185–190. Google Scholar


S. Merino , J. Potti 1995. Mites and blow flies decrease growth and survival in nestling pied flycatchers. Oikos 73: 95–103. Google Scholar


S. Merino , J. Potti 1996. Weather dependent effects of nest ectoparasites on their bird hosts. Ecography 19: 107–113. Google Scholar


B. L. Morrison , L. S. Johnson 2002. Feeding of House Wren nestling afflicted by hematophagous ectoparasites: a test of the parental compensation hypothesis. Condor 104:183–187. Google Scholar


L. Naef-Daenzer , B. Naef-Daenzer , R. G. Nager 2000. Prey selection and foraging performance of breeding Great Tits Parus major in relation to food availability. J. Avian Biol. 31: 206–214. Google Scholar


E. L. O'Brien , B. L. Morrison , L. S. Johnson 2001. Assessing the effects of haematophagous ectoparasites on the health of nestling birds: haematocrit vs haemoglobin levels in House Wrens parasitized by blow fly larvae. J. Avian Biol. 32: 73–76. Google Scholar


C. M. Perrins 1965. Population fluctuations and clutch size in the Great Tit Parus major L. J. Anim. Ecol. 34: 601–647. Google Scholar


C. M. Perrins 1970. The timing of birds' breeding seasons. Ibis 112: 242–255. Google Scholar


C. M. Perrins 1991. Tits and their caterpillar food supply. Ibis 133 Suppl.: 49–54. Google Scholar


C. M. Perrins , R. H. McCleery 2001. The effect of fledging mass on the lives of great tits Parus major.Ardea 89: 135–142. Google Scholar


C. Petit , M. Hossaert-McKey , P. Perret , J. Blondel , M. M. Lambrechts 2002. Blue tits use plants and olfaction to maintain an aromatic environment for nestlings. Ecol. Lett. 5: 585–589. Google Scholar


H. Richner 1998. Host-parasite interactions and life-history evolution. Zoology 101: 333–344. Google Scholar


H. Richner , A. Oppliger , P. Christe 1993. Effect of an ectoparasite on reproduction in great tits. J. Anim. Ecol. 62: 703–710. Google Scholar


H. Richner , F. Tripet 1999. Ectoparasitism and the tradeoff between current and future reproduction. Oikos 78: 557–561. Google Scholar


R. Riddington , A. G. Gosier 1995. Differences in reproductive success and parental qualities between habitats in the Great Tit Parus major. Ibis 137: 371–378. Google Scholar


M. Rothschild , T. Clay 1952. Fleas, Flukes and Cuckoos — A Study of Bird Parasites. Collins, London. Google Scholar


C. W. Sabrosky , G. F. Bennett , T. L. Whitworth 1989. Bird blowflies (Protocalliphora) (Diptera: Calliphoridae) in North America with notes on the Palearctic species. Smithsonian Institution Press, Washington. Google Scholar


A. Simon 2003. Conséquences écophysiologiques et évolutives de l'ectoparasite Protocalliphora sur la Mésange Bleue en Corse. PhD Thesis, Université de Sherbrooke, Sherbrooke, Canada. Google Scholar


A. Simon , D. W. Thomas , J. Blondel , M. M. Lambrechts , P. Perret 2003. Within-brood distribution of ectoparasite attacks on nestling blue tits: a test of the tasty chick hypothesis using inulin as a tracer. Oikos 102: 551–558. Google Scholar


A. Simon , D. W. Thomas , J. Blondel , P. Perret , M. M. Lambrechts 2004. Physiological ecology of Mediterranean Blue Tits (Parus caeruleus L.): Effects of ectoparasites (Protocalliphora spp.) and food abundance on metabolic capacity of nestlings. Physiol. Bioch. Zoology 77: 492–501. Google Scholar


R. R. Sokal , F. J. Rohlf 1995. Biometry. 3rd ed. Freeman, New York. Google Scholar


StatSoft. 1996. S TATISTICA for Windows Manual. StatSoft, Inc, Tulusa. Google Scholar


J. M. Tinbergen , M. C. Boerlijst 1990. Nestling weight and survival in individual Great Tits Parus major. J. Anim. Ecol. 59: 1113–1128. Google Scholar


L Tremblay , D. W. Thomas , M. M. Lambrechts , J. Blondel , P. Perret 2003. Variation in Blue Tit breeding performance across gradients in habitat richness. Ecology 84: 3033–3043. Google Scholar


F. Tripet , M. Glaser , H. Richner 2002. Behavioural responses to ectoparasites: time-budget adjustments and what matters to Blue Tits Parus caeruleus infested by fleas. Ibis 144: 461–69. Google Scholar


F. Tripet , H. Richner 1997. Host responses to ectoparasites: food compensation by parent blue tits. Oikos 78: 557–561. Google Scholar


J. H. van Balen 1973. A comparative study of the breeding ecology of the Great Tit Parus major in different habitats. Ardea 61: 1–93. Google Scholar


T. Wesołowski 2001. Host-parasite interactions in natural holes: marsh tits (Parus palustris) and blow flies (Protocalliphora falcozi). J. Zool. 255: 495–503. Google Scholar


T. L. Whitworth , G. F. Bennett 1992. Pathogenicity of larval Protocalliphora (Diptera: Calliphoridae) parasitizing nestling birds. Can. J. Zool. 70: 2184-2191. Google Scholar
Jerzy Bańbura, Philippe Perret, Jacques Blondel, Donald W. Thomas, Mireille Cartan-Son, and Marcel M. Lambrechts "Effects of Protocalliphora Parasites on Nestling Food Composition in Corsican Blue Tits Parus caeruleus: Consequences for Nestling Performance," Acta Ornithologica 39(2), 93-103, (1 December 2004).
Received: 1 March 2004; Accepted: 1 September 2004; Published: 1 December 2004
Blue Tit
food composition
nestling performance
Parental care
Back to Top