Earl E. Werner

An Experimental Test of the Effects of Predation Risk on Habitat Use in Fish

We present an experiment designed to test the hypothesis that fish respond to both relative predation risk and habitat profitability in choosing habitats in which to feed. Identical populations of three size—classes of bluegill sunfish (Lepomis macrochirus) were stocked on both sides of a divided pond (29 m in diameter), and eight piscivorous largemouth bass (Micropterus salmoides) were introduced to one side. Sizes of both species were chosen such that the small class of bluegills was very vulnerable to the bass, whereas the largest class was invulnerable to bass predation. We then compared mortality, habitat use, and growth of each size—class in the presence and absence of the bass. Only the small size—class suffered significant mortality from the bass (each bass consumed on average about one small bluegill every 3.8 d); the two larger size—classes exhibited similar mortality rates on both sides of the pond. In the absence of the bass, we found that habitat use of all size—classes was similar and that the pattern of habitat use maximized foraging return rates (Werner et al. 1983). In the presence of the bass the two larger size—classes chose habitats to maximize return rates, but the small size—class obtained a greater fraction of its diet from the vegetation habitat, where foraging return rates were only one—third of those in the more open habitats. The small size—class further exhibited a significant depression in individual growth in the presence of the bass; the growth increment during the experiment was 27% less than that for small bluegills in the absence of the bass. Because of the reduced utilization of more open habitats by the small fish in the presence of bass, resources in these habitats were released to the larger size—classes, which showed greater growth in the presence of the bass than in its absence. We develop methods to predict the additional mortality expected on a cohort due to a reduction in growth rate (because individuals are spending a longer time in vunerable sizes), and discuss and potential for predation risk to enforce size—class segregation, which leads de facto to resource partitioning.

A REVIEW OF TRAIT‐MEDIATED INDIRECT INTERACTIONS IN ECOLOGICAL COMMUNITIES

In this paper we review the empirical studies documenting trait-mediated indirect interactions (TMIIs) in food webs. Basic models and empirical approaches that form the foundation of our conceptualization of species interactions generally assume that interactions are an intrinsic property of the two interacting species and therefore are governed by their respective densities. However, if a species reacts to the presence of a second species by altering its phenotype, then the trait changes in the reacting species can alter the per capita effect of the reacting species on other species and, consequently, population density or fitness of the other species. Such trait-mediated indirect interactions can reinforce or oppose density-mediated effects and have been largely overlooked by community ecologists. We first briefly develop the case for the broad mechanistic basis for TMIIs and then review the direct evidence for TMIIs in various permutations of simple three- to four-species food webs. We find strong evid...

Ecological Consequences of the Trade-Off between Growth and Mortality Rates Mediated by Foraging Activity

Animals are frequently faced with trade-offs created by the fact that both resource acquisition and risk of mortality increase with activity, for example, with foraging speed or time spent foraging. We develop models predicting adaptive responses for both foraging speed and proportion of time active when individual growth rate and mortality risk are functions of these variables. Using the criterion that animals should minimize the ratio of mortality to growth rates, we show that, when both growth and mortality rates are linear with activity levels, the latter should be either maximal or minimal depending on resource level. If growth rate is a decelerating function of activity, then speed or time active should decrease with increases in resources, handling time, or the effect of activity on mortality rate. By contrast, if mortality rate unrelated to activity increases, then activity rate also should increase. We also develop predictions for cases in which time horizon is critical using a dynamic programming framework. The general patterns of predicted activity responses are similar to the time-invariant analytical solutions, but foraging speed is reduced relative to the analytical solutions when time remaining is long or when accumulated reserves are high. This effect is ameliorated when accumulated reserves (size) increase resource capture efficiency or reduce mortality risk. If resources decline with time (e.g., because of competition) optimal foraging speeds are also higher than predicted by the analytical solutions. We discuss the relation of our predictions to previous models and the available empirical evidence. The majority of available data appear to be consistent with our models, and in some cases quantitative comparisons are quite close. Finally, we discuss the implications of our results for ontogenetic changes in behavior and for population- and community-level phenomena, particularly the role of activity responses in competitive interactions and indirect effects and patterns of coexistence among competitors.

Ontogenetic Habitat Shifts in Bluegill: The Foraging Rate‐Predation Risk Trade‐off

The bluegill sunfish (Lepomis macrochirus) undergoes several habitat shifts between the littoral and pelagic zones of small lakes during its life history. After hatching in the littoral zone, bluegill fry migrate to the pelagic zone to feed on zooplankton. In this study the fry then returned to the littoral zone in four different lakes at a relatively constant size of 12.5 mm standard length. Several years are spent feeding in the littoral zone vegetation before the bluegill again shifts to feeding on zooplankton, first in the water column above littoral vegetation and subsequently in the true pelagic zone. This shift to feeding on zooplankton occurred at a specific body size within a lake, but the size ranged from 50 to 83 mm among five different lakes. The size at which the shift occurred was directly correlated with the density of the major predator of the bluegill in these lakes, the largemouth bass (Micropterus salmoides). We demonstrate that the bluegill is faced with a growth (or feeding) rate-predation risk trade-off in making these habitat shifts. Analyses of stomach contents, the growth of small fish caged in the pelagic zone, and predictions of foraging rates in both habitats all indicate that the pelagic zone is the more profitable habitat for all size classes of the bluegill. Through a series of pond experiments we further show that risk of predation by largemouth bass was 40-80 times as great for small bluegills in the open water as for those in the vegetation. We interpret the patterns of habitat use by the bluegill in terms of a model that explicitly weights the costs (predation) and benefits (growth) of making a size-specific habitat shift to the pelagic. Finally, we discuss evidence that the bluegill can facultatively respond to changes in feeding rates and predation risk, and the consequences of such ontogenetic habitat shifts to community dynamics.

Amphibian Metamorphosis: Growth Rate, Predation Risk, and the Optimal Size at Transformation

Many taxa have evolved complex life cycles featuring a dramatic shift in habitat or resource use at metamorphosis. Despite their prevalence and unique characteristics, we understand little about the adaptive properties and evolution of these life histories. I offer a conceptual framework that considers how size-specific growth and mortality rates in both habitats interact with size at metamorphosis to affect lifetime fitness. This model predicts the size at metamorphosis that maximizes fitness, and I use this framework to interpret the wide variation in the life history structure of the amphibians. In particular, I speculate on the adaptive significance of the tadpole stage of the anurans and on the cause of variation in the size at metamorphosis both between and within anuran families. Further, I predict the conditions under which direct development or paedomorphosis will be selected for, and I offer hypotheses on the selective factors that may contribute to the three-stage life history of the newts. Finally, I comment on the evolution and maintenance of complex life histories.

Behavioral and Life‐Historical Responses of Larval American Toads to an Odonate Predator

This study examines the responses of larval American toads (Bufo ameri- canus) to the non-lethal presence of an odonate predator (Anax junius). We performed a laboratory experiment where toad larvae were raised at four food rations crossed with the non-lethal presence (i.e., constrained Anax) and absence of the predator. Tadpoles facul- tatively responded by metamorphosing at smaller sizes in the presence of the predator and at lower food rations. Tadpoles also responded behaviorally to the presence of predators by reducing activity and altering spatial distribution. These latter reactions appeared to contribute to reduced growth rates in the presence of the predator at a given food level. We attempted to separate the effect of the predator on size at metamorphosis into com- ponents due to the effect on growth and to more direct effects of the predator, by comparing size at metamorphosis for individuals growing at the same rate in the presence and absence of the predator (i.e., at different food levels). Our data suggest that the metamorphic response may be mediated primarily through the behavioral effects on growth, which then affect size at metamorphosis. These results are consistent with theories of amphibian metamor- phosis that predict that size at metamorphosis should depend on the relation between growth opportunities and risk of mortality in the larval and adult habitats. We discuss the importance of non-lethal effects of predators on prey performance, species interactions, and the evolution of prey defenses.

Experimental tests of optimal habitat use in fish: the role of relative habitat profitability.

Utilizing optimal foraging theory and laboratory estimates of foraging costs, we predict the choice of foods and use of habitats by fish in the field. These predictions are tested with the bluegill sunfish (Lepomis macrochirus) foraging in three habitats (open water, sediments, and vege- tation) in a pond. Relations describing prey encounter rates in each habitat as a function of prey size, prey density, and fish size were derived from laboratory experiments. These relations permitted us to estimate prey encounter rates based on weekly prey samples in each habitat of the pond. We then determined the optimal diet and profitability (net energy return) for each habitat through time. Predictions of optimal diet exhibited good qualitative correspondence to the actual diet of the fish in the open water and vegetation, although we consistently predicted a slightly narrower diet than the fish were choosing. The model correctly predicted the magnitude of the change in size selection on Daphnia pulex with fish size and with decline in prey density. Predictions of optimal diet in the sediments were considerably in error apparently due to a tendency for late-instar midges to burrow deep in the sediments, thereby becoming unavailable to the fish. In this case habitat profitabilities were computed simply on the basis of the actual observed diet. Predictions of optimal habitat use, i.e., when the fish should switch habitats to maximize feeding rates, showed striking correspondence to the actual habitat use of the fish; the bluegills switched from feeding in the open water column to feeding from the sediments within a few days of our predictions. The actual habitat use pattern differs dramatically from a null model of random habitat use. We indicate how this approach may be useful in studying intra- and interspecific exploitative interactions.

Filling key gaps in population and community ecology

We propose research to fill key gaps in the areas of population and community ecology, based on a National Science Foundation workshop identifying funding priorities for the next 5-10 years. Our vision for the near future of ecology focuses on three core areas: predicting the strength and context-dependence of species interactions across multiple scales; identifying the importance of feedbacks from individual interactions to ecosystem dynam- ics; and linking pattern with process to understand species coexistence. We outline a combination of theory devel- opment and explicit, realistic tests of hypotheses needed to advance population and community ecology.

Species Packing and Niche Complementarity in Three Sunfishes

This study develops a method to relate foraging theory to species-packing theory. Cost curves, which rank prey by their cost-benefit ratio to the predator, are quantitatively determined for three species of sunfishes (Centrarchidae) that differ systematically in their morphology. The cost curves are used to estimate extremes in the range of food sizes in the diet of a fish given its size and morphology (species). The distribution of available resources is found to be lognormal and, with the above diet ranges, permits the calculation of the niche width and location on the food size axis for individual fish. The extremes in niche width and location for size-distributed populations of these species are then determined by combining and weighing the contribution of each size class. Overlap on the food size coordinate for populations of Lepomis macrochirus and Micropterus salmoides is shown to be very close to that predicted by current species-packing theory. It is predicted that these species occupy similar habitats and segregate on the food size axis while the third species, which is intermediate in morphology (L. cyanellus), should be excluded from these habitats and show complementarity on niche dimensions. Data on habitat utilization of these species from natural communities confirm these predictions. Species packing on the food size coordinate is discussed in relation to species populations which are size distributed.

The contribution of trait-mediated indirect effects to the net effects of a predator

Many prey modify traits in response to predation risk and this modification of traits can influence the preys resource acquisition rate. A predator thus can have a “nonlethal” impact on prey that can lead to indirect effects on other community members. Such indirect interactions are termed trait-mediated indirect interactions because they arise from a predators influence on prey traits, rather than prey density. Because such nonlethal predator effects are immediate, can influence the entire prey population, and can occur over the entire prey lifetime, we argue that nonlethal predator effects are likely to contribute strongly to the net indirect effects of predators (i.e., nonlethal effects may be comparable in magnitude to those resulting from killing prey). This prediction was supported by an experiment in which the indirect effects of a larval dragonfly (Anax sp.) predator on large bullfrog tadpoles (Rana catesbeiana), through nonlethal effects on competing small bullfrog tadpoles, were large relative to indirect effects caused by density reduction of the small tadpoles (the lethal effect). Treatments in which lethal and nonlethal effects of Anax were manipulated independently indicated that this result was robust for a large range of different combinations of lethal and nonlethal effects. Because many, if not most, prey modify traits in response to predators, our results suggest that the magnitude of interaction coefficients between two species may often be dynamically related to changes in other community members, and that many indirect effects previously attributed to the lethal effects of predators may instead be due to shifts in traits of surviving prey.