Foraging and vulnerability traits modify predator-prey body mass allometry: freshwater macroinvertebrates as a case study.

1. Predation is often size selective, but the role of other traits of the prey and predators in their interactions is little known. This hinders our understanding of the causal links between trophic interactions and the structure of animal communities. Better knowledge of trophic traits underlying predator-prey interactions is also needed to improve models attempting to predict food web structure and dynamics from known species traits. 2. We carried out laboratory experiments with common freshwater macroinvertebrate predators (diving beetles, dragonfly and damselfly larvae and water bugs) and their prey to assess how body size and traits related to foraging (microhabitat use, feeding mode and foraging mode) and to prey vulnerability (microhabitat use, activity and escape behaviour) affect predation strength. 3. The underlying predator-prey body mass allometry characterizing mean prey size and total predation pressure was modified by feeding mode of the predators (suctorial or chewing). Suctorial predators fed upon larger prey and had ˜3 times higher mass-specific predation rate than chewing predators of the same size and may thus have stronger effect on prey abundance. 4. Strength of individual trophic links, measured as mortality of the focal prey caused by the focal predator, was determined jointly by the predator and prey body mass and their foraging and vulnerability traits. In addition to the feeding mode, interactions between prey escape behaviour (slow or fast), prey activity (sedentary or active) and predator foraging mode (searching or ambush) strongly affected prey mortality. Searching predators was ineffective in capturing fast-escape prey in comparison with the remaining predator-prey combinations, while ambush predators caused higher mortality than searching predators and the difference was larger in active prey. 5. Our results imply that the inclusion of the commonly available qualitative data on foraging traits of predators and vulnerability traits of prey could substantially increase biological realism of food web descriptions.

[1]  Steven L. Chown,et al.  Mean mass-specific metabolic rates are strikingly similar across life's major domains: Evidence for life's metabolic optimum , 2008, Proceedings of the National Academy of Sciences.

[2]  M. Emmerson,et al.  Predator–prey body size, interaction strength and the stability of a real food web , 2004 .

[3]  A. Mougi,et al.  Evolutionary ecology of inducible morphological plasticity in predator–prey interaction: toward the practical links with population ecology , 2009, Population Ecology.

[4]  Sara Taskinen,et al.  smatr 3– an R package for estimation and inference about allometric lines , 2012 .

[5]  K. Andersen,et al.  Asymptotic Size Determines Species Abundance in the Marine Size Spectrum , 2006, The American Naturalist.

[6]  P. Tikkanen,et al.  The roles of active predator choice and prey vulnerability in determining the diet of predatory stonefly (Plecoptera) nymphs , 1997 .

[7]  J. Lighton,et al.  Scaling of insect metabolic rate is inconsistent with the nutrient supply network model , 2007 .

[8]  Neo D. Martinez,et al.  Simple rules yield complex food webs , 2000, Nature.

[9]  G. Woodward,et al.  Body‐size determinants of niche overlap and intraguild predation within a complex food web , 2002 .

[10]  W. Murdoch,et al.  EFFECTS OF THE GENERAL PREDATOR, NOTONECTA (HEMIPTERA) UPON A FRESHWATER COMMUNITY , 1984 .

[11]  M. Uriarte,et al.  Experimental evidence for a behavior-mediated trophic cascade in a terrestrial food chain. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[12]  D. Réale,et al.  Personality and the emergence of the pace-of-life syndrome concept at the population level , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[13]  Oswald J. Schmitz,et al.  Trophic cascades : the primacy of trait-mediated indirect interactions , 2004 .

[14]  J. Elser,et al.  Soil acidity, ecological stoichiometry and allometric scaling in grassland food webs , 2009, Global Change Biology.

[15]  R. W. Sheldon,et al.  The Size Distribution of Particles in the OCEAN1 , 1972 .

[16]  S. Downes.  Size-dependent predation by snakes: selective foraging or differential prey vulnerability? , 2002 .

[17]  F. A. Streams.  Effect of prey size on attack components of the functional response by Notonecta undulata , 1994, Oecologia.

[18]  Jens O. Riede,et al.  Stepping in Elton's footprints: a general scaling model for body masses and trophic levels across ecosystems. , 2011, Ecology letters.

[19]  Rudolf P. Rohr,et al.  Phylogenetic signal in predator-prey body-size relationships. , 2011, Ecology.

[20]  Christian Mazza,et al.  Modeling Food Webs: Exploring Unexplained Structure Using Latent Traits , 2010, The American Naturalist.

[21]  Martin Wikelski,et al.  The physiology/life-history nexus , 2002 .

[22]  J. Norberg,et al.  Trophic interactions in rockpool food webs: regulation of zooplankton and phytoplankton by Notonecta and Daphnia , 1998 .

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

[24]  P. Giller.  THE CONTROL OF HANDLING TIME AND ITS EFFECTS ON THE FORAGING STRATEGY OF A HETEROPTERAN PREDATOR, NOTONECTA , 1980 .

[25]  G. Woodward,et al.  The impact of a sit-and-wait predator: separating consumption and prey emigration , 2002 .

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

[27]  R. Pastorok.  PREY VULNERABILITY AND SIZE SELECTION BY CHAOBORUS LARVAE , 1981 .

[28]  K. Šimek,et al.  Prey-size selection by freshwater flagellated protozoa , 1990 .

[29]  A. Rossberg,et al.  Food webs: experts consuming families of experts. , 2005, Journal of theoretical biology.

[30]  C. Wesenberg‐Lund.  Biologie der Süsswasserinsekten , 1943 .

[31]  G. Woodward,et al.  Body Size: Body size and predatory interactions in freshwaters: scaling from individuals to communities , 2007 .

[32]  P. Bailey.  The effect of predation risk on the predatory behaviour of a sit-and-wait predator,Ranatra dispar (Heteroptera: Nepidae), the water stick insect , 1986, Journal of Ethology.

[33]  A. J. Riveros,et al.  Metabolic scaling in insects supports the predictions of the WBE model. , 2011, Journal of insect physiology.

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

[35]  Björn C. Rall,et al.  Taxonomic versus allometric constraints on non‐linear interaction strengths , 2011 .

[36]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[37]  Drew Purves,et al.  The Probabilistic Niche Model Reveals the Niche Structure and Role of Body Size in a Complex Food Web , 2010, PloS one.

[38]  J. Stachowicz,et al.  Behavioral Types of Predator and Prey Jointly Determine Prey Survival: Potential Implications for the Maintenance of Within-Species Behavioral Variation , 2011, The American Naturalist.

[39]  M. Hasegawa,et al.  Dietary Program for Rearing the Larvae of a Diving Beetle, Dytiscus sharpi (Wehncke), in the Laboratory (Coleoptera: Dytiscidae) , 2009 .

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

[41]  C. F. Gaymer,et al.  Prey selection and predatory impact of four major sea stars on a soft bottom subtidal community , 2004 .

[42]  Werner Ulrich,et al.  BODY SIZES OF CONSUMERS AND THEIR RESOURCES , 2005 .

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

[44]  U. Dieckmann,et al.  How trophic interaction strength depends on traits , 2010, Theoretical Ecology.

[45]  James H. Brown,et al.  Body Size: The metabolic theory of ecology and the role of body size in marine and freshwater ecosystems , 2007 .

[46]  O. Schmitz,et al.  Trait and density mediated indirect interactions in simple food webs , 2004 .

[47]  P. Barbosa,et al.  Ecology of Predator-Prey Interactions , 2005 .

[48]  M. Westoby,et al.  Bivariate line‐fitting methods for allometry , 2006, Biological reviews of the Cambridge Philosophical Society.

[49]  K. Wirtz.  Who is eating whom? Morphology and feeding type determine the size relation between planktonic predators and their ideal prey , 2012 .

[50]  D. Raffaelli,et al.  Body Size: The Structure and Function of Aquatic Ecosystems: The Structure and Function of Aquatic Ecosystems , 2007 .

[51]  P. Crowley,et al.  Modeling Arthropod Predation: Wasteful Killing by Damselfly Naiads , 1975 .

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

[53]  Owen L. Petchey,et al.  Seeing Double:: Size-Based and Taxonomic Views of Food Web Structure , 2011 .

[54]  S. Sultan,et al.  Ecological consequences of phenotypic plasticity. , 2005, Trends in ecology & evolution.

[55]  D. Boukal,et al.  Who Eats Whom in a Pool? A Comparative Study of Prey Selectivity by Predatory Aquatic Insects , 2012, PloS one.

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

[57]  L. Bersier,et al.  The signature of phylogenetic constraints on food-web structure , 2008 .

[58]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[59]  Richard J. Williams,et al.  The probabilistic niche model reveals substantial variation in the niche structure of empirical food webs. , 2011, Ecology.

[60]  Owen L. Petchey,et al.  Universal temperature and body-mass scaling of feeding rates , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[61]  S. Bayley,et al.  Effects of a top invertebrate predator (Dytiscus alaskanus; Coleoptera: Dytiscidae) on fishless pond ecosystems , 2010, Hydrobiologia.

[62]  Rudolf P. Rohr,et al.  Phylogeny versus body size as determinants of food web structure , 2012, Proceedings of the Royal Society B: Biological Sciences.

[63]  B. J. Cockrell,et al.  Predator ingestion rate and its bearing on feeding time and the theory of oprimal diets , 1978 .

[64]  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.

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

[66]  L. F. Toledo,et al.  Behavioural defences of anurans: an overview , 2011 .

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

[68]  A. Flecker,et al.  Prey preference of stoneflies: sedentary vs mobile prey , 1987 .

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

[70]  Jean Chesson,et al.  The Estimation and Analysis of Preference and Its Relatioship to Foraging Models , 1983 .

[71]  A. Flecker,et al.  Prey size selection by carnivorous stoneflies1 , 1987 .

[72]  Owen L. Petchey,et al.  Body-size distributions and size-spectra: universal indicators of ecological status? , 2010, Biology Letters.