Parasite intensity is driven by temperature in a wild bird

10.24072/pcjournal.65 - Peer Community Journal, Volume 1 (2021), article no. e60.

Get full text PDF Peer reviewed and recommended by PCI

Increasing awareness that parasitism is an essential component of nearly all aspects of ecosystem functioning, as well as a driver of biodiversity, has led to rising interest in the consequences of climate change in terms of parasitism and disease spread. Yet empirical knowledge on the extent and ways in which climatic factors affect parasite prevalence and intensities remains scarce. In an 18-year, multi-site, correlative study we investigated the contributions of weather variables and other factors to spatio-temporal variation in infestation by blowfly parasitic larvae (Protocalliphora spp.) in nests of Corsican blue tits (Cyanistes caeruleus). We found that ambient temperature during the nestling stage is strongly and positively related to parasite load (number of parasites per chick), both across broods when controlling for year, and across years. In addition, annual mean parasite load also increased with minimal spring temperature, and decreased with increasing average temperature in the previous summer. There was no indication of a dependence of parasite dynamics on host dynamics in this system, likely due in part to the wide host range of blowflies that do not solely rely on blue tit hosts. This suggests a major effect of temperature during the blowfly life cycle, with potential implications for blowfly host interactions across their geographical range as climate keeps warming up. Finally, given that ambient temperature increases throughout the breeding season and that blowflies negatively affect survival and recruitment of blue tits, these results also mean that parasites, along with caterpillar availability, can drive selection for breeding date in this system.

Published online:
DOI: 10.24072/pcjournal.65
Mennerat, Adèle 1, 2; Charmantier, Anne 3; Perret, Philippe 3; Hurtrez-Boussès, Sylvie 4, 5; Lambrechts, Marcel M. 3

1 Department of Biological Sciences, University of Bergen, Norway
2 EDYSAN, Université de Picardie Jules Verne, CNRS, Amiens, France
3 CEFE, Univ Montpellier, CNRS, IRD, INRAE, Montpellier SupAgro, EPHE, Montpellier, France
4 Département de Biologie Écologie, Faculté des Sciences, Univ Montpellier, Montpellier, France
5 MIVEGEC, Univ Montpellier, CNRS, IRD, Montpellier, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Mennerat, Ad\`ele and Charmantier, Anne and Perret, Philippe and Hurtrez-Bouss\`es, Sylvie and Lambrechts, Marcel M.},
     title = {Parasite intensity is driven by temperature in a wild bird},
     journal = {Peer Community Journal},
     eid = {e60},
     publisher = {Peer Community In},
     volume = {1},
     year = {2021},
     doi = {10.24072/pcjournal.65},
     url = {}
AU  - Mennerat, Adèle
AU  - Charmantier, Anne
AU  - Perret, Philippe
AU  - Hurtrez-Boussès, Sylvie
AU  - Lambrechts, Marcel M.
TI  - Parasite intensity is driven by temperature in a wild bird
JO  - Peer Community Journal
PY  - 2021
DA  - 2021///
VL  - 1
PB  - Peer Community In
UR  -
UR  -
DO  - 10.24072/pcjournal.65
ID  - 10_24072_pcjournal_65
ER  - 
%0 Journal Article
%A Mennerat, Adèle
%A Charmantier, Anne
%A Perret, Philippe
%A Hurtrez-Boussès, Sylvie
%A Lambrechts, Marcel M.
%T Parasite intensity is driven by temperature in a wild bird
%J Peer Community Journal
%D 2021
%V 1
%I Peer Community In
%R 10.24072/pcjournal.65
%F 10_24072_pcjournal_65
Mennerat, Adèle; Charmantier, Anne; Perret, Philippe; Hurtrez-Boussès, Sylvie; Lambrechts, Marcel M. Parasite intensity is driven by temperature in a wild bird. Peer Community Journal, Volume 1 (2021), article  no. e60. doi : 10.24072/pcjournal.65.

Peer reviewed and recommended by PCI : 10.24072/pci.ecology.100012

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Altizer, S.; Ostfeld, R. S.; Johnson, P. T. J.; Kutz, S.; Harvell, C. D. Climate Change and Infectious Diseases: From Evidence to a Predictive Framework, Science, Volume 341 (2013) no. 6145, pp. 514-519 | DOI

[2] Andreasson, F.; Nord, A.; Nilsson, J.-Å. Experimentally increased nest temperature affects body temperature, growth and apparent survival in blue tit nestlings, Journal of Avian Biology, Volume 49 (2018) no. 2, pp. 1-14 | DOI

[3] Banbura, J. e. a. Sex differences in parental care in a Corsican Blue Tit Parus caeruleus population, Ardea, Volume 89 (2001), pp. 517-526

[4] Bańbura, J.; Perret, P.; Blondel, J.; Thomas, D. W.; Cartan-Son, M.; Lambrechts, M. M. Effects ofProtocalliphoraParasites on Nestling Food Composition in Corsican Blue TitsParus caeruleus: Consequences for Nestling Performance, Acta Ornithologica, Volume 39 (2004) no. 2, pp. 93-103 | DOI

[5] Bennett, G. F.; Whitworth, T. L. Studies on the life history of some species of Protocalliphora (Diptera: Calliphoridae), Canadian Journal of Zoology, Volume 69 (1991) no. 8, pp. 2048-2058 | DOI

[6] Blondel, J. Breeding Strategies of the Blue Tit and Coal Tit (Parus) in Mainland and Island Mediterranean Habitats: A Comparison, The Journal of Animal Ecology, Volume 54 (1985) no. 2, pp. 531-556 | DOI

[7] Blondel, J.; Thomas, D. W.; Charmantier, A.; Perret, P.; Bourgault, P.; Lambrechts, M. M. A Thirty-Year Study of Phenotypic and Genetic Variation of Blue Tits in Mediterranean Habitat Mosaics, BioScience, Volume 56 (2006) no. 8, pp. 661-673 | DOI

[8] Brooks, D. R.; Hoberg, E. P. How will global climate change affect parasite–host assemblages?, Trends in Parasitology, Volume 23 (2007) no. 12, pp. 571-574 | DOI

[9] Calosi, P.; Bilton, D. T.; Spicer, J. I.; Votier, S. C.; Atfield, A. What determines a species’ geographical range? Thermal biology and latitudinal range size relationships in European diving beetles (Coleoptera: Dytiscidae), Journal of Animal Ecology, Volume 79 (2010) no. 1, pp. 194-204 | DOI

[10] Cantarero, A.; López-Arrabé, J.; Redondo, A. J.; Moreno, J. Behavioural responses to ectoparasites in pied flycatchersFicedula hypoleuca: an experimental study, Journal of Avian Biology, Volume 44 (2013) no. 6, pp. 591-599 | DOI

[11] Castaño-Vázquez, F.; Martínez, J.; Merino, S.; Lozano, a. M. Experimental manipulation of temperature reduce ectoparasites in nests of blue titsCyanistes caeruleus, Journal of Avian Biology, Volume 49 (2018) no. 8, pp. 1-6 | DOI

[12] Charlier, J.; Ghebretinsae, A. H.; Levecke, B.; Ducheyne, E.; Claerebout, E.; Vercruysse, J. Climate-driven longitudinal trends in pasture-borne helminth infections of dairy cattle, International Journal for Parasitology, Volume 46 (2016) no. 13-14, pp. 881-888 | DOI

[13] Charmantier, A.; Kruuk, L. E. B.; Lambrechts, M. M. Parasitism reduces the potential for evolution in a wild bird population, Evolution, Volume 58 (2004) no. 1, pp. 203-206 | DOI

[14] Chown, S. L.; Nicolson, S. Insect Physiological Ecology, Oxford University Press, 2004 | DOI

[15] Christe, P.; Oppliger, A.; Richner, H. Ectoparasite affects choice and use of roost sites in the great tit, Parus major, Animal Behaviour, Volume 47 (1994) no. 4, pp. 895-898 | DOI

[16] Clayton, D. H.; Moore, J. Host parasite evolution: general principles and avian models ( D Clayton and J Moore , Eds.). - Oxford University Press., Oxford University Press, (1997)

[17] David, J. R.; Gibert, P.; Moreteau, B.; Gilchrist, G. W.; Huey, R. B. The fly that came in from the cold: geographic variation of recovery time from low-temperature exposure inDrosophila subobscura, Functional Ecology, Volume 17 (2003) no. 4, pp. 425-430 | DOI

[18] Dawson, R. D.; Hillen, K. K.; Whitworth, T. L. Effects of Experimental Variation in Temperature on Larval Densities of ParasiticProtocalliphora(Diptera: Calliphoridae) in Nests of Tree Swallows (Passeriformes: Hirundinidae), Environmental Entomology, Volume 34 (2005) no. 3, pp. 563-568 | DOI

[19] Descamps, S.; Blondel, J.; Lambrechts, M. M.; Hurtrez-Boussès, S.; Thomas, F. Asynchronous hatching in a blue tit population: a test of some predictions related to ectoparasites, Canadian Journal of Zoology, Volume 80 (2002) no. 8, pp. 1480-1484 | DOI

[20] Dudaniec, R. Y.; Fessl, B.; Kleindorfer, S. Interannual and interspecific variation in intensity of the parasitic fly, Philornis downsi, in Darwin’s finches, Biological Conservation, Volume 139 (2007) no. 3-4, pp. 325-332 | DOI

[21] Eads, D. A.; Hoogland, J. L. Factors that affect parasitism of black‐tailed prairie dogs by fleas, Ecosphere, Volume 7 (2016) no. 7 | DOI

[22] Eeva, T.; Lehikoinen, E.; Nurmi, J. Effects of ectoparasites on breeding success of great tits (Parus major) and pied flycatchers (Ficedula hypoleuca) in an air pollution gradient, Canadian Journal of Zoology, Volume 72 (1994) no. 4, pp. 624-635 | DOI

[23] Eeva, T.; Andersson, T.; Berglund, Å. M. M.; Brommer, J. E.; Hyvönen, R.; Klemola, T.; Laaksonen, T.; Loukola, O.; Morosinotto, C.; Rainio, K.; Sirkiä, P. M.; Vesterinen, E. J. Species and abundance of ectoparasitic flies (Diptera) in pied flycatcher nests in Fennoscandia, Parasites & Vectors, Volume 8 (2015) no. 1, pp. 1-9 | DOI

[24] Elderd, B. D.; Reilly, J. R. Warmer temperatures increase disease transmission and outbreak intensity in a host-pathogen system, Journal of Animal Ecology, Volume 83 (2014) no. 4, pp. 838-849 | DOI

[25] Enriquez, T.; Colinet, H. Basal tolerance to heat and cold exposure of the spotted wing drosophila,Drosophila suzukii, PeerJ, Volume 5 (2017) | DOI

[26] Feder, M. E.; Blair, N.; Figueras, H. Natural thermal stress and heat-shock protein expression in Drosophila larvae and pupae, Functional Ecology, Volume 11 (1997) no. 1, pp. 90-100 | DOI

[27] Grosbois, V.; Henry, P.-Y.; Blondel, J.; Perret, P.; Lebreton, J.-D.; Thomas, D. W.; Lambrechts, M. M. Climate impacts on Mediterranean blue tit survival: an investigation across seasons and spatial scales, Global Change Biology, Volume 12 (2006) no. 12, pp. 2235-2249 | DOI

[28] Harvell, C. D.; Mitchell, C. E.; Ward, J. R.; Altizer, S.; Dobson, A. P.; Ostfeld, R. S.; Samuel, M. D. Climate Warming and Disease Risks for Terrestrial and Marine Biota, Science, Volume 296 (2002) no. 5576, pp. 2158-2162 | DOI

[29] Heeb, P.; Werner, I.; Richner, H.; Kolliker, M. Horizontal Transmission and Reproductive Rates of Hen Fleas in Great Tit Nests, The Journal of Animal Ecology, Volume 65 (1996) no. 4, pp. 474-484 | DOI

[30] Heeb, P.; Kölliker, M.; Richner, H. Bird–ectoparasite interactions, nest humidity, and ectoparasite community structure, Ecology, Volume 81 (2000) no. 4, pp. 958-968 | DOI

[31] Hercus, M. J.; Berrigan, D.; Blows, M. W.; Magiafoglou, A.; Hoffmann, A. A. Resistance to temperature extremes between and within life cycle stages in Drosophila serrata, D. birchii and their hybrids: intraspecific and interspecific comparisons, Biological Journal of the Linnean Society, Volume 71 (2000) no. 3, pp. 403-416 | DOI

[32] Hernandez, A. D.; Poole, A.; Cattadori, I. M. Climate changes influence free-living stages of soil-transmitted parasites of European rabbits, Global Change Biology, Volume 19 (2013) no. 4, pp. 1028-1042 | DOI

[33] Hudson, P. J.; Dobson, A. P.; Lafferty, K. D. Is a healthy ecosystem one that is rich in parasites?, Trends in Ecology & Evolution, Volume 21 (2006) no. 7, pp. 381-385 | DOI

[34] Hurtrez-Boussès, S.; Perret, P.; Renaud, F.; Blondel, J. High blowfly parasitic loads affect breeding success in a Mediterranean population of blue tits, Oecologia, Volume 112 (1997) no. 4, pp. 514-517 | DOI

[35] Hurtrez-Bousses, S.; Blondel, J.; Perret, P.; Fabreguettes, J.; Renaud, F. R. Chick parasitism by blowflies affects feeding rates in a Mediterranean population of blue tits, Ecology Letters, Volume 1 (1998) no. 1, pp. 17-20 | DOI

[36] Hurtrez-Boussès, S.; Garine-Wichatitsky, M. d.; Perret, P.; Blondel, J.; Renaud, F. Variations in prevalence and intensity of blow fly infestations in an insular Mediterranean population of blue tits, Canadian Journal of Zoology, Volume 77 (1999) no. 2, pp. 337-341 | DOI

[37] Hurtrez-Boussès, S.; Renaud, F.; Blondel, J.; Perret, P.; Galan, M.-J. Effects of ectoparasites of young on parents’ behaviour in a Mediterranean population of Blue Tits, Journal of Avian Biology, Volume 31 (2000) no. 2, pp. 266-269 | DOI

[38] IPCC Annex I: Atlas of Global and Regional Climate Projections. - In: van Oldenborgh, G. J . et al. (eds), Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press., (2013)

[39] Jamriska, J. e. a. Host spectrum of bird blow flies of the genus Protocalliphora Hough , 1899 (Diptera , Calliphoridae) in Slovakia, Sylvia, Volume 46 (2010), pp. 125-132

[40] Jánošková, V.; Országh, I.; Jamriška, J.; Kopáni, M. Pre-imaginal stages of the blowfly <i>Protocalliphora falcozi</i> in nests of the tree sparrow (<i>Passer montanus</i>), Entomologica Fennica, Volume 21 (2010) no. 2, pp. 107-116 | DOI

[41] Khaliq, I.; Böhning-Gaese, K.; Prinzinger, R.; Pfenninger, M.; Hof, C. The influence of thermal tolerances on geographical ranges of endotherms, Global Ecology and Biogeography, Volume 26 (2017) no. 6, pp. 650-668 | DOI

[42] Kingsolver, J. G.; Buckley, L. B. Quantifying thermal extremes and biological variation to predict evolutionary responses to changing climate, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 372 (2017) no. 1723 | DOI

[43] Kleindorfer, S.; Dudaniec, R. Y. Love thy neighbour? Social nesting pattern, host mass and nest size affect ectoparasite intensity in Darwin’s tree finches, Behavioral Ecology and Sociobiology, Volume 63 (2009) no. 5, pp. 731-739 | DOI

[44] Lambrechts, M. M.; Caro, S.; Charmantier, A.; Gross, N.; Galan, M.-J.; Perret, P.; Cartan-Son, M.; Dias, P. C.; Blondel, J.; Thomas, D. W. Habitat quality as a predictor of spatial variation in blue tit reproductive performance: a multi-plot analysis in a heterogeneous landscape, Oecologia, Volume 141 (2004) no. 4, pp. 555-561 | DOI

[45] Loye, J.; Zuk, M. Bird - parasite interactions: ecology, evolution and behaviour, Oxford University Press, (1991)

[46] Marrot, P.; Garant, D.; Charmantier, A. Multiple extreme climatic events strengthen selection for earlier breeding in a wild passerine, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 372 (2017) no. 1723 | DOI

[47] Marrot, P.; Charmantier, A.; Blondel, J.; Garant, D. Current spring warming as a driver of selection on reproductive timing in a wild passerine, Journal of Animal Ecology, Volume 87 (2018) no. 3, pp. 754-764 | DOI

[48] Mas-Coma, S.; Valero, M. A.; Bargues, M. D. Climate change effects on trematodiases, with emphasis on zoonotic fascioliasis and schistosomiasis, Veterinary Parasitology, Volume 163 (2009) no. 4, pp. 264-280 | DOI

[49] Matyukhin, A. V.; Krivosheina, M. G. Contribution to the knowledge of Diptera (Insecta) parasitizing on birds, Entomological Review, Volume 88 (2008) no. 2, pp. 258-259 | DOI

[50] Mennerat, A.; Perret, P.; P. Caro, S.; Heeb, P.; M. Lambrechts, M. Aromatic plants in blue tit Cyanistes caeruleus nests: no negative effect on blood-sucking Protocalliphora blow fly larvae, Journal of Avian Biology, Volume 39 (2008) no. 2, pp. 127-132 | DOI

[51] Mennerat, A.; Mirleau, P.; Blondel, J.; Perret, P.; Lambrechts, M. M.; Heeb, P. Aromatic plants in nests of the blue tit Cyanistes caeruleus protect chicks from bacteria, Oecologia, Volume 161 (2009) no. 4, pp. 849-855 | DOI

[52] Merino, S.; Potti, J. Weather dependent effects of nest ectoparasites on their bird hosts, Ecography, Volume 19 (1996) no. 2, pp. 107-113 | DOI

[53] Møller, A. P.; Allander, K.; Dufva, R. Fitness Effects of Parasites on Passerine Birds: A Review, Population Biology of Passerine Birds, Springer Berlin Heidelberg, Berlin, Heidelberg, 1990, pp. 269-280 | DOI

[54] Møller, A. P.; Merino, S.; Soler, J. J.; Antonov, A.; Badás, E. P.; Calero-Torralbo, M. A.; de Lope, F.; Eeva, T.; Figuerola, J.; Flensted-Jensen, E.; Garamszegi, L. Z.; González-Braojos, S.; Gwinner, H.; Hanssen, S. A.; Heylen, D.; Ilmonen, P.; Klarborg, K.; Korpimäki, E.; Martínez, J.; Martínez-de la Puente, J.; Marzal, A.; Matthysen, E.; Matyjasiak, P.; Molina-Morales, M.; Moreno, J.; Mousseau, T. A.; Nielsen, J. T.; Pap, P. L.; Rivero-de Aguilar, J.; Shurulinkov, P.; Slagsvold, T.; Szép, T.; Szöllősi, E.; Török, J.; Vaclav, R.; Valera, F.; Ziane, N. Assessing the Effects of Climate on Host-Parasite Interactions: A Comparative Study of European Birds and Their Parasites, PLoS ONE, Volume 8 (2013) no. 12 | DOI

[55] Moreno, J.; Merino, S.; Lobato, E.; Ruiz-De-Castañeda, R.; Martínez-De La Puente, J.; Del Cerro, S.; Rivero-De Aguilar, J. Nest-dwelling ectoparasites of two sympatric hole-nesting passerines in relation to nest composition: An experimental study, Écoscience, Volume 16 (2009) no. 3, pp. 418-427 | DOI

[56] Ogden, N. H.; Lindsay, L. R. Effects of Climate and Climate Change on Vectors and Vector-Borne Diseases: Ticks Are Different, Trends in Parasitology, Volume 32 (2016) no. 8, pp. 646-656 | DOI

[57] Owen, D.; Ash, J. Additional records of Protocalliphora (Diptera) in birds’ nests. - Br. Birds XLVIII: 225–229., British Birds, Volume XLVIII (1955), pp. 225-229

[58] Porlier, M.; Charmantier, A.; Bourgault, P.; Perret, P.; Blondel, J.; Garant, D. Variation in phenotypic plasticity and selection patterns in blue tit breeding time: between- and within-population comparisons, Journal of Animal Ecology, Volume 81 (2012) no. 5, pp. 1041-1051 | DOI

[59] Potti, J. Blowfly Infestation at the Nestling Stage Affects Egg Size in the Pied FlycatcherFicedula hypoleuca, Acta Ornithologica, Volume 43 (2008) no. 1, pp. 76-82 | DOI

[60] Remeš, V.; Krist, M. Nest design and the abundance of parasiticProtocalliphorablow flies in two hole-nesting passerines, Écoscience, Volume 12 (2005) no. 4, pp. 549-553 | DOI

[61] Rohr, J. R.; Dobson, A. P.; Johnson, P. T.; Kilpatrick, A. M.; Paull, S. H.; Raffel, T. R.; Ruiz-Moreno, D.; Thomas, M. B. Frontiers in climate change–disease research, Trends in Ecology & Evolution, Volume 26 (2011) no. 6, pp. 270-277 | DOI

[62] Roiz, D.; Ruiz, S.; Soriguer, R.; Figuerola, J. Climatic effects on mosquito abundance in Mediterranean wetlands, Parasites & Vectors, Volume 7 (2014) no. 1 | DOI

[63] Rose, H.; Hoar, B.; Kutz, S. J.; Morgan, E. R. Exploiting parallels between livestock and wildlife: Predicting the impact of climate change on gastrointestinal nematodes in ruminants, International Journal for Parasitology: Parasites and Wildlife, Volume 3 (2014) no. 2, pp. 209-219 | DOI

[64] Simon, A.; Thomas, D.; Blondel, J.; Perret, P.; Lambrechts, M. M. Physiological Ecology of Mediterranean Blue Tits (Parus caeruleus L.): Effects of Ectoparasites (Protocalliphora spp.) and Food Abundance on Metabolic Capacity of Nestlings, Physiological and Biochemical Zoology, Volume 77 (2004) no. 3, pp. 492-501 | DOI

[65] Simon, A.; Thomas, D. W.; Speakman, J. R.; Blondel, J.; Perret, P.; Lambrechts, M. M. Impact of ectoparasitic blowfly larvae (Protocalliphora spp.) on the behavior and energetics of nestling Blue Tits, Journal of Field Ornithology, Volume 76 (2005) no. 4, pp. 402-410 | DOI

[66] Stromberg, B. E. Environmental factors influencing transmission, Veterinary Parasitology, Volume 72 (1997) no. 3-4, pp. 247-264 | DOI

[67] Thomas, D. W.; Shipley, B.; Blondel, J.; Perret, P.; Simon, A.; Lambrechts, M. M. Common paths link food abundance and ectoparasite loads to physiological performance and recruitment in nestling blue tits, Functional Ecology, Volume 21 (2007) no. 5, pp. 947-955 | DOI

[68] Noordwijk, A. V.; McCleery, R.; Perrins, C. Selection for the Timing of Great Tit Breeding in Relation to Caterpillar Growth and Temperature, The Journal of Animal Ecology, Volume 64 (1995) no. 4, pp. 451-458 | DOI

[69] Visser, M. E.; Holleman, L. J. M.; Gienapp, P. Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird, Oecologia, Volume 147 (2006) no. 1, pp. 164-172 | DOI

[70] Wesołowski, T. Host–parasite interactions in natural holes: marsh tits ( Parus palustris ) and blow flies ( Protocalliphora falcozi ), Journal of Zoology, Volume 255 (2001) no. 4, pp. 495-503 | DOI

Cited by Sources: