Warming, plant phenology and the spatial dimension of trophic mismatch for large herbivores

Temporal advancement of resource availability by warming in seasonal environments can reduce reproductive success of vertebrates if their own reproductive phenology does not also advance with warming. Indirect evidence from large-scale analyses suggests, however, that migratory vertebrates might compensate for this by tracking phenological variation across landscapes. Results from our two-year warming experiment combined with seven years of observations of plant phenology and offspring production by caribou (Rangifer tarandus) in Greenland, however, contradict evidence from large-scale analyses. At spatial scales relevant to the foraging horizon of individual herbivores, spatial variability in plant phenology was reduced—not increased—by both experimental and observed warming. Concurrently, offspring production by female caribou declined with reductions in spatial variability in plant phenology. By highlighting the spatial dimension of trophic mismatch, these results reveal heretofore unexpected adverse consequences of climatic warming for herbivore population ecology.

[1]  J. Kingsolver,et al.  Migration, local adaptation and the evolution of plasticity , 2002 .

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

[3]  J. T. Giesel.  Reproductive Strategies as Adaptations to Life in Temporally Heterogeneous Environments , 1976 .

[4]  Jonathan Roughgarden,et al.  Population Dynamics in a Spatially Varying Environment: How Population Size "Tracks" Spatial Variation in Carrying Capacity , 1974, The American Naturalist.

[5]  G. Kitagawa,et al.  Akaike Information Criterion Statistics , 1988 .

[6]  S. Levin.  Population Dynamic Models in Heterogeneous Environments , 1976 .

[7]  E. Post,et al.  Synchrony between caribou calving and plant phenology in depredated and non-depredated populations , 2003 .

[8]  Nils Chr. Stenseth,et al.  CLIMATIC VARIABILITY, PLANT PHENOLOGY, AND NORTHERN UNGULATES , 1999 .

[9]  R. White.  Foraging patterns and their multiplier effects on productivity of northern ungulates , 1983 .

[10]  S. Albon,et al.  Plant phenology and the benefits of migration in a temperate ungulate , 1992 .

[11]  Mark Hebblewhite,et al.  A MULTI-SCALE TEST OF THE FORAGE MATURATION HYPOTHESIS IN A PARTIALLY MIGRATORY UNGULATE POPULATION , 2008 .

[12]  E. Post.  LARGE‐SCALE CLIMATE SYNCHRONIZES THE TIMING OF FLOWERING BY MULTIPLE SPECIES , 2003 .

[13]  D. Klein.  Variation in quality of caribou and reindeer forage plants associated with season, plant part, and phenology , 1990 .

[14]  C. Both,et al.  The effect of climate change on the correlation between avian life‐history traits , 2005 .

[15]  D. Klein.  Tundra Ranges North of the Boreal Forest. , 1970 .

[16]  R. Gao,et al.  [Heat stress characteristics of photosystem II in eggplant]. , 1981, Ying yong sheng tai xue bao = The journal of applied ecology.

[17]  Nathalie Pettorelli,et al.  Importance of climatological downscaling and plant phenology for red deer in heterogeneous landscapes , 2005, Proceedings of the Royal Society B: Biological Sciences.

[18]  A. Hofgaard,et al.  Foraging and movement paths of female reindeer: insights from fractal analysis, correlated random walks, and Lévy flights , 2002 .

[19]  Derek W. Bailey,et al.  Large Herbivore Foraging and Ecological HierarchiesLandscape ecology can enhance traditional foraging theory , 1987 .

[20]  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.

[21]  R. White,et al.  The Effect of Forage Structure and Availability on Food Intake, Biting Rate, Bite Size and Daily Eating Time of Reindeer , 1981 .

[22]  P. C. Elkie,et al.  Seasonal movement patterns of woodland caribou (Rangifer tarandus caribou) , 2004 .

[23]  D. Klein.  The introduction, increase, and crash of reindeer on St. Matthew Island. , 1968 .

[24]  Xiaoqiu Chen,et al.  Spatial and temporal variation of phenological growing season and climate change impacts in temperate eastern China , 2005 .

[25]  E. Post,et al.  Phenological sequences reveal aggregate life history response to climatic warming. , 2008, Ecology.

[26]  R. White,et al.  Habitat Preference and Forage Consumption by Reindeer and Caribou near Atkasook, Alaska , 1980 .

[27]  E. Post,et al.  Caribou calf production and seasonal range quality during a population decline , 1999 .

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

[29]  The relationship between weather and caribou productivity for the La-Poile Caribou Herd, Newfoundland , 1991 .

[30]  A. Mysterud,et al.  Plant phenology, migration and geographical variation in body weight of a large herbivore: the effect of a variable topography , 2001 .

[31]  Nathalie Pettorelli,et al.  Climate predictability and breeding phenology in red deer: timing and synchrony of rutting and calving in Norway and France , 2005 .

[32]  J. Wiens.  Population Responses to Patchy Environments , 1976 .

[33]  J. Bryant,et al.  Selection of Winter Forage by Subarctic Browsing Vertebrates: The Role of Plant Chemistry , 1980 .

[34]  N. Pettorelli,et al.  The relative role of winter and spring conditions: linking climate and landscape-scale plant phenology to alpine reindeer body mass , 2005, Biology Letters.

[35]  L. Edenius,et al.  Spatial Heterogeneity and Hierarchical Feeding Habitat Selection by Reindeer , 2006 .

[36]  G. Henry,et al.  Open‐top designs for manipulating field temperature in high‐latitude ecosystems , 1997 .

[37]  Lars Gustafsson,et al.  Large–scale geographical variation confirms that climate change causes birds to lay earlier , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[38]  P. Lundberg,et al.  The evolution of partial migration in Birds. , 1988, Trends in ecology & evolution.

[39]  T. Skogland,et al.  Responses of Caribou and Reindeer to Global Warming , 1997 .

[40]  Marcel E. Visser,et al.  Warmer springs lead to mistimed reproduction in great tits (Parus major) , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[41]  Marcel E Visser,et al.  Shifts in phenology due to global climate change: the need for a yardstick , 2005, Proceedings of the Royal Society B: Biological Sciences.

[42]  T. Skogland.  Comparative social organization of wild reindeer in relation to food, mates and predator avoidance , 1989 .

[43]  W. Ballard,et al.  Factors limiting productivity of the Central Arctic Caribou Herd of Alaska , 2004 .