Trait-mediated indirect interactions in size-structured populations: Trait-mediated effects, density dependence, and the dynamic stability of ecological systems 7. Plant effects on herbivore-enemy interactions in natural systems 8. The implications of adaptive prey behavior for ecological communities: Community consequences of phenotypic plasticity of terrestrial plants: Model-based, response surface approaches to quantifying indirect interactions Part II.
Indirect evolutionary interactions in a multi-trophic system The role of trait-mediated indirect interactions for multispecies plant-animal mutualisms Consequences of trait evolution in a multi-species system Part III. Species functional traits, trophic control, and the ecosystem consequences of adaptive foraging in the middle of food chains Effects of herbivores on terrestrial ecosystem processes: Functional and heritable consequences of plant genotype on community composition and ecosystem processes Microbial mutualists and biodiversity in ecosystems Integrating trait-mediated effects and non-trophic interactions in the study of biodiversity and ecosystem functioning Part IV.
Natural enemy functional identity, trait-mediated interactions, and biological control Trait-mediated effects modify patch-size density relationships in insect herbivores and parasitoids Plasticity and trait-mediated indirect interactions among plants Climate change, phenology, and the nature of consumer-resource interactions: His research focus is on population biology of insect herbivores, plant-herbivore interactions, multi-trophic interactions and the linkage from gene to ecosystem.
In particular, he is interested in how trait-mediated indirect effects create ecological communities and biodiversity. He studies the linkage between two important components of natural systems: Holt , University of Florida Robert D. Holt is Arthur R. He is an evolutionary and community ecologist whose contributions are principally theoretical, but always tied to concrete processes in the natural world. Price, Takayuki Ohgushi, Oswald J. Frank van Veen, H. Rudolf, Michael Barfield, Kailen A. Cressler, Toshinori Okuyama, Benjamin M.
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The contribution of trait-mediated indirect effects to the net effects of a predator
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We examined the indirect effects of larval dragonfly predators Anax sp.
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Small bullfrog tadpoles react strongly to presence of Anax by reducing activity levels 19 , whereas the large bullfrog tadpoles are much less vulnerable and react only weakly. We therefore can examine indirect effects of the predator on competitors through vulnerable prey without confounding effects of the predator on the competitors. Further, we used a low density of large bullfrog tadpoles to minimize their effects on resources and therefore permit a clearer differentiation of nonlethal and lethal effects of the predator through small bullfrog tadpoles.
Mesocosms mimicking small pond environments were constructed in cylindrical cattle watering tanks filled with 1, liters of well water and inoculated with phytoplankton, periphyton, and zooplankton from a local pond. Dry oak leaves Quercus sp. We added 15 mg of nitrogen in the form of NH 4 NO 3 , and 2. Three levels of density reduction in small tadpoles were crossed with four levels of induced foraging reduction to effectively create 12 different combinations in the predator—prey effect space.
We isolated prey foraging reduction no density reduction by using different numbers of caged Anax zero, one, two, and four to which the small tadpoles react due to chemical cues that diffuse out of the permeable cages. The 12 different combinations thus spanned a range of hypothetical predator—prey interactions, i. All 13 treatments were randomly distributed in each of four spatial blocks. We then added five large bullfrog tadpoles 1. Nutrients originating from caged Anax do not contribute significantly to the tadpole growth rates and hence do not confound the results presented here S.
We performed behavioral observations of tadpoles on seven occasions; during the afternoon of days 5, 7, 9, 21, and 23, and during the night 1—4 a. We slowly circled each tank and recorded the number of tadpoles above the tank floor i. This was done from four to six times over a 2- or 3-h period and the data for each tank were averaged for each measurement period.
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Bullfrog tadpoles generally react to Anax by spending more time on the tank floor and becoming less active Note, these behavioral responses do not represent a direct assessment of the magnitude of foraging reduction of the tadpoles. This assessment would require a more detailed understanding of how behavioral traits such as percent of time spent active relate to the foragers ability to garner food. Rather, the behavioral observations were made to ensure that the small tadpoles indeed perceived, and responded to, the caged Anax predators, and to gain a qualitative estimate of how different numbers of caged Anax affected the relative tadpole foraging effort.
The presence of Anax had a large negative effect on tadpole traits related to foraging effort, and this effect was a function of the density of caged Anax Fig. Equally strong effects were also observed on days 7, 9, 20, and The small bullfrogs reacted slightly more to the lethal Anax two uncaged Anax than to four caged Anax. In summary, the behavioral patterns of the small tadpoles suggest that lethal and caged Anax had a negative effect on the foraging effort of the small bullfrog tadpoles throughout the experiment, that the effect was stronger with more caged Anax , and that four caged Anax had roughly the same effect as two lethal Anax.
In contrast, the caged Anax had no effect on the position and activity levels of the large bullfrog tadpoles. Behavioral response of small bullfrog tadpoles to caged Anax. The number of tadpoles active swimming or feeding was lower in tanks with caged Anax throughout the experiment data presented here were collected early in the experiment on July 7. Large bullfrog tadpoles gained considerably more mass 2.
This difference is presumably due to the indirect effects of Anax both through changes in density and behavior of small tadpoles. When the nonlethal effect was isolated, increased number of caged Anax from zero to one, two, and four caged Anax had a large, monotonically increasing, effect on large tadpole growth Fig. Growth final minus initial mass of large bullfrog tadpoles with and without two lethal Anax. Additional treatments allowed us to decompose the net indirect effect of the Anax into contributions due to foraging reduction, density reduction, and an interaction between these two effects see text.
Average large bullfrog tadpole growth g, final minus initial mass as a function of small bullfrog tadpole C 1 density reduction using nets and foraging rate reduction using caged Anax. For clarity, error bars are not included. Comparison of large bullfrog tadpole growth in the lethal Anax treatment with the manual removal treatments suggest that the Anax -induced reduction in small tadpole foraging rate contributed substantially to the total indirect effect of Anax on the large tadpoles. The actual effect of lethal Anax on the large bullfrogs 2. Further, the indirect effect of lethal Anax on large bullfrog tadpoles causing a 2.
We suspect two potential causes for this disparity i. First, tadpoles may gain mass at a faster rate as they grow larger. Thus the two mechanisms i. Second, both the removal and trait modification of the small tadpoles represent a decrease in herbivory on the resources. If resources respond nonlinearly to this decrease, then the increase in resources may be greater than the sum of the increases caused by density and foraging reduction of small tadpoles in isolation.
Results of the 12 different hypothetical predator—prey interactions indicated that the nonlethal effect of the predator contributed substantially to the net indirect effect of the predator over a large range of the predator—prey effect space Fig. To relate the hypothetical i. For example, because two free Anax had a slightly larger effect on tadpole behavior than four caged Anax , we can estimate that the effect of one, two, and four caged Anax is approximately that of one-half, one, and two lethal uncaged Anax.
Clearly this procedure provides rough estimates; however, we use this exercise only to provide a qualitative understanding of the relative contribution of the nonlethal effect of predators. Representation in predator—prey effect space of the contribution of foraging reduction and density reduction to the total indirect effect of the predator on large bullfrog tadpoles. Units for both density and foraging reduction represent one lethal Anax in the experimental tank environment and were calibrated by extrapolating from the effect of Anax in the lethal Anax treatment on density and behavior of the small tadpoles.
We derived these regions by examining the impact of foraging reduction and density reduction in the factorial design treatments Fig. In fact, when the nonlethal effect was relatively low equivalent to approximately one-half lethal Anax , it contributed substantially to the total indirect effect of the predator even at high density-reduction rates equivalent to approximately three to four lethal Anax.
This experiment demonstrated that the nonlethal effect of a predator can contribute substantially to its net indirect effect over a large range of predator—prey effect space Figs. Our data suggest that the lethal effect i. This was the case even at high predation removal rates. Our results make clear that phenotypic responses of prey likely play a large role in determining the consequences of species interactions. Other investigations have suggested that TMIIs are likely important in diverse systems refs. These studies have primarily examined the nonlethal effect of a predator by either examining the nonlethal effect isolated from the density effect or by investigating predator—prey interactions in size ranges where predation is negligible e.
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Here we show that the nonlethal effect can be influential not only when density effects are low, but over a large range of induced foraging rate reduction—predation rate combinations, including those where predation rates are high. Although perhaps counterintuitive, there are two straightforward reasons behind these results. First, the nonlethal effects occur independent of lethal effects; i. Second, nonlethal effects occur over the duration of each prey's lifetime.
Thus the nonlethal effects are transmitted from the predator to the resources and therefore competitors even through prey that are ultimately killed. For example, if prey at age X are killed by a predator, the indirect effects of the predator through induced trait changes in the prey to time X still have affected the system. These two reasons suggest that TMIIs can be important at high, as well as low, predation rates. Our results have far-reaching implications to the study of ecological communities.
Indirect interactions that arise from predator-induced trait changes phenotypic plasticity differ from those that arise from density changes in fundamental ways. First, it is likely that indirect interactions resulting from a predator's effect on density and traits of prey will exhibit markedly different density dependencies.
For example, a few predators may have a strong effect on prey traits and hence a large effect on the net foraging impact of the prey but little effect on prey density, whereas many predators will have a proportionately stronger effect on prey densities. Second, indirect interactions arising from changes in traits of a species imply that the interaction magnitudes between two species are dependent on the background species assemblage.
Thus we cannot predict the dynamics of complex assemblages on the basis of interactions of small subsets of species in isolation 13 — Rather, models must recognize that interaction strengths between any two species change dynamically with the density of other species in the system. Recent theoretical work shows that inclusion of higher-order terms that would be required to describe our short-term results can have a profound influence on predictions of models describing long-term population dynamics 13 , 25 — In conclusion, experimentally isolating the separate components of the indirect effects of a predator and examining the predator—prey phase effect of predator—prey interactions demonstrated that a predator-induced modification in prey traits can contribute substantially to the net indirect effect of a predator even when there are large density effects.
The typical representation of ecological communities, in which trait modification is tacitly assumed to be inconsequential, is thus inadequate to describe the dynamics of the community examined here. An abundance of recent empirical evidence demonstrates that the reaction of the anuran larvae to their predator that underlies our results is exhibited in many species from diverse taxa. This demonstration suggests that our results likely apply to a broad range of ecological communities, and that many effects traditionally attributed to predators eating prey may actually be due to predators inducing changes in the traits of their prey.
We thank Robert Rommel and Chad Walasek for assistance in conducting the experiment. Vandermeer for helpful comments on the manuscript. We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.
Skip to main content. The contribution of trait-mediated indirect effects to the net effects of a predator Scott D. Peacor and Earl E. PNAS March 27, 98 7 ; https: Abstract Many prey modify traits in response to predation risk and this modification of traits can influence the prey's resource acquisition rate. Figure 1 The model food web. Methods We used a simple community in aquatic mesocosms to test whether the nonlethal predator effect can be influential over a wide range of predator—prey effect space.
Results The presence of Anax had a large negative effect on tadpole traits related to foraging effort, and this effect was a function of the density of caged Anax Fig. Figure 2 Behavioral response of small bullfrog tadpoles to caged Anax.