Phenological asynchrony: a ticking time-bomb for seemingly stable populations?

Climate change has been shown to induce shifts in the timing of life-history events. As a result, interactions between species can become disrupted, with potentially detrimental effects. Predicting these consequences has proven challenging. We apply structured population models to a well-characterised great tit-caterpillar model system and identify thresholds of temporal asynchrony, beyond which the predator population will rapidly go extinct. Our model suggests that phenotypic plasticity in predator breeding timing initially maintains temporal synchrony in the face of environmental change. However, under projections of climate change, predator plasticity was insufficient to keep pace with prey phenology. Directional evolution then accelerated, but could not prevent mismatch. Once predator phenology lagged behind prey by more than 24 days, rapid extinction was inevitable, despite previously stable population dynamics. Our projections suggest that current population stability could be masking a route to population collapse, if high greenhouse gas emissions continue.

[1]  P. Thomas,et al.  Climate warming disrupts mast seeding and its fitness benefits in European beech , 2020, Nature Plants.

[2]  Emily G. Simmonds,et al.  Testing the effect of quantitative genetic inheritance in structured models on projections of population dynamics , 2020, Oikos.

[3]  Emily G Simmonds,et al.  Cue identification in phenology: A case study of the predictive performance of current statistical tools , 2019, The Journal of animal ecology.

[4]  Marcel E Visser,et al.  Phenological mismatch drives selection on elevation, but not on slope, of breeding time plasticity in a wild songbird , 2018, Evolution; international journal of organic evolution.

[5]  András Liker,et al.  Impact of urbanization on abundance and phenology of caterpillars and consequences for breeding in an insectivorous bird. , 2018, Ecological applications : a publication of the Ecological Society of America.

[6]  Ying Huang,et al.  chngpt: threshold regression model estimation and inference , 2017, BMC Bioinformatics.

[7]  Emily G Simmonds,et al.  Incubation behavior adjustments, driven by ambient temperature variation, improve synchrony between hatch dates and caterpillar peak in a wild bird population , 2017, Ecology and evolution.

[8]  Yanhui Fan,et al.  PyHLA: tests for the association between HLA alleles and diseases , 2017, BMC Bioinformatics.

[9]  Julia A. Barthold,et al.  Modeling Adaptive and Non-adaptive Responses of Populations to Environmental Change , 2016, bioRxiv.

[10]  Martijn van de Pol,et al.  Identifying the best climatic predictors in ecology and evolution , 2016 .

[11]  Liam D. Bailey,et al.  climwin: An R Toolbox for Climate Window Analysis , 2016, bioRxiv.

[12]  N. Schmidt,et al.  Effects of food abundance and early clutch predation on reproductive timing in a high Arctic shorebird exposed to advancements in arthropod abundance , 2016, Ecology and evolution.

[13]  Paul M. Thompson,et al.  Phenological sensitivity to climate across taxa and trophic levels , 2016, Nature.

[14]  B. Sheldon,et al.  The evolution of labile traits in sex‐ and age‐structured populations , 2016, The Journal of animal ecology.

[15]  Amanda S. Gallinat,et al.  Autumn, the neglected season in climate change research. , 2015, Trends in ecology & evolution.

[16]  Jan‐Åke Nilsson,et al.  The eco‐evolutionary consequences of interspecific phenological asynchrony – a theoretical perspective , 2015 .

[17]  Consequences of information use in breeding habitat selection on the evolution of settlement time , 2015 .

[18]  C. Parmesan,et al.  Geographic mosaics of phenology, host preference, adult size and microhabitat choice predict butterfly resilience to climate warming , 2015 .

[19]  Marcel E Visser,et al.  Why climate change will invariably alter selection pressures on phenology , 2014, Proceedings of the Royal Society B: Biological Sciences.

[20]  A. J. Mark Hewison,et al.  Mismatch Between Birth Date and Vegetation Phenology Slows the Demography of Roe Deer , 2014, PLoS biology.

[21]  Anne Charmantier,et al.  Climate change and timing of avian breeding and migration: evolutionary versus plastic changes , 2013, Evolutionary applications.

[22]  M. Visser,et al.  Is microevolution the only emergency exit in a warming world? Temperature influences egg laying but not its underlying mechanisms in great tits. , 2013, General and comparative endocrinology.

[23]  B. Sheldon,et al.  Quantitative Assessment of the Importance of Phenotypic Plasticity in Adaptation to Climate Change in Wild Bird Populations , 2013, PLoS biology.

[24]  Bernt-Erik Sæther,et al.  Population Growth in a Wild Bird Is Buffered Against Phenological Mismatch , 2013, Science.

[25]  Marcel E Visser,et al.  Phenological mismatch strongly affects individual fitness but not population demography in a woodland passerine. , 2013, The Journal of animal ecology.

[26]  J. Gaillard,et al.  Modeling reproductive trajectories of roe deer females: fixed or dynamic heterogeneity? , 2012, Theoretical population biology.

[27]  J. Quesada,et al.  The diet of Great Tit Parus major nestlings in a Mediterranean Iberian forest: the important role of spiders , 2011 .

[28]  Ag Stephens,et al.  UK Climate Change Projections Report , 2010 .

[29]  T. Clutton‐Brock,et al.  Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments , 2010 .

[30]  Toke Thomas Høye,et al.  The effects of phenological mismatches on demography , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[31]  Camille Parmesan,et al.  Phenological asynchrony between herbivorous insects and their hosts: signal of climate change or pre-existing adaptive strategy? , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[32]  T. Sparks,et al.  Changes in migration , 2010 .

[33]  R. Lande,et al.  Adaptation, Plasticity, and Extinction in a Changing Environment: Towards a Predictive Theory , 2010, PLoS biology.

[34]  Matthew D. Collins,et al.  UK Climate Projections Science Report: Climate Change Projections , 2009 .

[35]  M. Visser,et al.  Spatial and temporal variation in the relative contribution of density dependence, climate variation and migration to fluctuations in the size of great tit populations. , 2009, The Journal of animal ecology.

[36]  Marcel E Visser,et al.  Keeping up with a warming world; assessing the rate of adaptation to climate change , 2008, Proceedings of the Royal Society B: Biological Sciences.

[37]  C. Parmesan Influences of species, latitudes and methodologies on estimates of phenological response to global warming , 2007 .

[38]  Vincent R. Gray Climate Change 2007: The Physical Science Basis Summary for Policymakers , 2007 .

[39]  H. Mooney,et al.  Shifting plant phenology in response to global change. , 2007, Trends in ecology & evolution.

[40]  M. Visser,et al.  WHY BREEDING TIME HAS NOT RESPONDED TO SELECTION FOR EARLIER BREEDING IN A SONGBIRD POPULATION , 2006, Evolution; international journal of organic evolution.

[41]  J. Peñuelas,et al.  European phenological response to climate change matches the warming pattern , 2006 .

[42]  C. Both,et al.  Global Climate Change Leads to Mistimed Avian Reproduction , 2004 .

[43]  Denis Réale,et al.  Genetic and plastic responses of a northern mammal to climate change , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[44]  Alexei G. Sankovski,et al.  Special report on emissions scenarios : a special report of Working group III of the Intergovernmental Panel on Climate Change , 2000 .

[45]  M. Visser,et al.  Great Tit Parus major survival and the beech-crop cycle. , 2000 .

[46]  C. Perrins,et al.  Effects of elevated temperature on multi‐species interactions: the case of Pedunculate Oak, Winter Moth and Tits , 1999 .

[47]  Erik Matthysen,et al.  Effects of habitat fragmentation on provisioning rates, diet and breeding success in two species of tit (great tit and blue tit) , 1998, Oecologia.

[48]  J. V. Balen Population Fluctuations of the Great Tit and Feeding Conditions in Winter , 2015 .

[49]  R. Lande The maintenance of genetic variability by mutation in a polygenic character with linked loci. , 1975, Genetical research.

[50]  D. Cushing The Regularity of the Spawning Season of Some Fishes , 1969 .

[51]  Christopher M. Perrins,et al.  Population fluctuations and clutch size in the Great tit , 1965 .

[52]  J. D. Matthews THE INFLUENCE OF WEATHER ON THE FREQUENCY OF BEECH MAST YEARS IN ENGLAND , 1955 .