Evan L. Preisser

SCARED TO DEATH? THE EFFECTS OF INTIMIDATION AND CONSUMPTION IN PREDATOR–PREY INTERACTIONS

Predation is a central feature of ecological communities. Most theoretical and empirical studies of predation focus on the consequences of predators consuming their prey. Predators reduce prey population densities through direct consumption (a density- mediated interaction, DMI), a process that may indirectly affect the preys resources, com- petitors, and other predators. However, predators can also affect prey population density by stimulating costly defensive strategies. The costs of these defensive strategies can include reduced energy income, energetic investment in defensive structures, lower mating success, increased vulnerability to other predators, or emigration. Theoretical and empirical studies confirm the existence of these induced costs (trait-mediated interactions, TMIs); however, the relative importance of intimidation (TMI) and consumption (DMI) effects remains an open question. We conducted a meta-analysis assessing the magnitude of both TMIs and DMIs in predator-prey interactions. On average, the impact of intimidation on prey de- mographics was at least as strong as direct consumption (63% and 51% the size of the total predator effect, respectively). This contrast is even more pronounced when we consider the cascading effects of predators on their preys resources: density effects attenuated through food chains, while TMIs remained strong, rising to 85% of the total predator effect. Predators can thus strongly influence resource density even if they consume few prey items. Finally, intimidation was more important in aquatic than terrestrial ecosystems. Our results suggest that the costs of intimidation, traditionally ignored in predator-prey ecology, may actually be the dominant facet of trophic interactions.

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.

PREDATOR HUNTING MODE AND HABITAT DOMAIN ALTER NONCONSUMPTIVE EFFECTS IN PREDATOR–PREY INTERACTIONS

Predators can affect prey populations through changes in traits that reduce predation risk. These trait changes (nonconsumptive effects, NCEs) can be energetically costly and cause reduced prey activity, growth, fecundity, and survival. The strength of nonconsumptive effects may vary with two functional characteristics of predators: hunting mode (actively hunting, sit-and-pursue, sit-and-wait) and habitat domain (the ability to pursue prey via relocation in space; can be narrow or broad). Specifically, cues from fairly stationary sit-and-wait and sit-and-pursue predators should be more indicative of imminent predation risk, and thereby evoke stronger NCEs, compared to cues from widely ranging actively hunting predators. Using a meta-analysis of 193 published papers, we found that cues from sit-and-pursue predators evoked stronger NCEs than cues from actively hunting predators. Predator habitat domain was less indicative of NCE strength, perhaps because habitat domain provides less reliable information regarding imminent risk to prey than does predator hunting mode. Given the importance of NCEs in determining the dynamics of prey communities, our findings suggest that predator characteristics may be used to predict how changing predator communities translate into changes in prey. Such knowledge may prove particularly useful given rates of local predator change due to habitat fragmentation and the introduction of novel predators.

FROM INDIVIDUALS TO ECOSYSTEM FUNCTION: TOWARD AN INTEGRATION OF EVOLUTIONARY AND ECOSYSTEM ECOLOGY

An important goal in ecology is developing general theory on how the species composition of ecosystems is related to ecosystem properties and functions. Progress on this front is limited partly because of the need to identify mechanisms controlling functions that are common to a wide range of ecosystem types. We propose that one general mechanism, rooted in the evolutionary ecology of all species, is adaptive foraging behavior in response to predation risk. To support our claim, we present two kinds of empirical evidence from plant-based and detritus-based food chains of terrestrial and aquatic ecosystems. The first kind comes from experiments that explicitly trace how adaptive foraging influences ecosystem properties and functions. The second kind comes from a synthesis of studies that individually examine complementary components of particular ecosystems that together provide an integrated perspective on the link between adaptive foraging and ecosystem function. We show that the indirect effects of predators on plant diversity, plant productivity, nutrient cycling, trophic transfer efficiencies, and energy flux caused by consumer foraging shifts in response to risk are qualitatively different from effects caused by reductions in prey density due to direct predation. We argue that a perspective of ecosystem function that considers effects of consumer behavior in response to predation risk will broaden our capacity to explain the range of outcomes and contingencies in trophic control of ecosystems. This perspective also provides an operational way to integrate evolutionary and ecosystem ecology, which is an important challenge in ecology.

Observer bias and the detection of low-density populations

Monitoring programs increasingly are used to document the spread of invasive species in the hope of detecting and eradicating low-density infestations before they become established. However, interobserver variation in the detection and correct identification of low-density populations of invasive species remains largely unexplored. In this study, we compare the abilities of volunteer and experienced individuals to detect low-density populations of an actively spreading invasive species, and we explore how interobserver variation can bias estimates of the proportion of sites infested derived from occupancy models that allow for both false negative and false positive (misclassification) errors. We found that experienced individuals detected small infestations at sites where volunteers failed to find infestations. However, occupancy models erroneously suggested that experienced observers had a higher probability of falsely detecting the species as present than did volunteers. This unexpected finding is an artifact of the modeling framework and results from a failure of volunteers to detect low-density infestations rather than from false positive errors by experienced observers. Our findings reveal a potential issue with site occupancy models that can arise when volunteer and experienced observers are used together in surveys.

The Many Faces of Fear: Comparing the Pathways and Impacts of Nonconsumptive Predator Effects on Prey Populations

Background Most ecological models assume that predator and prey populations interact solely through consumption: predators reduce prey densities by killing and consuming individual prey. However, predators can also reduce prey densities by forcing prey to adopt costly defensive strategies. Methodology/Principal Findings We build on a simple Lotka-Volterra predator-prey model to provide a heuristic tool for distinguishing between the demographic effects of consumption (consumptive effects) and of anti-predator defenses (nonconsumptive effects), and for distinguishing among the multiple mechanisms by which anti-predator defenses might reduce prey population growth rates. We illustrate these alternative pathways for nonconsumptive effects with selected empirical examples, and use a meta-analysis of published literature to estimate the mean effect size of each pathway. Overall, predation risk tends to have a much larger impact on prey foraging behavior than measures of growth, survivorship, or fecundity. Conclusions/Significance While our model provides a concise framework for understanding the many potential NCE pathways and their relationships to each other, our results confirm empirical research showing that prey are able to partially compensate for changes in energy income, mitigating the fitness effects of defensive changes in time budgets. Distinguishing the many facets of nonconsumptive effects raises some novel questions, and will help guide both empirical and theoretical studies of how predation risk affects prey dynamics.

Selection of Reference Genes for RT-qPCR Analysis in Coccinella septempunctata to Assess Un-intended Effects of RNAi Transgenic Plants.

The development of genetically engineered plants that employ RNA interference (RNAi) to suppress invertebrate pests opens up new avenues for insect control. While this biotechnology shows tremendous promise, the potential for both non-target and off-target impacts, which likely manifest via altered mRNA expression in the exposed organisms, remains a major concern. One powerful tool for the analysis of these un-intended effects is reverse transcriptase-quantitative polymerase chain reaction, a technique for quantifying gene expression using a suite of reference genes for normalization. The seven-spotted ladybeetle Coccinella septempunctata, a commonly used predator in both classical and augmentative biological controls, is a model surrogate species used in the environmental risk assessment (ERA) of plant incorporated protectants (PIPs). Here, we assessed the suitability of eight reference gene candidates for the normalization and analysis of C. septempunctata v-ATPase A gene expression under both biotic and abiotic conditions. Five computational tools with distinct algorisms, geNorm, Normfinder, BestKeeper, the ΔCt method, and RefFinder, were used to evaluate the stability of these candidates. As a result, unique sets of reference genes were recommended, respectively, for experiments involving different developmental stages, tissues, and ingested dsRNAs. By providing a foundation for standardized RT-qPCR analysis in C. septempunctata, our work improves the accuracy and replicability of the ERA of PIPs involving RNAi transgenic plants.

Multiple Forms of Vector Manipulation by a Plant-Infecting Virus: Bemisia tabaci and Tomato Yellow Leaf Curl Virus

ABSTRACT For many insect-vectored plant viruses, the relationship between feeding behavior and vector competence may prove integral to an understanding of the epidemiology of the resulting plant disease. While plant-infecting viruses are well known to change host plant physiology in a way that makes them more attractive to vectors, viral manipulation of the vectors themselves has only recently been reported. Previous research suggested that the rapid spread of Tomato yellow leaf curl virus (TYLCV) throughout China has been facilitated by its primary vector, the whitefly Bemisia tabaci. We conducted two experiments testing the impact of TYLCV infection of the host plant (tomato) and vector (B. tabaci biotypes B and Q) on whitefly feeding behavior. Whiteflies of biotypes B and Q both appeared to find TYLCV-infected plants more attractive, probing them more quickly and having a greater number of feeding bouts; this did not, however, alter the total time spent feeding. Viruliferous whiteflies fed more readily than uninfected whiteflies and spent more time salivating into sieve tube elements. Because vector salivation is essential for viral transmission, this virally mediated alteration of behavior should provide TYLCV a direct fitness benefit. This is the first report of such manipulation by a nonpropagative virus that belongs to an exclusively plant-infecting family of viruses (Geminiviridae). In the context of previous research showing that feeding on TYLCV-infected plants harms biotype B but helps biotype Q, the fact that both biotypes were equally affected by TYLCV also suggests that the virus may alter the biotype B-biotype Q competitive interaction in favor of biotype Q.

Climate Affects Predator Control of an Herbivore Outbreak

Herbivore outbreaks and the accompanying devastation of plant biomass can have enormous ecological effects. Climate directly affects such outbreaks through plant stress or alterations in herbivore life‐history traits. Large‐scale variation in climate can indirectly affect outbreaks through trophic interactions, but the magnitude of such effects is unknown. On the California coast, rainfall in years during and immediately previous to mass lupine mortality was two‐thirds that of years without such mortality. However, neither mature lupines nor their root‐feeding herbivores are directly affected by annual variation in rainfall. By increasing soil moisture to levels characteristic of summers following El Niño/Southern Oscillation (ENSO) events, we increased persistence of a predator (the entomopathogenic nematode Heterorhabditis marelatus). This led to suppression of an outbreak of the herbivorous moth Hepialus californicus, indirectly protecting bush lupine (Lupinus arboreus). Our results are consistent with the marine‐oriented Menge‐Sutherland hypothesis (Menge and Sutherland 1987) that abiotic stress has greater effects on higher than on lower trophic levels. The mechanisms producing these results differ from those proposed by Menge‐Sutherland, however, highlighting differences between trophic processes in underground and terrestrial/marine food webs. Our evidence suggests that herbivore outbreaks and mass lupine mortality are indirectly affected by ENSO’s facilitation of top‐down control in this food web.

Variation in Plant Defense against Invasive Herbivores: Evidence for a Hypersensitive Response in Eastern Hemlocks (Tsuga canadensis)

Herbivores can trigger a wide array of morphological and chemical changes in their host plants. Feeding by some insects induces a defensive hypersensitive response, a defense mechanism consisting of elevated H2O2 levels and tissue death at the site of herbivore feeding. The invasive hemlock woolly adelgid Adelges tsugae (‘HWA’) and elongate hemlock scale Fiorinia externa (‘EHS’) feed on eastern hemlocks; although both are sessile sap feeders, HWA causes more damage than EHS. The rapid rate of tree death following HWA infestation has led to the suggestion that feeding induces a hypersensitive response in hemlock trees. We assessed the potential for an herbivore-induced hypersensitive response in eastern hemlocks by measuring H2O2 levels in foliage from HWA-infested, EHS-infested, and uninfested trees. Needles with settled HWA or EHS had higher H2O2 levels than control needles, suggesting a localized hypersensitive plant response. Needles with no direct contact to settled HWA also had high H2O2 levels, suggesting that HWA infestation may induce a systemic defense response in eastern hemlocks. There was no similar systemic defensive response in the EHS treatment. Our results showed that two herbivores in the same feeding guild had dramatically different outcomes on the health of their shared host.