Section: Ecology
Topic: Ecology, Population biology, Environmental sciences

Identifying drivers of spatio-temporal variation in survival in four blue tit populations

Bastianelli, Olivier1, 2; Robert, Alexandre2; Doutrelant, Claire1 ; de Franceschi, Christophe1; Giovannini, Pablo1; Charmantier, Anne1  
1 CEFE, Univ Montpellier, CNRS, EPHE, IRD, Montpellier, France
2 Centre d'Ecologie et des Sciences de la Conservation (CESCO), Muséum national d'Histoire naturelle, Centre National de la Recherche Scientifique (CNRS), Sorbonne Université, CP 135, 57 rue Cuvier 75005 Paris, France

Corresponding author(s): Charmantier, Anne (anne.charmantier@cefe.cnrs.fr)

10.24072/pcjournal.17 - Peer Community Journal, Volume 1 (2021), article no. e11.

Get full text PDF Peer reviewed and recommended by PCI
article image

In a context of rapid climate change, the influence of large-scale and local climate on population demography is increasingly scrutinized, yet studies are usually focused on one population. Demographic parameters, including survival, can vary significantly across populations of a given species, depending on global or local climatic fluctuations but also on many other population-specific parameters such as breeding density, habitat naturalness, predation or parasitism. Such ecological differences between populations could lead to different paces-of-life (POL), whereby populations where individuals display higher reproductive investment and bolder behaviours would have lower survival probabilities. We use here long-term (19 to 38 years) monitoring datasets from four Mediterranean populations of blue tits (Cyanistes caeruleus) to investigate the effects of sex, age class, large-scale and local climate temporal variation and population breeding density, on adult survival, using Capture-Mark-Recapture modelling. Environment heterogeneity in these four populations (two in evergreen and two in deciduous forests) has been linked to strong multi-trait phenotypic variation, suggesting blue tits in deciduous forests display faster POL compared to their conspecifics in evergreen habitats. The present results show heterogeneity in average survival probabilities across the four populations, with, as predicted, lower survival in the fast blue tits occupying deciduous habitats. Interestingly, the year-to-year variation in survival probabilities was synchronous among populations. This suggests that regional environmental conditions could drive survival fluctuations across populations. However, breeding densities were not correlated across populations, and we found no evidence that adult survival is correlated with either large-scale or local, climate temporal variation in these four blue tit populations. Finally, two of the focal populations displayed a linear temporal decrease in adult survival over the study period, calling for further investigation to explain this decline. Overall, this multi-site study shows that blue tit parental survival from one spring to the next can vary substantially across years, in a synchronous way across populations, yet the climate indices we used are not correlated with the temporal variation. This calls for further investigations in other potential drivers such as resource (in particular insect) abundance, predation or parasitism.

Published online:
DOI: 10.24072/pcjournal.17
Type: Research article

Bastianelli, Olivier 1, 2; Robert, Alexandre 2; Doutrelant, Claire 1; de Franceschi, Christophe 1; Giovannini, Pablo 1; Charmantier, Anne 1

1 CEFE, Univ Montpellier, CNRS, EPHE, IRD, Montpellier, France
2 Centre d'Ecologie et des Sciences de la Conservation (CESCO), Muséum national d'Histoire naturelle, Centre National de la Recherche Scientifique (CNRS), Sorbonne Université, CP 135, 57 rue Cuvier 75005 Paris, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
@article{10_24072_pcjournal_17,
     author = {Bastianelli, Olivier and Robert, Alexandre and Doutrelant, Claire and de Franceschi, Christophe and Giovannini, Pablo and Charmantier, Anne},
     title = {Identifying drivers of spatio-temporal variation in survival in four blue tit populations},
     journal = {Peer Community Journal},
     eid = {e11},
     publisher = {Peer Community In},
     volume = {1},
     year = {2021},
     doi = {10.24072/pcjournal.17},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.17/}
}
TY  - JOUR
AU  - Bastianelli, Olivier
AU  - Robert, Alexandre
AU  - Doutrelant, Claire
AU  - de Franceschi, Christophe
AU  - Giovannini, Pablo
AU  - Charmantier, Anne
TI  - Identifying drivers of spatio-temporal variation in survival in four blue tit populations
JO  - Peer Community Journal
PY  - 2021
VL  - 1
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.17/
DO  - 10.24072/pcjournal.17
ID  - 10_24072_pcjournal_17
ER  - 
%0 Journal Article
%A Bastianelli, Olivier
%A Robert, Alexandre
%A Doutrelant, Claire
%A de Franceschi, Christophe
%A Giovannini, Pablo
%A Charmantier, Anne
%T Identifying drivers of spatio-temporal variation in survival in four blue tit populations
%J Peer Community Journal
%D 2021
%V 1
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.17/
%R 10.24072/pcjournal.17
%F 10_24072_pcjournal_17
Bastianelli, Olivier; Robert, Alexandre; Doutrelant, Claire; de Franceschi, Christophe; Giovannini, Pablo; Charmantier, Anne. Identifying drivers of spatio-temporal variation in survival in four blue tit populations. Peer Community Journal, Volume 1 (2021), article  no. e11. doi : 10.24072/pcjournal.17. https://peercommunityjournal.org/articles/10.24072/pcjournal.17/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.ecology.100085

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] Alves, J. A.; Gunnarsson, T. G.; Sutherland, W. J.; Potts, P. M.; Gill, J. A. Linking warming effects on phenology, demography, and range expansion in a migratory bird population, Ecology and Evolution, Volume 9 (2019) no. 5, pp. 2365-2375 | DOI

[2] André, J.-B.; Rousset, F. Does extrinsic mortality accelerate the pace of life? A bare-bones approach, Evolution and Human Behavior, Volume 41 (2020) no. 6, pp. 486-492 | DOI

[3] Banbura, J.; Perret, P.; Blondel, J.; Sauvages, A.; Galan, M. J.; Lambrechts, M. M. Sex differences in parental care in a Corsican Blue Tit Parus caeruleus population, Ardea, Volume 89 (2001)

[4] Barbraud, C.; Weimerskirch, H. Climate and density shape population dynamics of a marine top predator, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 270 (2003) no. 1529, pp. 2111-2116 | DOI

[5] Blondel, J.; Dervieux, A.; Maistre, M.; Perret, P. Feeding ecology and life history variation of the blue tit in Mediterranean deciduous and sclerophyllous habitats, Oecologia, Volume 88 (1991) no. 1, pp. 9-14 | DOI

[6] Blondel, J.; Pradel, R.; Lebreton, J.-D. Low Fecundity Insular Blue Tits Do Not Survive Better as Adults than High Fecundity Mainland Ones, The Journal of Animal Ecology, Volume 61 (1992) no. 1 | 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 | DOI

[8] Bonamour, S.; Chevin, L.-M.; Charmantier, A.; Teplitsky, C. Phenotypic plasticity in response to climate change: the importance of cue variation, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 374 (2019) no. 1768 | DOI

[9] Bouwhuis, S.; Choquet, R.; Sheldon, B. C.; Verhulst, S. The Forms and Fitness Cost of Senescence: Age-Specific Recapture, Survival, Reproduction, and Reproductive Value in a Wild Bird Population, The American Naturalist, Volume 179 (2012) no. 1 | DOI

[10] BURKE, D. M.; ELLIOTT, K.; MOORE, L.; DUNFORD, W.; NOL, E.; PHILLIPS, J.; HOLMES, S.; FREEMARK, K. Patterns of Nest Predation on Artificial and Natural Nests in Forests, Conservation Biology, Volume 18 (2004) no. 2, pp. 381-388 | DOI

[11] Burnham, K. P.; Anderson, D. R. Practical Use of the Information-Theoretic Approach, Model Selection and Inference, Springer New York, New York, NY, 1998, pp. 75-117 | DOI

[12] Cartwright, S. J.; Nicoll, M. A.; Jones, C. G.; Tatayah, V.; Norris, K. Anthropogenic Natal Environmental Effects on Life Histories in a Wild Bird Population, Current Biology, Volume 24 (2014) no. 5, pp. 536-540 | DOI

[13] Chang-Yang, C.-H.; Sun, I.-F.; Tsai, C.-H.; Lu, C.-L.; Hsieh, C.-F. ENSO and frost codetermine decade-long temporal variation in flower and seed production in a subtropical rain forest, Journal of Ecology, Volume 104 (2016) no. 1, pp. 44-54 | DOI

[14] Charmantier, A.; Blondel, J.; Perret, P.; Harmelin-Vivien, M. Tracing site-specific isotopic signatures along a Blue TitCyanistes caeruleusfood chain, Ibis, Volume 156 (2014) no. 1, pp. 165-175 | DOI

[15] Charmantier, A.; Doutrelant, C.; Dubuc-Messier, G.; Fargevieille, A.; Szulkin, M. Mediterranean blue tits as a case study of local adaptation, Evolutionary Applications, Volume 9 (2016) no. 1, pp. 135-152 | DOI

[16] Chevin, L.-M.; Collins, S.; Lefèvre, F. Phenotypic plasticity and evolutionary demographic responses to climate change: taking theory out to the field, Functional Ecology, Volume 27 (2013) no. 4, pp. 967-979 | DOI

[17] Choquet, R.; Lebreton, J.-D.; Gimenez, O.; Reboulet, A.-M.; Pradel, R. U-CARE: Utilities for performing goodness of fit tests and manipulating CApture-REcapture data, Ecography, Volume 32 (2009) no. 6, pp. 1071-1074 | DOI

[18] Choquet, R.; Rouan, L.; Pradel, R. Program E-Surge: A Software Application for Fitting Multievent Models, Modeling Demographic Processes In Marked Populations, Springer US, Boston, MA, 2009, pp. 845-865 | DOI

[19] Class, B.; Kluen, E.; Brommer, J. E. Evolutionary quantitative genetics of behavioral responses to handling in a wild passerine, Ecology and Evolution, Volume 4 (2014) no. 4, pp. 427-440 | DOI

[20] Clutton-Brock, T.; Isvaran, K. Sex differences in ageing in natural populations of vertebrates, Proceedings of the Royal Society B: Biological Sciences, Volume 274 (2007) no. 1629, pp. 3097-3104 | DOI

[21] Conte, M.; Giuffrida, A.; Tedesco, S. The Mediterranean oscillation: impact on precipitation and hydrology in Italy, Publications of the Academy of Finland, Helsinki, 1989

[22] Cuervo, J. J.; Møller, A. P. Temporal Variation in Population Size of European Bird Species: Effects of Latitude and Marginality of Distribution, PLoS ONE, Volume 8 (2013) no. 10 | DOI

[23] Fisman, D. N.; Hauck, T. S.; Tuite, A. R.; Greer, A. L. An IDEA for Short Term Outbreak Projection: Nearcasting Using the Basic Reproduction Number, PLoS ONE, Volume 8 (2013) no. 12 | DOI

[24] Culina, A.; Lachish, S.; Sheldon, B. C. Evidence of a link between survival and pair fidelity across multiple tit populations, Journal of Avian Biology, Volume 46 (2015) no. 5, pp. 507-515 | DOI

[25] Dalgleish, H. J.; Koons, D. N.; Hooten, M. B.; Moffet, C. A.; Adler, P. B. Climate influences the demography of three dominant sagebrush steppe plants, Ecology, Volume 92 (2011) no. 1, pp. 75-85 | DOI

[26] DeCesare, N. J.; Hebblewhite, M.; Bradley, M.; Hervieux, D.; Neufeld, L.; Musiani, M. Linking habitat selection and predation risk to spatial variation in survival, Journal of Animal Ecology, Volume 83 (2014) no. 2, pp. 343-352 | DOI

[27] DHONDT, A. A.; KEMPENAERS, B.; CLOBERT, J. Sparrowhawk Accipiter nisus predation and Blue Tit Parus caeruleus adult annual survival rate, Ibis, Volume 140 (2008) no. 4, pp. 580-584 | DOI

[28] DHONDT, A. A. Reproduction and survival of polygynous and monogamous Blue Tit Parus caeruleus, Ibis, Volume 129 (1987) no. 2, pp. 327-334 | DOI

[29] Dijkstra, C.; Daan, S.; Tinbergen, J. M. Family Planning in the Kestrel (Falco Tinnunculus): the Ultimate Control of Covariation of Laying Date and Clutch Size, Behaviour, Volume 114 (1990) no. 1-4, pp. 83-116 | DOI

[30] Dubuc-Messier, G.; Réale, D.; Perret, P.; Charmantier, A. Environmental heterogeneity and population differences in blue tits personality traits, Behavioral Ecology, Volume 28 (2017) | DOI

[31] Dubuc-Messier, G.; Caro, S. P.; Perrier, C.; van Oers, K.; Réale, D.; Charmantier, A. Gene flow does not prevent personality and morphological differentiation between two blue tit populations, Journal of Evolutionary Biology, Volume 31 (2018) no. 8, pp. 1127-1137 | DOI

[32] Fay, R.; Weimerskirch, H.; Delord, K.; Barbraud, C. Population density and climate shape early-life survival and recruitment in a long-lived pelagic seabird, Journal of Animal Ecology, Volume 84 (2015) no. 5, pp. 1423-1433 | DOI

[33] Frederiksen, M.; Bregnballe, T. Evidence for density-dependent survival in adult cormorants from a combined analysis of recoveries and resightings, Journal of Animal Ecology, Volume 69 (2000) no. 5, pp. 737-752 | DOI

[34] Galipaud, M.; Kokko, H. Adaptation and plasticity in life-history theory: How to derive predictions., Evolution and Human Behavior, Volume 41 (2020) no. 6, pp. 493-501 | DOI

[35] Gamelon, M.; Grøtan, V.; Nilsson, A. L. K.; Engen, S.; Hurrell, J. W.; Jerstad, K.; Phillips, A. S.; Røstad, O. W.; Slagsvold, T.; Walseng, B.; Stenseth, N. C.; Sæther, B.-E. Interactions between demography and environmental effects are important determinants of population dynamics, Science Advances, Volume 3 (2017) no. 2 | DOI

[36] García-Navas, V.; Ferrer, E. S.; Sanz, J. J. Prey selectivity and parental feeding rates of Blue Tits Cyanistes caeruleus in relation to nestling age, Bird Study, Volume 59 (2012) no. 2, pp. 236-242 | DOI

[37] García-Navas, V.; Ferrer, E. S.; Sanz, J. J.; Ortego, J. The role of immigration and local adaptation on fine-scale genotypic and phenotypic population divergence in a less mobile passerine, Journal of Evolutionary Biology, Volume 27 (2014) no. 8, pp. 1590-1603 | DOI

[38] Garcia-Navas, V.; Sanz, J. J. Environmental and Within-Nest Factors Influencing Nestling-Feeding Patterns of Mediterranean Blue Tits (Cyanistes caeruleus), The Condor, Volume 114 (2012) no. 3, pp. 612-621 | DOI

[39] Griffith, S. C.; Ornborg, J.; Russell, A. F.; Andersson, S.; Sheldon, B. C. Correlations between ultraviolet coloration, overwinter survival and offspring sex ratio in the blue tit, Journal of Evolutionary Biology, Volume 16 (2003) no. 5, pp. 1045-1054 | DOI

[40] 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

[41] Gustafsson, L. Interspecific Competition Lowers Fitness in Collared Flycatchers Ficedula Albicollis: An Experimental Demonstration, Ecology, Volume 68 (1987) no. 2, pp. 291-296 | DOI

[42] Hadfield, J. D.; Burgess, M. D.; Lord, A.; Phillimore, A. B.; Clegg, S. M.; Owens, I. P. Direct versus indirect sexual selection: genetic basis of colour, size and recruitment in a wild bird, Proceedings of the Royal Society B: Biological Sciences, Volume 273 (2006) no. 1592, pp. 1347-1353 | DOI

[43] HORAK, P.; LEBRETON, J.-D. Survival of adult Great Tits Parus major in relation to sex and habitat; a comparison of urban and rural populations, Ibis, Volume 140 (1998) no. 2, pp. 205-209 | DOI

[44] Iserbyt, A.; Griffioen, M.; Eens, M.; Müller, W. Enduring rules of care within pairs - how blue tit parents resume provisioning behaviour after experimental disturbance, Scientific Reports, Volume 9 (2019) no. 1 | DOI

[45] Laidre, K. L.; Atkinson, S.; Regehr, E. V.; Stern, H. L.; Born, E. W.; Wiig, Ø.; Lunn, N. J.; Dyck, M. Interrelated ecological impacts of climate change on an apex predator, Ecological Applications, Volume 30 (2020) no. 4 | DOI

[46] 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

[47] Lambrechts, M. M.; Charmantier, A.; Demeyrier, V.; Lucas, A.; Perret, S.; Abouladzé, M.; Bonnet, M.; Canonne, C.; Faucon, V.; Grosset, S.; le Prado, G.; Lidon, F.; Noell, T.; Pagano, P.; Perret, V.; Pouplard, S.; Spitaliéry, R.; Bernard, C.; Perret, P.; Blondel, J.; Grégoire, A. Nest design in a changing world: Great tit Parus major nests from a Mediterranean city environment as a case study, Urban Ecosystems, Volume 20 (2017) no. 6, pp. 1181-1190 | DOI

[48] Le Cœur, C.; Chantepie, S.; Pisanu, B.; Chapuis, J.-L.; Robert, A. Inter-annual and inter-individual variations in survival exhibit strong seasonality in a hibernating rodent, Oecologia, Volume 181 (2016) no. 3, pp. 795-807 | DOI

[49] Lebreton, J.-D.; Burnham, K. P.; Clobert, J.; Anderson, D. R. Modeling Survival and Testing Biological Hypotheses Using Marked Animals: A Unified Approach with Case Studies, Ecological Monographs, Volume 62 (1992) no. 1, pp. 67-118 | DOI

[50] Limbourg, T.; Mateman, A. C.; Lessells, C. M. Opposite differential allocation by males and females of the same species, Biology Letters, Volume 9 (2013) no. 1 | DOI

[51] Lionello, P.; Malanotte-Rizzoli, P.; Boscolo, R. Mediterranean climate variability, Elsevier, 2006

[52] Loison, A.; Festa-Bianchet, M.; Gaillard, J.-M.; Jorgenson, J. T.; Jullien, J.-M. AGE-SPECIFIC SURVIVAL IN FIVE POPULATIONS OF UNGULATES: EVIDENCE OF SENESCENCE, Ecology, Volume 80 (1999) no. 8, pp. 2539-2554 | DOI

[53] Massardier-Galatà, L.; Morinay, J.; Bailleul, F.; Wajnberg, E.; Guinet, C.; Coquillard, P. Breeding success of a marine central place forager in the context of climate change: A modeling approach, PLOS ONE, Volume 12 (2017) no. 3 | DOI

[54] Mazerolle, D. F.; Dufour, K. W.; Hobson, K. A.; Haan, H. E. d. Effects of large-scale climatic fluctuations on survival and production of young in a Neotropical migrant songbird, the yellow warblerDendroica petechia, Journal of Avian Biology, Volume 36 (2005) no. 2, pp. 155-163 | DOI

[55] McLean, N.; Lawson, C. R.; Leech, D. I.; Pol, M. Predicting when climate‐driven phenotypic change affects population dynamics, Ecology Letters, Volume 19 (2016) no. 6, pp. 595-608 | DOI

[56] Newton, I. The role of nest sites in limiting the numbers of hole-nesting birds: A review, Biological Conservation, Volume 70 (1994) no. 3, pp. 265-276 | DOI

[57] Norberg, J.; Urban, M. C.; Vellend, M.; Klausmeier, C. A.; Loeuille, N. Eco-evolutionary responses of biodiversity to climate change, Nature Climate Change, Volume 2 (2012) no. 10, pp. 747-751 | DOI

[58] Nord, A.; Nilsson, J.-Å. Long-term consequences of high incubation temperature in a wild bird population, Biology Letters, Volume 12 (2016) no. 4 | DOI

[59] Nur, N. The Consequences of Brood Size for Breeding Blue Tits II. Nestling Weight, Offspring Survival and Optimal Brood Size, The Journal of Animal Ecology, Volume 53 (1984) no. 2 | DOI

[60] Nur, N. The Consequences of Brood Size for Breeding Blue Tits I. Adult Survival, Weight Change and the Cost of Reproduction, The Journal of Animal Ecology, Volume 53 (1984) no. 2 | DOI

[61] OLANO-MARIN, J.; MUELLER, J. C.; KEMPENAERS, B. Heterozygosity and survival in blue tits (Cyanistes caeruleus): contrasting effects of presumably functional and neutral loci, Molecular Ecology, Volume 20 (2011) no. 19, pp. 4028-4041 | DOI

[62] Perdeck, A. C.; Visser, M. E.; Van Balen, J. H. Great Tit Parus major survival, and the beech-crop cycle, Ardea, Volume 88 (2000) no. 1

[63] Porneluzi, P. A.; Faaborg, J. Season-Long Fecundity, Survival, and Viability of Ovenbirds in Fragmented and Unfragmented Landscapes, Conservation Biology, Volume 13 (1999) no. 5, pp. 1151-1161 | DOI

[64] POST, E.; STENSETH, N. C. Large‐scale climatic fluctuation and population dynamics of moose and white‐tailed deer, Journal of Animal Ecology, Volume 67 (1998) no. 4, pp. 537-543 | DOI

[65] Réale, D.; Garant, D.; Humphries, M. M.; Bergeron, P.; Careau, V.; Montiglio, P.-O. Personality and the emergence of the pace-of-life syndrome concept at the population level, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 365 (2010) no. 1560, pp. 4051-4063 | DOI

[66] Reed, T. E.; Grøtan, V.; Jenouvrier, S.; Sæther, B.-E.; Visser, M. E. Population Growth in a Wild Bird Is Buffered Against Phenological Mismatch, Science, Volume 340 (2013) no. 6131, pp. 488-491 | DOI

[67] Robert, A. The effects of spatially correlated perturbations and habitat configuration on metapopulation persistence, Oikos, Volume 118 (2009) no. 10, pp. 1590-1600 | DOI

[68] Sangüesa-Barreda, G.; Camarero, J. J.; Sánchez-Salguero, R.; Gutiérrez, E.; Linares, J. C.; Génova, M.; Ribas, M.; Tíscar, P. A.; López-Sáez, J. A. Droughts and climate warming desynchronize Black pine growth across the Mediterranean Basin, Science of The Total Environment, Volume 697 (2019) | DOI

[69] Selonen, V.; Wistbacka, R.; Korpimäki, E. Food abundance and weather modify reproduction of two arboreal squirrel species, Journal of Mammalogy, Volume 97 (2016) no. 5, pp. 1376-1384 | DOI

[70] Senner, N. R.; Stager, M.; Sandercock, B. K. Ecological mismatches are moderated by local conditions for two populations of a long-distance migratory bird, Oikos, Volume 126 (2017) no. 1, pp. 61-72 | DOI

[71] Siriwardena, G.; Baillie, S.; Wilson, J. Variation in the survival rates of some British passerines with respect to their population trends on farmland, Bird Study, Volume 45 (1998) no. 3, pp. 276-292 | DOI

[72] Siriwardena, G. M.; Baillie, S. R.; Wilson, J. D. Temporal variation in the annual survival rates of six granivorous birds with contrasting population trends, Ibis, Volume 141 (1999) no. 4, pp. 621-636 | DOI

[73] Stjernman, M.; Råberg, L.; Nilsson, J. Survival costs of reproduction in the blue tit ( Parus caeruleus ): a role for blood parasites?, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 271 (2004) no. 1555, pp. 2387-2394 | DOI

[74] TREMBLAY, I.; THOMAS, D.; BLONDEL, J.; PERRET, P.; LAMBRECHTS, M. M. The effect of habitat quality on foraging patterns, provisioning rate and nestling growth in Corsican Blue Tits Parus caeruleus, Ibis, Volume 147 (2005) no. 1, pp. 17-24 | DOI

[75] Visser, M. E.; Gienapp, P. Evolutionary and demographic consequences of phenological mismatches, Nature Ecology & Evolution, Volume 3 (2019) no. 6, pp. 879-885 | DOI

[76] 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

[77] Visser, M. E.; Noordwijk, A. J. v.; Tinbergen, J. M.; Lessells, C. M. Warmer springs lead to mistimed reproduction in great tits (Parus major), Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 265 (1998) no. 1408, pp. 1867-1870 | DOI

[78] Watson, M. J. What drives population-level effects of parasites? Meta-analysis meets life-history, International Journal for Parasitology: Parasites and Wildlife, Volume 2 (2013), pp. 190-196 | DOI

[79] Williams, J. L.; Jacquemyn, H.; Ochocki, B. M.; Brys, R.; Miller, T. E. X. Life history evolution under climate change and its influence on the population dynamics of a long-lived plant, Journal of Ecology, Volume 103 (2015) no. 4, pp. 798-808 | DOI

[80] Winkler, D. W.; Ringelman, K. M.; Dunn, P. O.; Whittingham, L.; Hussell, D. J. T.; Clark, R. G.; Dawson, R. D.; Johnson, L. S.; Rose, A.; Austin, S. H.; Robinson, W. D.; Lombardo, M. P.; Thorpe, P. A.; Shutler, D.; Robertson, R. J.; Stager, M.; Leonard, M.; Horn, A. G.; Dickinson, J.; Ferretti, V.; Massoni, V.; Bulit, F.; Reboreda, J. C.; Liljesthröm, M.; Quiroga, M.; Rakhimberdiev, E.; Ardia, D. R. Latitudinal variation in clutch size-lay date regressions inTachycinetaswallows: effects of food supply or demography?, Ecography, Volume 37 (2014) no. 7, pp. 670-678 | DOI

[81] Wolkovich, E. M.; Cook, B. I.; McLauchlan, K. K.; Davies, T. J. Temporal ecology in the Anthropocene, Ecology Letters, Volume 17 (2014) no. 11, pp. 1365-1379 | DOI

[82] Wood, K. A.; Newth, J. L.; Hilton, G. M.; Nolet, B. A.; Rees, E. C. Inter-annual variability and long-term trends in breeding success in a declining population of migratory swans, Journal of Avian Biology, Volume 47 (2016) no. 5, pp. 597-609 | DOI

[83] Woodbridge, J.; Fyfe, R.; Smith, D.; Pelling, R.; Vareilles, A.; Batchelor, R.; Bevan, A.; Davies, A. L. What drives biodiversity patterns? Using long‐term multidisciplinary data to discern centennial‐scale change, Journal of Ecology, Volume 109 (2021) no. 3, pp. 1396-1410 | DOI

Cited by Sources:

block.super