Greater temperature sensitivity of plant phenology at colder sites: implications for convergence across northern latitudes

Warmer temperatures are accelerating the phenology of organisms around the world. Temperature sensitivity of phenology might be greater in colder, higher latitude sites than in warmer regions, in part because small changes in temperature constitute greater relative changes in thermal balance at colder sites. To test this hypothesis, we examined up to 20 years of phenology data for 47 tundra plant species at 18 high‐latitude sites along a climatic gradient. Across all species, the timing of leaf emergence and flowering was more sensitive to a given increase in summer temperature at colder than warmer high‐latitude locations. A similar pattern was seen over time for the flowering phenology of a widespread species, Cassiope tetragona. These are among the first results highlighting differential phenological responses of plants across a climatic gradient and suggest the possibility of convergence in flowering times and therefore an increase in gene flow across latitudes as the climate warms.

[1]  L. C. Bliss.  Adaptations of Arctic and Alpine Plants to Environmental Conditions , 1962 .

[2]  Harold A. Mooney,et al.  THE ECOLOGY OF ARCTIC AND ALPINE PLANTS , 1968 .

[3]  F. Chapin,et al.  Ecotypic differentiation of growth processes in Carex aquatilis along latitudinal and local gradients. , 1981 .

[4]  J. McGraw,et al.  Experimental ecology of Dryas octopetala ecotypes. I. Ecotypic differentiation and life-cycle stages of selection , 1983 .

[5]  W. D. Billings.  5 – Phytogeographic and Evolutionary Potential of the Arctic Flora and Vegetation in a Changing Climate , 1992 .

[6]  D. Rubin,et al.  Inference from Iterative Simulation Using Multiple Sequences , 1992 .

[7]  G. Shaver,et al.  9 – Phenology, Resource Allocation, and Growth of Arctic Vascular Plants , 1992 .

[8]  T. Callaghan,et al.  COMPARATIVE RESPONSES OF PHENOLOGY AND REPRODUCTIVE DEVELOPMENT TO SIMULATED ENVIRONMENTAL-CHANGE IN SUB-ARCTIC AND HIGH ARCTIC PLANTS , 1993 .

[9]  T. Callaghan,et al.  Growth responses of four sub-Arctic dwarf shrubs to simulated environmental change , 1994 .

[10]  M. Williamson,et al.  Relationships between first flowering date and temperature in the flora of a locality in central England , 1995 .

[11]  G. Henry,et al.  Tundra plants and climate change: the International Tundra Experiment (ITEX) , 1997 .

[12]  Konrad A Hughen,et al.  Arctic Environmental Change of the Last Four Centuries , 1997 .

[13]  E. Lévesque,et al.  Phenological and growth responses of Papaver radicatum along altitudinal gradients in the Canadian High Arctic , 1997 .

[14]  U. Molau,et al.  Responses of Dryas octopetala to ITEX environmental manipulations: a synthesis with circumpolar comparisons , 1997 .

[15]  B. Schmid,et al.  Latitudinal population differentiation in two species of Solidago (Asteraceae) introduced into Europe. , 1998, American journal of botany.

[16]  T. E. Thórhallsdóttir.  Flowering phenology in the central highland of Iceland and implications for climatic warming in the Arctic , 1998, Oecologia.

[17]  S. Oberbauer,et al.  Effects of extended growing season and soil warming on carbon dioxide and methane exchange of tussock tundra in Alaska , 1998 .

[18]  Robert D. Hollister,et al.  RESPONSES OF TUNDRA PLANTS TO EXPERIMENTAL WARMING:META‐ANALYSIS OF THE INTERNATIONAL TUNDRA EXPERIMENT , 1999 .

[19]  W. Oechel,et al.  Acclimation of ecosystem CO2 exchange in the Alaskan Arctic in response to decadal climate warming , 2000, Nature.

[20]  C. Tucker,et al.  Higher northern latitude normalized difference vegetation index and growing season trends from 1982 to 1999 , 2001, International journal of biometeorology.

[21]  Isabelle Chuine,et al.  Phenology is a major determinant of tree species range , 2001 .

[22]  Thomas Lenormand,et al.  Gene flow and the limits to natural selection , 2002 .

[23]  O. Hoegh‐Guldberg,et al.  Ecological responses to recent climate change , 2002, Nature.

[24]  G. Fox.  Assortative Mating and Plant Phenology: Evolutionary and Practical Consequences , 2003 .

[25]  G. Yohe,et al.  A globally coherent fingerprint of climate change impacts across natural systems , 2003, Nature.

[26]  Growth dynamics and phenology , 2003 .

[27]  O. Savolainen,et al.  Environmental and genetic effects on flowering differences between northern and southern populations of Arabidopsis lyrata (Brassicaceae). , 2004, American journal of botany.

[28]  J. McGraw.  Experimental ecology of Dryas octopetala ecotypes , 1987, Oecologia.

[29]  J. Welker,et al.  CO2 exchange in three Canadian High Arctic ecosystems: response to long‐term experimental warming , 2004 .

[30]  F. Chapin,et al.  Evidence and Implications of Recent Climate Change in Northern Alaska and Other Arctic Regions , 2004 .

[31]  J. Schaber,et al.  Responses of spring phenology to climate change , 2004 .

[32]  A. Stead.  Pollination-induced flower senescence: a review , 2004, Plant Growth Regulation.

[33]  Kjell Arild Høgda,et al.  Environmental phenology and geographical gradients in moose body mass , 2006, Oecologia.

[34]  Steven F. Oberbauer,et al.  Plant community responses to experimental warming across the tundra biome , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[35]  J. Kohler,et al.  A long-term Arctic snow depth record from Abisko, northern Sweden, 1913–2004 , 2006 .

[36]  A long-term Arctic snow depth record from Abisko, northern Sweden, 1913–2004 , 2006 .

[37]  I. Pen,et al.  Geographical patterns of adaptation within a species’ range: interactions between drift and gene flow , 2006, Journal of evolutionary biology.

[38]  Toke T. Høye,et al.  Rapid advancement of spring in the High Arctic , 2007, Current Biology.

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

[40]  T. Høye,et al.  The Impact of Climate on Flowering in the High Arctic—The Case of Dryas in a Hybrid Zone , 2007 .

[41]  Steven F. Oberbauer,et al.  TUNDRA CO2 FLUXES IN RESPONSE TO EXPERIMENTAL WARMING ACROSS LATITUDINAL AND MOISTURE GRADIENTS , 2007 .

[42]  E. Post,et al.  Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[43]  A. Latimer.  Geography and resource limitation complicate metabolism-based predictions of species richness. , 2007, Ecology.

[44]  L. C. Blisst.  ADAPTATIONS OF ARCTIC AND ALPINE PLANTS TO ENVIRONMENTAL CONDITIONS * , 2007 .

[45]  Eric Post,et al.  Warming, plant phenology and the spatial dimension of trophic mismatch for large herbivores , 2008, Proceedings of the Royal Society B: Biological Sciences.

[46]  Richard B Primack,et al.  Global warming and flowering times in Thoreau's Concord: a community perspective. , 2008, Ecology.

[47]  Josep Peñuelas,et al.  Phenology Feedbacks on Climate Change , 2009, Science.

[48]  Martijn van de Pol,et al.  A simple method for distinguishing within- versus between-subject effects using mixed models , 2009, Animal Behaviour.

[49]  W. Thuiller,et al.  Comparing niche- and process-based models to reduce prediction uncertainty in species range shifts under climate change. , 2009, Ecology.

[50]  Marcel E Visser,et al.  Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? , 2009, The Journal of animal ecology.

[51]  I. Chuine.  Why does phenology drive species distribution? , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[52]  Jarrod D Hadfield,et al.  Differences in spawning date between populations of common frog reveal local adaptation , 2010, Proceedings of the National Academy of Sciences.

[53]  Y. Onda,et al.  Clinal Variation in Flowering Time and Vernalisation Requirement across a 3000-M Altitudinal Range in Perennial Arabidopsis kamchatica Ssp.Kamchatica and Annual Lowland Subspecies Kawasakiana , 2011 .

[54]  G. Henry,et al.  Responses of High Arctic wet sedge tundra to climate warming since 1980 , 2011 .

[55]  V. LeMay,et al.  Changes in high arctic tundra plant reproduction in response to long‐term experimental warming , 2011 .

[56]  S. Dullinger,et al.  Late snowmelt delays plant development and results in lower reproductive success in the High Arctic. , 2011, Plant science : an international journal of experimental plant biology.

[57]  S. Strauss,et al.  Gene flow increases fitness at the warm edge of a species’ range , 2011, Proceedings of the National Academy of Sciences.

[58]  Gaku Kudo,et al.  Global assessment of experimental climate warming on tundra vegetation: heterogeneity over space and time. , 2012, Ecology letters.

[59]  B. Cook,et al.  Divergent responses to spring and winter warming drive community level flowering trends , 2012, Proceedings of the National Academy of Sciences.

[60]  J. Welker,et al.  Interactions among shrub cover and the soil microclimate may determine future Arctic carbon budgets. , 2012, Ecology letters.

[61]  J. McGraw,et al.  Home site advantage in two long‐lived arctic plant species: results from two 30‐year reciprocal transplant studies , 2012 .

[62]  Benjamin Smith,et al.  Modelling Tundra Vegetation Response to Recent Arctic Warming , 2012, AMBIO.

[63]  Marc Macias-Fauria,et al.  Eurasian Arctic greening reveals teleconnections and the potential for structurally novel ecosystems , 2012 .

[64]  Steven F. Oberbauer,et al.  Plot-scale evidence of tundra vegetation change and links to recent summer warming. , 2012 .

[65]  R. Kotter,et al.  Ecology of climate change: the importance of biotic interactions , 2013 .

[66]  A. Phillimore,et al.  Inferring local processes from macro‐scale phenological pattern: a comparison of two methods , 2013 .

[67]  Eric Post,et al.  Advancing plant phenology and reduced herbivore production in a terrestrial system associated with sea ice decline , 2013, Nature Communications.

[68]  J. Welker,et al.  Complex carbon cycle responses to multi‐level warming and supplemental summer rain in the high Arctic , 2013, Global change biology.

[69]  J. Welker,et al.  Phenological response of tundra plants to background climate variation tested using the International Tundra Experiment , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[70]  B. Elberling,et al.  Snow cover and extreme winter warming events control flower abundance of some, but not all species in high arctic Svalbard , 2013, Ecology and evolution.

[71]  Stewart J. Cohen,et al.  Climate Change 2014: Impacts,Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change , 2014 .

[72]  S. Rumpf,et al.  Idiosyncratic Responses of High Arctic Plants to Changing Snow Regimes , 2014, PloS one.

[73]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[74]  Carl F. Salk,et al.  Tree phenology responses to winter chilling, spring warming, at north and south range limits , 2014 .

[75]  P. Jones,et al.  Updated high‐resolution grids of monthly climatic observations – the CRU TS3.10 Dataset , 2014 .

[76]  A. Nicotra,et al.  The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. , 2014, Ecology letters.

[77]  Niels Martin Schmidt,et al.  Climate sensitivity of shrub growth across the tundra biome , 2015 .

[78]  M. Vellend,et al.  The effects of experimental warming on the timing of a plant-insect herbivore interaction. , 2015, The Journal of animal ecology.

[79]  Anne D. Bjorkman,et al.  Contrasting effects of warming and increased snowfall on Arctic tundra plant phenology over the past two decades , 2015, Global change biology.

[80]  R. Barrett,et al.  Arctic plant responses to changing abiotic factors in northern Alaska. , 2015, American journal of botany.

[81]  Amanda S. Gallinat,et al.  Substantial variation in leaf senescence times among 1360 temperate woody plant species: implications for phenology and ecosystem processes. , 2015, Annals of botany.

[82]  S. Oberbauer,et al.  Diminished Response of Arctic Plants to Warming over Time , 2015, PloS one.

[83]  M. Vellend,et al.  Flowering time of butterfly nectar food plants is more sensitive to temperature than the timing of butterfly adult flight. , 2015, The Journal of animal ecology.

[84]  S. Higgins,et al.  Three decades of multi-dimensional change in global leaf phenology , 2015 .

[85]  N. Diffenbaugh,et al.  Observed and projected climate trends and hotspots across the National Ecological Observatory Network regions , 2015 .

[86]  S. Oberbauer,et al.  Plant phenological responses to a long‐term experimental extension of growing season and soil warming in the tussock tundra of Alaska , 2015, Global change biology.

[87]  E. Post,et al.  Root phenology in a changing climate. , 2016, Journal of experimental botany.

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

[89]  S. Wilson,et al.  The hidden season: growing season is 50% longer below than above ground along an arctic elevation gradient. , 2016, The New phytologist.

[90]  G. Phoenix,et al.  Arctic browning: extreme events and trends reversing arctic greening , 2016, Global change biology.

[91]  G. Phoenix,et al.  Contrasting synchrony in root and leaf phenology across multiple sub‐Arctic plant communities , 2016 .

[92]  R. Rockwell,et al.  Increased variance in temperature and lag effects alter phenological responses to rapid warming in a subarctic plant community , 2017, Global change biology.