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Abstract Many critical drivers of ecological systems exhibit regular scaling relationships, yet the underlying mechanisms explaining these relationships are often unknown. Trophic interaction strengths, which underpin ecosystem stability and dynamics, are no exception, exhibiting statistical scaling relationships with predator and prey traits that lack causal, evolutionary explanations. Here we propose two universal rules to explain the scaling of trophic interaction strengths through the relationship between a predator’s feeding rate and its prey’s density --- the so-called predator functional response. First, functional responses must allow predators to meet their energetic demands when prey are rare. Second, functional responses should approach their maxima near the highest prey densities that predators experience. We show that independently parameterized mathematical equations derived from these two rules predict functional response parameters across over 2,100 functional response experiments. The rules further predict consistent patterns of feeding rate saturation among predators, a slow-fast continuum among functional response parameters, and the allometric scaling of those parameters. The two rules thereby offer a potential ultimate explanation for the determinants of trophic interaction strengths and their scaling, revealing the importance of ecologically realized constraints to the complex, adaptive nature of functional response evolution. 

Abstract Ecologists differ in the degree to which they consider the linear Type I functional response to be an unrealistic versus sufficient representation of predator feeding rates. Empiricists tend to consider it unsuitably non-mechanistic and theoreticians tend to consider it necessarily simple. Holling’s original rectilinear Type I response is dismissed by satisfying neither desire, with most compromising on the smoothly saturating Type II response for which searching and handling are assumed to be mutually exclusive activities. We derive a “multiple-prey-at-a-time” response and a generalization that includes the Type III to reflect predators that can continue to search when handling an arbitrary number of already-captured prey. The multi-prey model clarifies the empirical relevance of the linear and rectilinear models and the conditions under which linearity can be a mechanistically-reasoned description of predator feeding rates, even when handling times are long. We find support for linearity in 35% of 2,591 compiled empirical datasets and support for the hypothesis that larger predator-prey body-mass ratios permit predators to search while handling greater numbers of prey. Incorporating the multi-prey response into the Rosenzweig-MacArthur population-dynamics model reveals that a non-exclusivity of searching and handling can lead to coexistence states and dynamics that are not anticipated by theory built on the Type I, II, or III response models. In particular, it can lead to bistable fixed-point and limit-cycle dynamics with long-term crawl-by transients between them under conditions where abundance ratios reflect top-heavy food webs and the functional response is linear. We conclude that functional response linearity should not be considered empirically unrealistic but also that more cautious inferences should be drawn in theory presuming the linear Type I to be appropriate. 

Abstract Predator and prey traits are important determinants of the outcomes of trophic interactions. In turn, the outcomes of trophic interactions shape predator and prey trait evolution. How species' traits respond to selection from trophic interactions depends crucially on whether and how heritable species' traits are and their genetic correlations. Of the many traits influencing the outcomes of trophic interactions, body size and movement traits have emerged as key traits. Yet, how these traits shape and are shaped by trophic interactions is unclear, as few studies have simultaneously measured the impacts of these traits on the outcomes of trophic interactions, their heritability, and their correlations within the same system.We used outcrossed lines of the ciliate protistParamecium caudatumfrom natural populations to examine variation in morphology and movement behaviour, the heritability of that variation, and its effects onParameciumsusceptibility to predation by the copepodMacrocyclops albidus.We found that theParameciumlines exhibited heritable variation in body size and movement traits. In contrast to expectations from allometric relationships, body size and movement speed showed little covariance among clonal lines. The proportion ofParameciumconsumed by copepods was positively associated withParameciumbody size and velocity but with an interaction such that greater velocities led to greater predation risk for large body‐sized paramecia but did not alter predation risk for smaller paramecia. The proportion of paramecia consumed was not related to copepod body size. These patterns of predation risk and heritable trait variation in paramecia suggest that copepod predation may act as a selective force operating independently on movement and body size and generating the strongest selection against large, high‐velocity paramecia.Our results illustrate how ecology and genetics can shape potential natural selection on prey traits through the outcomes of trophic interactions. Further simultaneous measures of predation outcomes, traits, and their quantitative genetics will provide insights into the evolutionary ecology of species interactions and their eco‐evolutionary consequences. Read the freePlain Language Summaryfor this article on the Journal blog. 

Abstract Predator feeding rates (described by their functional response) must saturate at high prey densities. Although thousands of manipulative functional response experiments show feeding rate saturation at high densities under controlled conditions, it remains unclearhowsaturated feeding rates are at natural prey densities. The general degree of feeding rate saturation has important implications for the processes determining feeding rates and how they respond to changes in prey density. To address this, we linked two databases—one of functional response parameters and one on mass–abundance scaling—through prey mass to calculate a feeding rate saturation index. We find that: (1) feeding rates may commonly be unsaturated and (2) the degree of saturation varies with predator and prey taxonomic identities and body sizes, habitat, interaction dimension and temperature. These results reshape our conceptualisation of predator–prey interactions in nature and suggest new research on the ecological and evolutionary implications of unsaturated feeding rates.