Phenology, ontogeny and the effects of climate change on the timing of species interactions.

Climate change is altering the phenology of many species and the timing of their interactions with other species, but the impacts of these phenological shifts on species interactions remain unclear. Classical approaches to the study of phenology have typically documented changes in the timing of single life-history events, while phenological shifts affect many interactions over entire life histories. In this study, we suggest an approach that integrates the phenology and ontogeny of species interactions with a fitness landscape to provide a common mechanistic framework for investigating phenological shifts. We suggest that this ontogeny-phenology landscape provides a flexible method to document changes in the relative phenologies of interacting species, examine the causes of these phenological shifts, and estimate their consequences for interacting species.

[1]  S. Archer,et al.  Defoliation and woody plant (shape Prosopis glandulosa) seedling regeneration: potential vs realized herbivory tolerance , 2004, Plant Ecology.

[2]  R. E. Ziemba,et al.  Foraging under the risk of cannibalism leads to divergence in body size among tiger salamander larvae , 2000, Oecologia.

[3]  E. Werner.  Ontogenetic Scaling of Competitive Relations: Size‐Dependent Effects and Responses in Two Anuran Larvae , 1994 .

[4]  O. Gordo,et al.  Phenology and climate change: a long-term study in a Mediterranean locality , 2005, Oecologia.

[5]  M. C. Urban.  Predator size and phenology shape prey survival in temporary ponds , 2007, Oecologia.

[6]  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.

[7]  D. Winkler,et al.  Climate change has affected the breeding date of tree swallows throughout North America , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[8]  H. Lieth.  Phenology and Seasonality Modeling , 1974, Ecological Studies.

[9]  R. Karban,et al.  Consequences of variation in flowering phenology for seed head herbivory and reproductive success in Erigeron glaucus (Compositae) , 1992, Oecologia.

[10]  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.

[11]  M. Sabelis,et al.  Prey attack and predators defend: counterattacking prey trigger parental care in predators , 2005, Proceedings of the Royal Society B: Biological Sciences.

[12]  M. C. Urban.  Salamander evolution across a latitudinal cline in gape-limited predation risk , 2008 .

[13]  S. Wissinger.  Niche Overlap and the Potential for Competition and Intraguild Predation Between Size‐Structured Populations , 1992 .

[14]  Michael D. Dettinger,et al.  Implementing a U.S. national phenology network , 2005 .

[15]  R. Svanbäck,et al.  UvA-DARE ( Digital Academic Repository ) Cannibalism in a size-structured population : energy extraction and control , 2022 .

[16]  J. Thompson,et al.  VARIATION IN INTERSPECIFIC INTERACTIONS , 1988 .

[17]  J. Bosch,et al.  Effect of temperature on Osmia lignaria (Hymenoptera: Megachilidae) prepupa-adult development, survival, and emergence. , 2005, Journal of economic entomology.

[18]  E. J. Maly.  Resource overlap between co-occurring copepods: effects of predation and environmental fluctuation , 1976 .

[19]  Marcel E. Visser,et al.  Predicting adaptation of phenology in response to climate change, an insect herbivore example , 2007 .

[20]  L. Greenberg,et al.  Juvenile Competitive Bottlenecks: The Perch (Perca Fluviatilis)-Roach (Rutilus Rutilus) Interaction , 1990 .

[21]  J. Stachowicz.  Mutualism, Facilitation, and the Structure of Ecological Communities , 2001 .

[22]  G. Lei,et al.  Parasitoid–host metapopulation dynamics: the causes and consequences of phenological asynchrony , 2004 .

[23]  J. Bascompte,et al.  Global change and species interactions in terrestrial ecosystems. , 2008, Ecology letters.

[24]  N. Pettorelli,et al.  Timing and abundance as key mechanisms affecting trophic interactions in variable environments. , 2005, Ecology letters.

[25]  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.

[26]  Carlos J. Melián,et al.  The nested assembly of plant–animal mutualistic networks , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Tim G Benton,et al.  Complex population dynamics and complex causation: devils, details and demography , 2006, Proceedings of the Royal Society B: Biological Sciences.

[28]  J. Levine,et al.  Rainfall effects on rare annual plants , 2008 .

[29]  R. Dirzo,et al.  Ontogenetic switches from plant resistance to tolerance: minimizing costs with age? , 2007, Ecology letters.

[30]  H. Wilbur.  Complex Life Cycles , 1980 .

[31]  C. Rahbek,et al.  Avian migrants adjust migration in response to environmental conditions en route , 2008, Biology Letters.

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

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

[34]  J. Abatzoglou,et al.  Tracking the rhythm of the seasons in the face of global change: phenological research in the 21st century. , 2009 .

[35]  T. Whitham,et al.  The Continuum of Plant Responses to Herbivory: The Influence of Plant Association, Nutrient Availability, and Timing , 1989, The American Naturalist.

[36]  V. Rudolf,et al.  Emergent impacts of cannibalism and size refuges in prey on intraguild predation systems , 2008, Oecologia.

[37]  V. Rudolf.  The influence of size-specific indirect interactions in predator-prey systems. , 2006, Ecology.

[38]  Judith L. Bronstein,et al.  ATTRACTING ANTAGONISTS: DOES FLORAL NECTAR INCREASE LEAF HERBIVORY? , 2004 .

[39]  V. Rudolf.  THE IMPACT OF CANNIBALISM IN THE PREY ON PREDATOR-PREY SYSTEMS. , 2008, Ecology.

[40]  G. Kudo,et al.  Does seed production of spring ephemerals decrease when spring comes early? , 2004, Ecological Research.

[41]  P. Starks,et al.  The ontogeny of immunity: development of innate immune strength in the honey bee (Apis mellifera). , 2008, Journal of insect physiology.

[42]  Jacob Weiner,et al.  Mechanisms determining the degree of size asymmetry in competition among plants , 1998, Oecologia.

[43]  E. Werner,et al.  THE ONTOGENETIC NICHE AND SPECIES INTERACTIONS IN SIZE-STRUCTURED POPULATIONS , 1984 .

[44]  D. E. Scott,et al.  Effects of Hatching Time for Larval Ambystomatid Salamanders , 2002, Copeia.

[45]  C. Holzapfel,et al.  BIDIRECTIONAL FACILITATION AND INTERFERENCE BETWEEN SHRUBS AND ANNUALS IN THE MOJAVE DESERT , 1999 .

[46]  G. Davidowitz,et al.  Reproductive biology of Datura wrightii: the benefits of a herbivorous pollinator. , 2009, Annals of botany.

[47]  O. Phillips,et al.  Extinction risk from climate change , 2004, Nature.

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

[49]  V. Rudolf.  Consequences of size structure in the prey for predator-prey dynamics: the composite functional response. , 2008, The Journal of animal ecology.

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

[51]  Brian D. Inouye,et al.  RESPONSE SURFACE EXPERIMENTAL DESIGNS FOR INVESTIGATING INTERSPECIFIC COMPETITION , 2001 .

[52]  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.

[53]  M. D. Schwartz.  Phenology: An Integrative Environmental Science , 2003, Tasks for Vegetation Science.

[54]  C. Parmesan.  Ecological and Evolutionary Responses to Recent Climate Change , 2006 .

[55]  Pejman Rohani,et al.  Two-species asymmetric competition: effects of age structure on intra- and interspecific interactions. , 2007, The Journal of animal ecology.

[56]  Michael D. Abràmoff,et al.  Image processing with ImageJ , 2004 .

[57]  Lennart Persson,et al.  Size-Structured Populations , 1988, Springer Berlin Heidelberg.

[58]  V. Rudolf.  Impact of cannibalism on predator-prey dynamics: size-structured interactions and apparent mutualism. , 2008, Ecology.

[59]  H. Wilbur.  Interactions Between Growing Predators and Growing Prey , 1988 .

[60]  G. Davidowitz,et al.  Nectar usage in a southern Arizona hawkmoth community , 2008 .

[61]  P. Coley,et al.  Effects of leaf age and plant life history patterns on herbivory , 1980, Nature.

[62]  O. Edenhofer,et al.  Mitigation from a cross-sectoral perspective , 2007 .

[63]  Bo Ebeman,et al.  Size-Structured Populations: Ecology and Evolution , 2011 .

[64]  E. Mccauley,et al.  The influence of size‐dependent life‐history traits on the structure and dynamics of populations and communities , 2003 .

[65]  G. Polis,et al.  Complex Trophic Interactions in Deserts: An Empirical Critique of Food-Web Theory , 1991, The American Naturalist.

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

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

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

[69]  Jane Memmott,et al.  Global warming and the disruption of plant-pollinator interactions. , 2007, Ecology letters.

[70]  James H. Brown,et al.  Effects of size and temperature on developmental time , 2002, Nature.

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

[72]  R. Marquis,et al.  Facing herbivory as you grow up: the ontogeny of resistance in plants. , 2005, Trends in ecology & evolution.

[73]  Size‐dependent foraging capacities and intercohort competition in an ontogenetic omnivore (Arctic char) , 2005 .

[74]  G. Polis,et al.  Food Web Complexity and Community Dynamics , 1996, The American Naturalist.

[75]  M. Blackman,et al.  Immunity and age: living in the past? , 2006, Trends in Immunology.