Deborah L. Finke

Predator diversity dampens trophic cascades

Food web complexity is thought to weaken the strength of terrestrial trophic cascades in which strong impacts of natural enemies on herbivores cascade to influence primary production indirectly. Predator diversity can enhance food web complexity because predators may feed on each other and on shared prey. In such cases, theory suggests that the impact of predation on herbivores relaxes and cascading effects on basal resources are dampened. Despite this view, no empirical studies have explicitly investigated the role of predator diversity in mediating primary productivity in a natural terrestrial system. Here we compare, in a coastal marsh community, impacts of arthropod predators on herbivores and plant productivity between a simple food web with a single predator species and a complex food web with a diverse predator assemblage. We show that enhancing predator diversity dampens enemy effects on herbivores and weakens trophic cascades. Consequently, changes in diversity at higher trophic levels can significantly alter ecosystem function in natural systems.

Intraguild predation diminished in complex-structured vegetation: Implications for prey suppression

Multiple-predator limitation of prey populations may be mediated by both predator–predator interactions and vegetation structure. Antagonistic interactions among predators, such as intraguild predation, can diminish the collective impact of natural enemies on prey population size. However, structurally complex vegetation may moderate such interactions by providing a refuge for predators, thereby enhancing prey suppression. Specifically, we examined the combined impact of two salt-marsh-inhabiting invertebrate predators, the mirid Tytthus vagus and the wolf spider Pardosa littoralis, on suppression of their shared prey, the planthopper Prokelisia dolus, in simple (thatch-free) and complex (thatch-rich) vegetation. In structurally simple habitats in the laboratory, the predators interacted antagonistically, due to the intraguild predation of mirids by spiders, and predation pressure on the planthopper population was relaxed. However, structurally complex habitats dampened this antagonistic interaction by providing a refuge for mirids from spider predation, thereby increasing the combined effectiveness of these predators in suppressing planthopper populations. Consistent with our laboratory results, we found enhanced co-occurrence of these predators in complex habitats in the field, where mirids are apparently at lower risk from spider predation and outbreaks of planthoppers are less likely. In contrast, in simple habitats, mirids were relatively less abundant, a finding consistent with the expectation of increased intraguild predation from spiders. Therefore, in this salt marsh system, complex vegetation diminished the occurrence of intraguild predation between mirids and spiders and increased overall enemy impact on their shared herbivore prey, demonstrating for the first time that plants can mediate enemy effects on insect herbivores by influencing predator–predator interactions.

BOTTOM-UP FORCES MEDIATE NATURAL-ENEMY IMPACT IN A PHYTOPHAGOUS INSECT COMMUNITY

We employed a combination of factorial experiments in the field and labo- ratory to investigate the relative magnitude and degree of interaction of bottom-up factors (two levels each of host-plant nutrition and vegetation complexity) and top-down forces (two levels of wolf-spider predation) on the population growth of Prokelisia planthoppers (P. dolus and P. marginata), the dominant insect herbivores on Spartina cordgrass through- out the intertidal marshes of North America. Treatments were designed to mimic combi- nations of plant characteristics and predator densities that occur naturally across habitats in the field. There were complex interactive effects between plant resources and spider predation on the population growth of planthoppers. The degree that spiders suppressed planthoppers depended on both plant nutrition and vegetation complexity, an interaction that was dem- onstrated both in the field and laboratory. Laboratory results showed that spiders checked planthopper populations most effectively on poor-quality Spartina with an associated matrix of thatch, all characteristics of high-marsh meadow habitats. It was also this combination of plant resources in concert with spiders that promoted the smallest populations of planthop- pers in our field experiment. Planthopper populations were most likely to escape the sup- pressing effects of predation on nutritious plants without thatch, a combination of factors associated with observed planthopper outbreaks in low-marsh habitats in the field. Thus, there is important spatial variation in the relative strength of forces with bottom-up factors dominating under low-marsh conditions and top-down forces increasing in strength at higher elevations on the marsh. Enhancing host-plant biomass and nutrition did not strengthen top-down effects on planthoppers, even though nitrogen-rich plants supported higher densities of wolf spiders and other invertebrate predators in the field. Rather, planthopper populations, particularly those of Prokelisia marginata, escaped predator restraint on high-quality plants, a result we attribute to its mobile life history, enhanced colonizing ability, and rapid growth rate. Thus, our results for Prokelisia planthoppers suggest that the life history strategy of a species is an important mediator of top-down and bottom-up impacts. In laboratory mesocosms, enhancing plant biomass and nutrition resulted in increased spider reproduction, a cascading effect associated with planthopper increases on high- quality plants. Although the adverse effects of spider predation on planthoppers cascaded down and fostered increased plant biomass in laboratory mesocosms, this result did not occur in the field where top-down effects attenuated. We attributed this outcome in part to the intraguild predation of other planthopper predators by wolf spiders. Overall, the general paradigm in this system is for bottom-up forces to dominate, and when predators do exert a significant suppressing effect on planthoppers, their impact is generally legislated by vegetation characteristics.

Niche Partitioning Increases Resource Exploitation by Diverse Communities

Classical ecological theory suggests that the coexistence of consumer species is fostered by resource-use differences, leading to greater resource use in communities with more species. However, explicit empirical support for this idea is lacking, because resource use by species is generally confounded with other species-specific attributes. We overcame this obstacle by co-opting behavioral plasticity in food choice among a group of animal consumers, allowing us to manipulate patterns of resource use while controlling for the effects of species identity and diversity. Within an aphid-parasitoid-radish community, we created a fully factorial manipulation of consumer resource-use breadth (specialist versus generalist) and species diversity (one versus three species) and found that resource exploitation improved with greater specialist, but not generalist, diversity. Therefore, resource partitioning, and not diversity per se, fostered greater overall resource consumption in our multispecies consumer communities.

Feeding-induced changes in plant quality mediate interspecific competition between sap-feeding herbivores.

Feeding-induced plant resistance is a well-documented phenomenon for leaf- chewing insects. Furthermore, feeding-induced resistance provides the mechanistic basis for many cases of delayed interspecific competition, whereby previous feeding by one species diminishes the performance of other herbivores which attack the same plant later in the season. This phenomenon, however, has been very poorly investigated for sap-feeding insects. The results we present here for salt marsh-inhabiting planthoppers ( Prokelisia dolus and P. marginata) provide one of the few known examples of delayed, plant-mediated interspecific competition between two sap-feeding insects. Three lines of experimental evidence from the laboratory, field cages, and open field plots provide support for the detrimental effects of previous feeding by one planthopper species on the subsequent survival and performance of the other. Laboratory experiments showed that prior feeding on cordgrass by one congener resulted in reduced performance of the other in the following generation. However, the effect was asymmetric. Prior feeding by P. dolus resulted in prolonged development and reduced body size (a correlate of fecundity) in P. marginata, whereas only development was protracted in P. dolus when plants were previously exposed to P. marginata. Consequently, P. dolus appears to be the superior competitor in the context of delayed, plant-mediated interactions. The negative effects of previous feeding by P. dolus on the development time, body size, and survival of P. marginata obtained in the laboratory were confirmed both in cages and on cage-free islets of cordgrass in the field. Feeding-induced reductions in host-plant quality by P. dolus may provide additional impetus for P. marginata to migrate from shared habitats on the high marsh to nutritionally superior plants in the low marsh rarely occupied by P. dolus. The mechanism underlying the delayed competitive effects between Prokelisia plan- thoppers is most likely diminished plant nutrition, because feeding by P. dolus significantly reduces the concentration of essential amino acids in cordgrass. The asymmetry of plant- mediated competition between the Prokelisia species may be due to the ability of P. dolus to better tolerate feeding-depleted levels of plant nitrogen via compensatory feeding. Even though these two planthoppers do not suffer significant fitness reductions during contemporaneous interactions, they compete severely in the context of feeding-induced plant resistance which is expressed later in the season. This result, coupled with the fact that most studies of interspecific interaction between herbivorous insects are contempo- raneous, indicates that interspecific competition may be profoundly underestimated as a structuring force in phytophagous insect communities.

Spatial refuge from intraguild predation: implications for prey suppression and trophic cascades.

The ability of predators to elicit a trophic cascade with positive impacts on primary productivity may depend on the complexity of the habitat where the players interact. In structurally-simple habitats, trophic interactions among predators, such as intraguild predation, can diminish the cascading effects of a predator community on herbivore suppression and plant biomass. However, complex habitats may provide a spatial refuge for predators from intraguild predation, enhance the collective ability of multiple predator species to limit herbivore populations, and thus increase the overall strength of a trophic cascade on plant productivity. Using the community of terrestrial arthropods inhabiting Atlantic coastal salt marshes, this study examined the impact of predation by an assemblage of predators containing Pardosa wolf spiders, Grammonota web-building spiders, and Tytthus mirid bugs on herbivore populations (Prokelisia planthoppers) and on the biomass of Spartina cordgrass in simple (thatch-free) and complex (thatch-rich) vegetation. We found that complex-structured habitats enhanced planthopper suppression by the predator assemblage because habitats with thatch provided a refuge for predators from intraguild predation including cannibalism. The ultimate result of reduced antagonistic interactions among predator species and increased prey suppression was enhanced conductance of predator effects through the food web to positively impact primary producers. Behavioral observations in the laboratory confirmed that intraguild predation occurred in the simple, thatch-free habitat, and that the encounter and capture rates of intraguild prey by intraguild predators was diminished in the presence of thatch. On the other hand, there was no effect of thatch on the encounter and capture rates of herbivores by predators. The differential impact of thatch on the susceptibility of intraguild and herbivorous prey resulted in enhanced top-down effects in the thatch-rich habitat. Therefore, changes in habitat complexity can enhance trophic cascades by predator communities and positively impact productivity by moderating negative interactions among predators.

Interactions between a hunting spider and a web‐builder: consequences of intraguild predation and cannibalism for prey suppression

Abstract.  1. Antagonistic interactions among invertebrate predators such as intraguild predation and cannibalism have the potential to dampen top‐down impacts on shared prey at lower trophic levels. Two abundant spider predators, the large wolf spider Pardosa littoralis and the small sheet‐web builder Grammonota trivitatta co‐occur on the salt marshes of eastern North America where they both attack planthoppers (Prokelisia spp.), the dominant herbivores on the marsh. Experiments both in the laboratory and field were used to assess the incidence of intraguild predation and cannibalism in these spiders and elucidate how such antagonistic interactions influence planthopper suppression.

Intra-guild predation relaxes natural enemy impacts on herbivore populations

Abstract. 1. To investigate the role of intra‐guild predation in mediating the impact of the natural enemy complex on herbivore populations, a manipulative field experiment was conducted using uncaged plots (islets of Spartina cordgrass) on a North American salt marsh. The densities (moderate or low) of two invertebrate predators, the generalist wolf spider Pardosa littoralis and the specialist mirid bug Tytthus vagus, were manipulated in a 2 × 2 factorial design, and the resulting treatment effects on the population growth of their herbivorous prey, Prokelisia planthoppers, were assessed.

Does intraguild predation enhance predator performance? A stoichiometric perspective

Ecological stoichiometry provides a novel context for elucidating the occurrence of intraguild predation. Recent data show that predators on average have a higher nitrogen content and lower C:N ratio than potential herbivorous prey. Thus, many predators may be nitrogen limited, and intraguild predation may allow them to increase their nitrogen intake and growth by supplementing a diet of herbivores with more nitrogen-rich intraguild prey. We tested this hypothesis using an assemblage of salt-marsh-inhabiting arthropods. First, we determined the nitrogen content and C:N ratio of taxa in four trophic groups (plants, herbivores, omnivores, and predators). Second, we fed an intraguild predator, the wolf spider Pardosa, one of three diets (herbivores, intraguild prey, or an alternating mix of the two) and measured spider survival, growth, capture rate, and biomass and nitrogen intake. In general, body nitrogen content increased and C:N ratio decreased from lower to higher trophic levels for marsh-inhabiting sp...

Increased primary production shifts the structure and composition of a terrestrial arthropod community

Numerous studies have examined relationships between primary production and biodiversity at higher trophic levels. However, altered production in plant communities is often tightly linked with concomitant shifts in diversity and composition, and most studies have not disentangled the direct effects of production on consumers. Furthermore, when studies do examine the effects of plant production on animals in terrestrial systems, they are primarily confined to a subset of taxonomic or functional groups instead of investigating the responses of the entire community. Using natural monocultures of the salt marsh cordgrass Spartina alterniflora, we were able to examine the impacts of increased plant production, independent of changes in plant composition and/or diversity, on the trophic structure, composition, and diversity of the entire arthropod community. If arthropod species richness increased with greater plant production, we predicted that it would be driven by: (1) an increase in the number of rare species, and/or (2) an increase in arthropod abundance. Our results largely supported our predictions: species richness of herbivores, detritivores, predators, and parasitoids increased monotonically with increasing levels of plant production, and the diversity of rare species also increased with plant production. However, rare species that accounted for this difference were predators, parasitoids, and detritivores, not herbivores. Herbivore species richness could be simply explained by the relationship between abundance and diversity. Using nonmetric multidimensional scaling (NMDS) and analysis of similarity (ANOSIM), we also found significant changes in arthropod species composition with increasing levels of production. Our findings have important implications in the intertidal salt marsh, where human activities have increased nitrogen runoff into the marsh, and demonstrate that such nitrogen inputs cascade to affect community structure, diversity, and abundance in higher trophic levels.