Scott D. Peacor

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...

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.

REVISITING THE CLASSICS: CONSIDERING NONCONSUMPTIVE EFFECTS IN TEXTBOOK EXAMPLES OF PREDATOR-PREY INTERACTIONS

Predator effects on prey dynamics are conventionally studied by measuring changes in prey abundance attributed to consumption by predators. We revisit four classic examples of predator-prey systems often cited in textbooks and incorporate subsequent studies of nonconsumptive effects of predators (NCE), defined as changes in prey traits (e.g., behavior, growth, development) measured on an ecological time scale. Our review revealed that NCE were integral to explaining lynx-hare population dynamics in boreal forests, cascading effects of top predators in Wisconsin lakes, and cascading effects of killer whales and sea otters on kelp forests in nearshore marine habitats. The relative roles of consumption and NCE of wolves on moose and consequent indirect effects on plant communities of Isle Royale depended on climate oscillations. Nonconsumptive effects have not been explicitly tested to explain the link between planktonic alewives and the size structure of the zooplankton, nor have they been invoked to attribute keystone predator status in intertidal communities or elsewhere. We argue that both consumption and intimidation contribute to the total effects of keystone predators, and that characteristics of keystone consumers may differ from those of predators having predominantly NCE. Nonconsumptive effects are often considered as an afterthought to explain observations inconsistent with consumption-based theory. Consequently, NCE with the same sign as consumptive effects may be overlooked, even though they can affect the magnitude, rate, or scale of a prey response to predation and can have important management or conservation implications. Nonconsumptive effects may underlie other classic paradigms in ecology, such as delayed density dependence and predator-mediated prey coexistence. Revisiting classic studies enriches our understanding of predator-prey dynamics and provides compelling rationale for ramping up efforts to consider how NCE affect traditional predator-prey models based on consumption, and to compare the relative magnitude of consumptive and NCE of predators.

TRAIT-MEDIATED INDIRECT INTERACTIONS IN A SIMPLE AQUATIC FOOD WEB

This investigation examines the role of trait-mediated indirect interactions in a simple aquatic food web. We conducted the experiments in cattle watering tanks in order to establish whether competitive and predator-prey interactions between two species are affected by other species in the system; i.e., are pairwise interaction strengths affected by the background species assemblage? We examined the survival and growth response of small bullfrog (Rana catesbeiana) and small green frog (Rana clamitans) tadpoles in the presence and absence of a competitor (large bullfrogs), the lethal presence of the larval odonate predator Tramea lacerata,and the nonlethal (caged) presence of the larval odonate predators Anax junius and Anax longipes. We demonstrate that large bullfrog competitors and caged Anax affect traits (foraging activity level) of small bullfrog and small green frog tadpoles and that these changes in traits, in turn, affect interactions of the small tadpole species with each other and with the other species. In particular, the following four trait- mediated indirect interactions were evident: (1) Presence of large bullfrog competitors increased the predation rate of Trameaon small green frogs and small bullfrogs. (2) Presence of nonlethal Anax reduced the predation rate of Tramea on small green frogs. (3) Presence of nonlethal Anax increased the competitive advantage of bullfrogs over green frogs. (4) Presence of nonlethal Anax facilitated midge invasion of the experimental units. The pro- posed mechanisms (changes in small tadpole activity) involved in these trait-mediated indirect interactions were supported by observational data on tadpole activity and resource levels in the experimental units, and in laboratory experiments examining tadpole activity responses to predators. The occurrence of strong trait-mediated indirect interactions in this simple food web underscores the potential importance of such interactions in animal com- munities.

LARGE NONLETHAL EFFECTS OF AN INVASIVE INVERTEBRATE PREDATOR ON ZOOPLANKTON POPULATION GROWTH RATE

We conducted a study to determine the contribution of lethal and nonlethal effects to a predators net effect on a preys population growth rate in a natural setting. We focused on the effects of an invasive invertebrate predator, Bythotrephes longimanus, on zooplankton prey populations in Lakes Michigan and Erie. Field data taken at multiple dates and locations in both systems indicated that the prey species Daphnia mendotae, Daphnia retrocurva, and Bosmina longirostris inhabited deeper portions of the water column as Bythotrephes biomass increased, possibly as an avoidance response to predation. This induced migration reduces predation risk but also can reduce birth rate due to exposure to cooler temperatures. We estimated the nonlethal (i.e., resulting from reduced birth rate) and lethal (i.e., consumptive) effects of Bythotrephes on D. mendotae and Bosmina longirostris. These estimates used diel field survey data of the vertical gradient of zooplankton prey density, Bythotrephes density, light intensity, and temperature with growth and predation rate models derived from laboratory studies. Results indicate that nonlethal effects played a substantial role in the net effect of Bythotrephes on several prey population growth rates in the field, with nonlethal effects on the same order of magnitude as or greater (up to 10-fold) than lethal effects. Our results further indicate that invasive species can have strong nonlethal, behaviorally based effects, despite short evolutionary coexistence with prey species.

PREDATOR EFFECTS ON AN ASSEMBLAGE OF CONSUMERS THROUGH INDUCED CHANGES IN CONSUMER FORAGING BEHAVIOR

This investigation examines how a predator-induced reduction in activity of a prey species (a “nonlethal” predator effect) affects the growth rate of the prey and, indirectly, the growth rate of competitors of the prey. We further determine how the magnitudes of these effects depend on density of the prey species. We develop a foraging model that predicts a predator will reduce the growth of a focal prey species at low prey density but have little effect at high prey density. The model also predicts that presence of the predator will indirectly facilitate growth of a competitor of the focal species, and that this effect will be negligible at low, and maximal at high, focal species density. Thus it is precisely where the effect of the predator on the growth of the focal species is minimum that the indirect effect on the competitor is maximum. We tested these predictions using a system of three species/size classes of anuran larvae and a larval odonate predator (Anax longipes) in cattle watering tanks. By c...

Lethal and nonlethal predator effects on an herbivore guild mediated by system productivity

Indirect effects propagated through intervening species in a food web have important effects on community properties. Traditionally, these indirect effects have been conceptualized as mediated through density changes of the intervening species, but it is becoming increasingly apparent that those mediated through trait (phenotypic) responses also can be very important. Because density- and trait-mediated indirect effects have different properties, it is critical that we understand the mechanisms of transmission in order to predict how they will interact, and when or where they will be important. In this study, we examined the mechanisms and consequences of the lethal (density-mediated) and nonlethal (trait-mediated) effects of a larval odonate predator on a guild of four herbivore species (a larval anuran and three species of snails) and their resources. We also manipulated system productivity in order to explore the effects of environmental context on the transmission of these two types of indirect effects. We show that trait-mediated effects arising from the predator can be very strong relative to density-mediated effects on both the competing herbivores and the species composition and production of their resources. A number of these indirect effects are shown to be contingent on productivity of the system. We further present evidence that trait- and density-mediated indirect effects originating from a predator may be transmitted independently through different routes in a food web, particularly when spatial responses of the transmitting prey are involved. Finally, effects on prey growth due to trait responses to the predator varied from negative to positive in predictable ways as a function of time and indirect effects on the larger food web. These results indicate the important role that trait-mediated indirect effects can play in trophic cascades and keystone predator interactions, and we discuss how the mechanisms involved can be incorporated in theory.

CONSUMPTIVE AND NONCONSUMPTIVE EFFECTS OF PREDATORS ON METACOMMUNITIES OF COMPETING PREY

Although predators affect prey both via consumption and by changing prey migration behavior, the interplay between these two effects is rarely incorporated into spatial models of predator-prey dynamics and competition among prey. We develop a model where generalist predators have consumptive effects (i.e., altering the likelihood of local prey extinction) as well as nonconsumptive effects (altering the likelihood of colonization) on spatially separated prey populations (metapopulations). We then extend this model to explore the effects of predators on competition among prey. We find that generalist predators can promote persistence of prey metapopulations by promoting prey colonization, but predators can also hasten system-wide extinction by either increasing local extinction or reducing prey migration. By altering rates of prey migration, predators in one location can exert remote control over prey dynamics in another location via predator-mediated changes in prey flux. Thus, the effect of predators may extend well beyond the proportion of patches they visit. In the context of prey metacommunities, predator-mediated shifts in prey migration and mortality can shift the competition-colonization trade-off among competing prey, leading to changes in the prey community as well as changes in the susceptibility of prey species to habitat loss. Consequently, native prey communities may be susceptible to invasion not only by exotic prey species that experience reduced amounts of mortality from resident predators, but also by exotic prey species that exhibit strong dispersal in response to generalist native predators. Ultimately, our work suggests that the consumptive and nonconsumptive effects of generalist predators may have strong, yet potentially cryptic, effects on competing prey capable of mediating coexistence, fostering invasion, and interacting with anthropogenic habitat alteration.

Context dependence of nonlethal effects of a predator on prey growth

Predators can have a large influence on their prey through induced changes in prey phenotype. Such “nonlethal” predator effects have been abundantly demonstrated empirically in both terrestrial and aquatic systems. But the extent to which changes in species traits alter short-term responses such as growth rate or probability of survival is not clear. Here we develop models to examine the nonlethal effects of predators on prey growth. Our analyses illustrate how the nonlethal effects of predators on individual prey growth depend on environmental context; e.g., factors such as focal species density, competitor density, resource dynamics, and the timescale over which the interactions occur. This context dependence arises because of complex interactions of three mechanisms; (1) the direct negative effect of induced reduction in foraging rates, which is opposed by (2) the potential positive effects of reductions in intra- and interspecific competition, and (3) resource responses to reduced foraging. We present new empirical work, and review previous work, on larval-anuran growth that is in general support of model predictions. The framework presented here can serve to facilitate the design and interpretation of experimental results and predict how the nonlethal predator effect on prey growth in natural systems will vary over time and space.

The spread, establishment and impacts of the spiny water flea, Bythotrephes longimanus, in temperate North America: a synopsis of the special issue

More than most sub-disciplines of ecology, the study of biological invasions is characterized by breadth rather than by depth. Studies of expanding ranges of invaders are common, as are post-invasion case studies, but we rarely have a deep understanding of the dynamics and regulators of the processes of invasion and resultant ecological transformations. This is unfortunate because such depth may well be needed to develop targeted, knowledge-based, management plans. In this collection we provide this needed depth of study of the key aspects of the invasion process for the spiny water flea, Bythotrephes longimanus. We do so by presenting the results of the work conducted by researchers in the Canadian Aquatic Invasive Species Network (CAISN), and several of their American and European collaborators over the past half decade. Given its rapid spread in the Great Lakes basin in North America, and the decreases in pelagic biodiversity that have ensued, the last decade has witnessed a surge of research on Bythotrephes. In this collection we learn much about mechanisms and dynamics of its spread, about the key role of humans in that spread, about the importance of Allee effects to establishment and persistence, about choices and parameterization of risk assessment models, about the value of comparing “effects” in native and invaded regions, about complex probable interactions of the invasion with impending changes in the climate, and about the regulators of the invader’s abundance and impacts. There should be much of interest in the collection for aquatic ecologists and invading species biologists alike.