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The ''Goldilocks Factor'' in Food Webs

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The ''Goldilocks Factor'' in Food Webs COMMENTARY The ‘‘Goldilocks factor’’ in food webs Eric L. Berlow*†‡, Ulrich Brose†§, and Neo D. Martinez† *University of California, Merced, Sierra Nevada Research Institute, Yosemite National Park, CA 95389; †Pacific Ecoinformatics and Computational Ecology Laboratory, 1604 McGee Avenue, Berkeley, CA 94703; and §Department of Biology, Darmstadt University of Technology, Schnittspahnstrasse 10, 64287 Darmstadt, Germany n a well known children’s tale, the harvesting, of one species might cause little girl, Goldilocks, nearly gets dramatic changes in the abundances of herself eaten by bears by boldly other species. Recent work (16–20) has choosing between the three bears’ shown how the body sizes of predators Iporridge bowls: one too hot and another and their prey can determine feeding rates too cold. In this issue of PNAS, the article and biomass flows in food webs. Although ‘‘Size, foraging, and food web structure,’’ large flows of biomass from prey to pred- by Petchey et al. (1), tells a similar story ator may not indicate strong predator con- of food webs in which predator species trol of prey populations (21), such flows choose between prey species that are too can still drive population dynamics (22). large or too small. In doing so, the au- Thus, the coupling of foraging theory with thors show how an easily observed species allometric considerations of metabolic trait—body size—can address long- Fig. 1. Cross-scale integration from individuals to theory may unite the structure of food standing ecological questions about who ecosystems. Petchey et al. (1) model organisms’ webs with biomass flows to predict spe- eats whom in complex natural communi- size-based foraging and integrate it with the net- cies’ population dynamics, which in turn work structure of food webs (red arrow). This work ties. Although previous models explain can elucidate the strengths of dynamic contributes to a broad research program that uses coupling between species (8). In this case, well the general network properties of body size to integrate different levels of trophic food webs, Petchey et al. go further by organization and interactions (blue arrows). species’ influence on each other and on explaining how the particular links found the outcomes of species loss are seen as between species within specific food webs emergent properties of population dynam- can result from optimal foraging of preda- The specific idea that the network ics, driven by foraging behavior and tors on prey that are neither too large nor structure of food webs may emerge from biomass flows that are constrained by spe- too small. Like Goldilocks, optimal preda- optimally foraging individuals is intuitively cies’ body size (15). tors choose food that is ‘‘just right.’’ appealing but technically challenging. Body size also allows integration of the In choosing their food, predators and Petchey et al.’s (1) two mathematical for- overall dynamic persistence of food webs other consumers create food webs—the aging functions require that three or four with the diversity and complexity of food feeding networks among species that sus- parameters be fitted to each food web. web structure (10). The mathematical im- tain the life support systems on earth. Further work is needed to address the probability of large, complex networks Ecologists continue to discover fascinating unexplained variability in these parame- persisting dynamically was recognized regularities in the structure of this interde- ters (up to 26 orders of magnitude) and early on (4). More recent theory finds pendent complexity (2, 3). Elucidating the to reduce the analytical complexity of for- that body size ratios between predators mechanisms responsible for these regulari- mulating and fitting them. Nonetheless, an and their prey occupy a Goldilocks-type ties is a fundamental step in tackling long- important contribution is their linking of ‘‘sweet spot’’ that enables diversity to standing questions in ecology that range body size to prey-handling times within enhance both system-level (9, 16) and from ‘‘What confers stability to complex the foraging functions, both of which fac- subsystem-level (22) stability. These stabi- lizing predator–prey body mass ratios are ecosystems?’’ (4) to ‘‘How does species tors set upper bounds to predators’ prey remarkably consistent with those found in loss alter the abundance of other spe- size. The more successful of the two func- the most comprehensive empirical data cies?’’ (5). Surprisingly simple rule-based tions also sets a lower limit to the body available (23). Buffering by larger organ- models successfully capture the overall sizes of prey species. This concept of con- isms’ low metabolic rate (9, 22) and structure of real food webs (2, 6, 7) and sumers feeding on contiguous ranges of higher mobility among variably productive enable further theoretical exploration by prey body masses within boundaries is patches (24) appear to underlie such sta- stochastically generating webs that mimic deeply rooted in foraging theory (12, 13) bility. Petchey et al. (1) provide more and is highly consistent with observed the overall structure of real webs (6, mechanistic insight into such allometric food web structure (14). However, this 8–10). However, such models lack mecha- integration of link-level biomass flows research has lacked the mechanistic bridge nistic explanations for their input parame- with population dynamics and system-level between foraging theory and food web ters and poorly predict the actual links in stability by showing that these parametric real food webs. Petchey et al. (1) have topology. Petchey et al. provide this bridge sweet spots are consistent with optimal synthesized the allometry of body size by integrating both the foraging conse- foraging. with optimal foraging theory to address quences of body size and the energy con- Leaving dynamics aside, the connection both the first limitation (11), and now the tent of individual prey. between body size and comparative analy- second, by assuming that predators are Between the narrow scale of an individ- more efficient at consuming prey that are ual’s foraging and the broad scale of smaller than themselves, but not too community patterns lie the strengths of Author contributions: E.L.B., U.B., and N.D.M. wrote the small. This ‘‘Goldilocks’’ model of food interactions between populations (15)— paper. choice successfully predicts up to 65% of another area of trophic ecology being in- The authors declare no conflict of interest. the feeding links in real food webs, and in tegrated by the use of body size (Fig. 1). See companion article on page 4191. doing so helps to solve the notoriously Understanding interaction strength in- ‡To whom correspondence should be addressed. E-mail: difficult problem of integrating ecology volves the critical ecological challenge of [email protected]. from individuals to ecosystems (Fig. 1). predicting when the extinction, or over- © 2008 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0800967105 PNAS ͉ March 18, 2008 ͉ vol. 105 ͉ no. 11 ͉ 4079–4080 Downloaded by guest on October 1, 2021 ses of the network structure of ecosystems These failures offer important insights ganism is to subdue and digest. Still, eco- also benefits from the mechanistic detail into the limits of body size alone as an logical interactions involve much more that Petchey et al. (1) provide. Seminal explanatory panacea. Predaceous and than just feeding (e.g., mutualisms, ecosys- early work found that species’ diets within aquatic herbivorous links were, as tem engineering) (38), and feeding in- a food web can form an unbroken seg- expected, much better predicted than par- volves more than just prey body size. But ment, or interval, along a fixed sequence asitic, parasitoid, and pathogenic interac- body size and feeding links seem to be of all species within the food web (25). tions. Similarly, terrestrial herbivorous the ‘‘low-hanging fruit’’ of ecological com- Body size helps explain the hierarchy in interactions were not as well predicted as plexity research. Both are universal and one of the earliest structural food web aquatic ones, and the three nondesert ter- relatively easy to measure for many organ- models, which proposed that larger or- restrial webs were fit rather poorly. All of isms. All species are made up of organ- dered species can eat smaller ordered spe- this suggests that some foraging modes fit isms that have mass, and no species we cies, but not vice versa (26). These two size-based optimal foraging models better know of escapes the food web. As such, ideas were then synthesized by the ‘‘niche than others. Body size may be most im- food webs form an essential core of criti- model’’ that assigned consumers unbroken portant to gape-limited or visual predators cal interdependence created by the class feeding ranges on a niche dimension that and perhaps unimportant to insect herbi- of species interactions for which we tend tends to be located below the consumer vores that choose plants on the basis on to have the most comprehensive data (27). Although this model has been shown leaf chemistry or plant defenses. Similarly, (35). Similarly, body size elegantly links to successfully predict overall food web energy maximization may be balanced by energy content, feeding behavior, and structure (6, 7, 28), Petchey et al. provide avoiding the risk of being consumed (32) metabolic needs. Does this mean that we a testable mechanistic interpretation of or by stoichiometric preferences for par- have chosen to search for our lost coins the niche axis in terms of body mass [see ticular nutrients (33). To better interpret under the lamppost simply because that is also Stouffer et al. (14)]. Such mechanisms such success and failure, it would help to are also relevant to empirical analyses of know whether a random model with fewer where the light is? We don’t think so.
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