Shifts in phenology due to global climate change: the need for a yardstick

Climate change has led to shifts in phenology in many species distributed widely across taxonomic groups. It is, however, unclear how we should interpret these shifts without some sort of a yardstick: a measure that will reflect how much a species should be shifting to match the change in its environment caused by climate change. Here, we assume that the shift in the phenology of a species' food abundance is, by a first approximation, an appropriate yardstick. We review the few examples that are available, ranging from birds to marine plankton. In almost all of these examples, the phenology of the focal species shifts either too little (five out of 11) or too much (three out of 11) compared to the yardstick. Thus, many species are becoming mistimed due to climate change. We urge researchers with long-term datasets on phenology to link their data with those that may serve as a yardstick, because documentation of the incidence of climate change-induced mistiming is crucial in assessing the impact of global climate change on the natural world.

[1]  S. Verhulst,et al.  The timing of birds' breeding seasons: a review of experiments that manipulated timing of breeding , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[2]  C. Both,et al.  Mistimed reproduction due to global climate change , 2006 .

[3]  Phillip Gienapp,et al.  Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird , 2006, Oecologia.

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

[5]  Lia Hemerik,et al.  A new statistical tool to predict phenology under climate change scenarios , 2005 .

[6]  D. Roy,et al.  The influence of temperature on migration of Lepidoptera into Britain , 2005 .

[7]  A. Mills.  Changes in the timing of spring and autumn migration in North American migrant passerines during a period of global warming , 2005 .

[8]  M. Whittingham,et al.  Warmer springs advance the breeding phenology of golden plovers Pluvialis apricaria and their prey (Tipulidae) , 2005, Oecologia.

[9]  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.

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

[11]  Daniel E. Schindler,et al.  CLIMATE CHANGE UNCOUPLES TROPHIC INTERACTIONS IN AN AQUATIC ECOSYSTEM , 2004 .

[12]  S. Wanless,et al.  Scale‐dependent climate signals drive breeding phenology of three seabird species , 2004 .

[13]  J. Pearce‐Higgins,et al.  Habitat selection, diet, arthropod availability and growth of a moorland wader: the ecology of European Golden Plover Pluvialis apricaria chicks , 2004 .

[14]  R. Dewar,et al.  Predicted changes in the synchrony of larval emergence and budburst under climatic warming , 1992, Oecologia.

[15]  T. Sparks,et al.  Arrival and Departure Dates , 2004 .

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

[17]  P. Dunn,et al.  Breeding Dates and Reproductive Performance , 2004 .

[18]  Charles M. Francis,et al.  The influence of climate on the timing and rate of spring bird migration , 2004, Oecologia.

[19]  C. Philippart,et al.  Climate‐related changes in recruitment of the bivalve Macoma balthica , 2003 .

[20]  P. A. Cotton.  Avian migration phenology and global climate change , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Sander,et al.  TROPHIC LEVELS ARE DIFFERENTIALLY SENSITIVE TO CLIMATE , 2003 .

[22]  Paul K. Strode.  Implications of climate change for North American wood warblers (Parulidae) , 2003 .

[23]  M. Kéry,et al.  Timing of autumn bird migration under climate change: advances in long–distance migrants, delays in short–distance migrants , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[24]  N. Stenseth,et al.  Trophic interactions under climate fluctuations: the Atlantic puffin as an example , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[25]  Christopher J. Butler.  The disproportionate effect of global warming on the arrival dates of short-distance migratory birds in North America , 2003 .

[26]  W. Cresswell,et al.  How great tits maintain synchronization of their hatch date with food supply in response to long-term variability in temperature , 2003 .

[27]  David L. Thomson,et al.  Variable responses to large-scale climate change in European Parus populations , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[28]  O. Hüppop,et al.  North Atlantic Oscillation and timing of spring migration in birds , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[30]  S. Schneider,et al.  Fingerprints of global warming on wild animals and plants , 2003, Nature.

[31]  C. Both,et al.  Predicting Life-Cycle Adaptation of Migratory Birds to Global Climate Change , 2002 .

[32]  Atle Mysterud,et al.  Climate, changing phenology, and other life history traits: Nonlinearity and match–mismatch to the environment , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[33]  C. McCulloch,et al.  Predicting the effects of climate change on avian life-history traits , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[34]  M. Noguer,et al.  Climate change 2001: The scientific basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change , 2002 .

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

[36]  C. Both,et al.  Adjustment to climate change is constrained by arrival date in a long-distance migrant bird , 2001, Nature.

[37]  Marcel E. Visser,et al.  Warmer springs disrupt the synchrony of oak and winter moth phenology , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[38]  S. Verhulst,et al.  Food, reproductive success and multiple breeding in the Great Tit Parus major , 2001 .

[39]  A. Rindorf,et al.  Effects of changes in sandeel availability on the reproductive output of seabirds , 2000 .

[40]  T. Sparks,et al.  Spring arrival patterns of the Cuckoo Cuculus canorus, Nightingale Luscinia megarhynchos and Spotted Flycatcher Musciapa striata in Britain , 2000 .

[41]  K. Armitage,et al.  Climate change is affecting altitudinal migrants and hibernating species. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Hughes,et al.  Biological consequences of global warming: is the signal already apparent? , 2000, Trends in ecology & evolution.

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

[44]  T. Sparks,et al.  Climate change and trophic interactions. , 1999, Trends in ecology & evolution.

[45]  T. Sparks.  Phenology and the changing pattern of bird migration in Britain , 1999 .

[46]  T. Sparks,et al.  Arrival and progression of the Swallow Hirundo rustica through Britain , 1998 .

[47]  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.

[48]  C. Perrins,et al.  Effects of elevated temperature and carbon dioxide on the nutritional quality of leaves of oak (Quercus robur L.) as food for the Winter Moth (Operophtera brumata L.) , 1998 .

[49]  T. Sparks,et al.  The effect of spring temperature on the appearance dates of British butterflies 1883–1993 , 1997 .

[50]  T. Backeljau,et al.  Synchronization of hatching date with budburst of individual host trees (Quercus robur) in the winter moth (Operophtera brumata) and its fitness consequences , 1997 .

[51]  J. Good,et al.  Synchronization of larval emergence in winter moth (Operophtera brumata L.) and budburst in pedunculate oak (Quercus robur L.) under simulated climate change , 1996 .

[52]  A. Houston,et al.  State-dependent life histories , 1996, Nature.

[53]  A. J. Noordwijk,et al.  Selection for the timing of great tit breeding in relation to caterpillar growth and temperature , 1995 .

[54]  T. Beebee,et al.  Amphibian breeding and climate , 1995, Nature.

[55]  Christopher M. Perrins,et al.  Laying dates and clutch size in the great tit , 1989 .

[56]  T. E. Martin.  Food as a limit on breeding birds: a life-history perspective , 1987 .

[57]  P. Feeny.  SEASONAL CHANGES IN OAK LEAF TANNINS AND NUTRIENTS AS A CAUSE OF SPRING FEEDING BY WINTER MOTH CATERPILLARS , 1970 .