Shifts in flowering phenology reshape a subalpine plant community

Significance Seasonal timing of biological events, phenology, is one of the strongest bioindicators of climate change. Our general understanding of phenological responses to climate change is based almost solely on the first day on which an event is observed, limiting our understanding of how ecological communities may be responding as a whole. Using a unique long-term record of flowering phenology from Colorado, we find that the number of species changing their flowering times likely has been underestimated and the magnitude of phenological change overestimated. In addition to earlier first flowering, we document a diverse assortment of other changes, such as delayed last flowering, as temperatures warm. This variety of species-level phenological shifts has ultimately reshaped various temporal components of the plant community. Phenology—the timing of biological events—is highly sensitive to climate change. However, our general understanding of how phenology responds to climate change is based almost solely on incomplete assessments of phenology (such as first date of flowering) rather than on entire phenological distributions. Using a uniquely comprehensive 39-y flowering phenology dataset from the Colorado Rocky Mountains that contains more than 2 million flower counts, we reveal a diversity of species-level phenological shifts that bring into question the accuracy of previous estimates of long-term phenological change. For 60 species, we show that first, peak, and last flowering rarely shift uniformly and instead usually shift independently of one another, resulting in a diversity of phenological changes through time. Shifts in the timing of first flowering on average overestimate the magnitude of shifts in the timing of peak flowering, fail to predict shifts in the timing of last flowering, and underrepresent the number of species changing phenology in this plant community. Ultimately, this diversity of species-level phenological shifts contributes to altered coflowering patterns within the community, a redistribution of floral abundance across the season, and an expansion of the flowering season by more than I mo during the course of our study period. These results demonstrate the substantial reshaping of ecological communities that can be attributed to shifts in phenology.

[1]  R. Primack,et al.  How well do first flowering dates measure plant responses to climate change? The effects of population size and sampling frequency , 2008 .

[2]  A. Miller‐Rushing,et al.  Emergence of a mid‐season period of low floral resources in a montane meadow ecosystem associated with climate change , 2011 .

[3]  A. Miller‐Rushing,et al.  Toward a synthetic understanding of the role of phenology in ecology and evolution , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[4]  J. Pleasants COMPETITION FOR BUMBLEBEE POLLINATORS IN ROCKY MOUNTAIN PLANT COMMUNITIES , 1980 .

[5]  A. King,et al.  Time Lags and the Balance of Positive and Negative Interactions in Driving Grassland Community Dynamics , 2009, The American Naturalist.

[6]  A. Fitter,et al.  Rapid Changes in Flowering Time in British Plants , 2002, Science.

[7]  O. Hüppop,et al.  Examining the total arrival distribution of migratory birds , 2005 .

[8]  Otso Ovaskainen,et al.  Community-level phenological response to climate change , 2013, Proceedings of the National Academy of Sciences.

[9]  M. Edwards,et al.  Impact of climate change on marine pelagic phenology and trophic mismatch , 2004, Nature.

[10]  Rampal S Etienne,et al.  Phenology drives mutualistic network structure and diversity. , 2012, Ecology letters.

[11]  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.

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

[13]  F. G. Stiles Coadapted Competitors: The Flowering Seasons of Hummingbird-Pollinated Plants in a Tropical Forest , 1977, Science.

[14]  A. Stewart,et al.  Interspecific competition reinstated as an important force structuring insect herbivore communities. , 1996, Trends in ecology & evolution.

[15]  Jordi Bascompte,et al.  Temporal dynamics in a pollination network. , 2008, Ecology.

[16]  A. Fitter,et al.  Spatial and temporal patterns of growth and nutrient uptake of five co-existing grasses , 1984 .

[17]  T. Høye,et al.  Long-term trends mask variation in the direction and magnitude of short-term phenological shifts. , 2013, American journal of botany.

[18]  S. Jackson,et al.  Novel climates, no‐analog communities, and ecological surprises , 2007 .

[19]  N. Waser Competition for Hummingbird Pollination and Sequential Flowering in Two Colorado Wildflowers , 1978 .

[20]  J. C. Marlin,et al.  Plant-Pollinator Interactions over 120 Years: Loss of Species, Co-Occurrence, and Function , 2013, Science.

[21]  John Harte,et al.  SUBALPINE MEADOW FLOWERING PHENOLOGY RESPONSES TO CLIMATE CHANGE: INTEGRATING EXPERIMENTAL AND GRADIENT METHODS , 2003 .

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

[23]  G. Walther Community and ecosystem responses to recent climate change , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[24]  M. V. Price,et al.  EFFECTS OF EXPERIMENTAL WARMING ON PLANT REPRODUCTIVE PHENOLOGY IN A SUBALPINE MEADOW , 1998 .

[25]  T. Mosquin Competition for pollinators as a stimulus for the evolution of flowering time , 1971 .

[26]  J. Ghazoul Floral diversity and the facilitation of pollination , 2006 .

[27]  R. Primack,et al.  Bird migration times, climate change, and changing population sizes , 2008 .

[28]  M. Power,et al.  Species Interactions Reverse Grassland Responses to Changing Climate , 2007, Science.

[29]  Toke T. Høye,et al.  Nonlinear flowering responses to climate: are species approaching their limits of phenological change? , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[30]  E. Post,et al.  Seasons and Life Cycles , 2009, Science.

[31]  J. Thomson,et al.  Consequences of variation in flowering time within and among individuals of Mertensia fusiformis (Boraginaceae), an early spring wildflower. , 2010, American journal of botany.

[32]  T. Høye,et al.  Shorter flowering seasons and declining abundance of flower visitors in a warmer Arctic , 2013 .

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

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

[35]  Ørjan Totland,et al.  How does climate warming affect plant-pollinator interactions? , 2009, Ecology letters.

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

[37]  H. Gregory McDonald,et al.  Spatial Response of Mammals to Late Quaternary Environmental Fluctuations , 1996, Science.

[38]  A. Biere,et al.  Time after time: flowering phenology and biotic interactions. , 2007, Trends in ecology & evolution.

[39]  A. Miller‐Rushing,et al.  Forecasting phenology: from species variability to community patterns. , 2012, Ecology letters.

[40]  J. Glanz Behind the Official Optimism, Flawed Projections , 1996, Science.

[41]  D. Inouye,et al.  Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. , 2008, Ecology.