Body‐mass constraints on foraging behaviour determine population and food‐web dynamics

1. In community and population ecology, there is a chronic gap between the classic Eltonian ecology describing patterns in abundance and body mass across species and ecosystems and the more process oriented foraging ecology addressing interactions and quantitative population dynamics. However, this dichotomy is arbitrary, because body mass also determines most species traits affecting foraging interactions and population dynamics. 2. In this review, allometric (body-mass dependent) scaling of handling times and attack rates are documented, whereas body-mass effects on Hill exponents (varying between hyperbolic type II and sigmoid type III functional responses) and predator interference coefficients are lacking. This review describes how these allometric relationships define a biological plausible parameter space for population dynamic models. 3. Consistent with the classic Eltonian description, species co-existence in consumer-resource models and tri-trophic food chains is restricted to intermediate consumer-resource body-mass ratios. Allometric population dynamic models allow understanding the processes of energy limitation and unstable dynamics leading to this restriction. Complex food webs are stabilized by high predator-prey body-mass ratios, which are consistent with those found in natural ecosystems. These high body-mass ratios yield positive diversity-stability and complexity-stability relationships thus supporting the classic picture of ecosystem stability. 4. Allometric-trophic network models, based on body mass and trophic information from ecosystems, bridge the gap between Eltonian community patterns and process-oriented foraging ecology and provide a new means to describe the dynamics and functioning of natural ecosystems.

[1]  P. Abrams.  The functional responses of adaptive consumers of two resources , 1987 .

[2]  Joan Saldaña,et al.  Body sizes of animal predators and animal prey in food webs , 1993 .

[3]  S. Levin,et al.  Size and scaling of predator-prey dynamics. , 2006, Ecology letters.

[4]  K S McCann,et al.  The dynamics of spatially coupled food webs. , 2005, Ecology letters.

[5]  C. S. Holling.  The components of prédation as revealed by a study of small-mammal prédation of the European pine sawfly. , 1959 .

[6]  Neo D. Martinez,et al.  Allometric scaling enhances stability in complex food webs. , 2006, Ecology letters.

[7]  Guy Woodward,et al.  Body size in ecological networks. , 2005, Trends in ecology & evolution.

[8]  Ralph Tollrian,et al.  Consumer‐food systems: why type I functional responses are exclusive to filter feeders , 2004, Biological reviews of the Cambridge Philosophical Society.

[9]  Susan C. Roberts,et al.  Energetic constraints on the diet of terrestrial carnivores , 1999, Nature.

[10]  Stable Url,et al.  Towards a Predator-Prey Model Incorporating Age Structure: The Effects of Predator and Prey Size on the Predation of Daphnia magna by Ischnura elegans , 1975 .

[11]  L. Ginzburg,et al.  The nature of predation: prey dependent, ratio dependent or neither? , 2000, Trends in ecology & evolution.

[12]  Jonathan M. Jeschke,et al.  PREDATOR FUNCTIONAL RESPONSES: DISCRIMINATING BETWEEN HANDLING AND DIGESTING PREY , 2002 .

[13]  S. Diehl,et al.  Size-dependent foraging efficiency, cannibalism and zooplankton community structure , 2000, Oecologia.

[14]  Annette Ostling,et al.  Unified spatial scaling of species and their trophic interactions , 2004, Nature.

[15]  Michel Loreau,et al.  The functional role of biodiversity in ecosystems: incorporating trophic complexity. , 2007, Ecology letters.

[16]  Nicolas Loeuille,et al.  Evolutionary emergence of size-structured food webs. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Carsten F. Dormann,et al.  Ecological networks - foodwebs and beyond , 2009 .

[18]  Ulrich Brose,et al.  Food‐web connectance and predator interference dampen the paradox of enrichment , 2008 .

[19]  K. Spitze.  Functional response of an ambush predator: Chaoborus americanus predation on Daphnia pulex , 1985 .

[20]  J. Bascompte,et al.  Ecological networks : beyond food webs Ecological networks – beyond food webs , 2008 .

[21]  E. Berlow,et al.  Foraging theory predicts predator-prey energy fluxes. , 2008, The Journal of animal ecology.

[22]  K. Leonardsson,et al.  Prey–predator size‐dependent functional response: derivation and rescaling to the real world , 2004 .

[23]  Donald L. DeAngelis,et al.  A MODEL FOR TROPHIC INTERACTION , 1975 .

[24]  Donald L. DeAngelis,et al.  A Model for Tropic Interaction , 1975 .

[25]  Neo D. Martinez,et al.  Scaling up keystone effects from simple to complex ecological networks , 2005 .

[26]  Neo D. Martinez,et al.  Simple prediction of interaction strengths in complex food webs , 2009, Proceedings of the National Academy of Sciences.

[27]  J. Beddington,et al.  Mutual Interference Between Parasites or Predators and its Effect on Searching Efficiency , 1975 .

[28]  Werner Ulrich,et al.  Consumer-resource body-size relationships in natural food webs. , 2006, Ecology.

[29]  Neo D. Martinez,et al.  Stabilization of chaotic and non-permanent food-web dynamics , 2004 .

[30]  S. Carpenter,et al.  Food Webs, Body Size, and Species Abundance in Ecological Community Description , 2005 .

[31]  Peter A. Abrams,et al.  THE EFFECTS OF ADAPTIVE BEHAVIOR ON THE TYPE-2 FUNCTIONAL RESPONSE' , 1990 .

[32]  Owen L Petchey,et al.  Size, foraging, and food web structure , 2008, Proceedings of the National Academy of Sciences.

[33]  Benjamin M. Bolker,et al.  COMPENSATORY LARVAL RESPONSES SHIFT TRADE‐OFFS ASSOCIATED WITH PREDATOR‐INDUCED HATCHING PLASTICITY , 2005 .

[34]  P. Yodzis,et al.  Body Size and Consumer-Resource Dynamics , 1992, The American Naturalist.

[35]  J. Lawton,et al.  Invertebrate predator-prey body size relationships: an explanation for upper triangular food webs and patterns in food web structure? , 1987, Oecologia.

[36]  M. Hassell,et al.  The Components of Arthropod Predation: I. The Prey Death-Rate , 1976 .

[37]  Richard J. Williams,et al.  Effects of network and dynamical model structure on species persistence in large model food webs , 2008, Theoretical Ecology.

[38]  Ulrich Brose,et al.  Allometric degree distributions facilitate food-web stability , 2007, Nature.

[39]  Elizabeth T. Borer,et al.  A cross-ecosystem comparison of the strength of trophic cascades , 2002 .

[40]  Leslie A. Real,et al.  The Kinetics of Functional Response , 1977, The American Naturalist.

[41]  Kevin S. McCann,et al.  Biological Conditions for Chaos in a Three‐Species Food Chain , 1994 .

[42]  James H. Brown,et al.  Toward a metabolic theory of ecology , 2004 .

[43]  Michel Loreau,et al.  Food-web constraints on biodiversity–ecosystem functioning relationships , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Barbara Drossel,et al.  Emergence of complexity in evolving niche-model food webs. , 2008, Journal of theoretical biology.

[45]  Jónsson,et al.  Effects of Predator-prey Body Size Ratios on the Stability of Food Chains. , 1998, Journal of Theoretical Biology.

[46]  R. Peters.  The Ecological Implications of Body Size , 1983 .

[47]  M. Kleiber.  Body size and metabolism , 1932 .

[48]  J. Shurin,et al.  The strength of trophic cascades across ecosystems: predictions from allometry and energetics , 2005 .

[49]  D. Wilson.  The Adequacy of Body Size as a Niche Difference , 1975, The American Naturalist.

[50]  J. F. Gilliam,et al.  FUNCTIONAL RESPONSES WITH PREDATOR INTERFERENCE: VIABLE ALTERNATIVES TO THE HOLLING TYPE II MODEL , 2001 .

[51]  Owen L. Petchey,et al.  Foraging biology predicts food web complexity , 2006, Proceedings of the National Academy of Sciences.

[52]  Ulrich Brose,et al.  Complex food webs prevent competitive exclusion among producer species , 2008, Proceedings of the Royal Society B: Biological Sciences.

[53]  Neil Rooney,et al.  From energetics to ecosystems : the dynamics and structure of ecological systems , 2006 .

[54]  Jaap van der Meer,et al.  Metabolic theories in ecology , 2006 .

[55]  William W. Murdoch,et al.  Functional Response and Stability in Predator-Prey Systems , 1975, The American Naturalist.