Susceptibility to predation affects trait-mediated indirect interactions by reversing interspecific competition

Numerous studies indicate that the behavioral responses of prey to the presence of predators can have an important role in structuring assemblages through trait-mediated indirect interactions. Few studies, however, have addressed how relative susceptibility to predation influences such interactions. Here we examine the effect of chemical cues from the common shore crab Carcinus maenas on the foraging behavior of two common intertidal gastropod molluscs. Of the two model consumers studied, Littorina littorea is morphologically more vulnerable to crab predation than Gibbula umbilicalis, and it exhibited greater competitive ability in the absence of predation threat. However, Littorina demonstrated a greater anti-predator response when experimentally exposed to predation cues, resulting in a lower level of foraging. This reversed the competitive interaction, allowing Gibbula substantially increased access to shared resources. Our results demonstrate that the susceptibility of consumers to predation can influence species interactions, and suggest that inter-specific differences in trait-mediated indirect interactions are another mechanism through which non-consumptive predator effects may influence trophic interactions.     

Predator biomass determines the magnitude of non-consumptive effects (NCEs) in both laboratory and field environments

Predator body size often indicates predation risk, but its significance in non-consumptive effects (NCEs) and predator risk assessment has been largely understudied. Although studies often recognize that predator body size can cause differing cascading effects, few directly examine prey foraging behavior in response to individual predator sizes or investigate how predator size is discerned. These mechanisms are important since perception of the risk imposed by predators dictates behavioral responses to predators and subsequent NCEs. Here, we evaluate the role of predator body size and biomass on risk assessment and the magnitude of NCEs by investigating mud crab foraging behavior and oyster survival in response to differing biomasses of blue crab predators using both laboratory and field methods. Cues from high predator biomass treatments including large blue crab predators and multiple small blue crab predators decreased mud crab foraging and increased oyster survival, whereas mud crab foraging in response to a single small blue crab did not differ from controls. Mud crabs also increased refuge use in the presence of large and multiple small, but not single small, blue crab predators. Thus, both predator biomass and aggregation patterns may affect the expression of NCEs. Understanding the impact of predator biomass may therefore be necessary to successfully predict the role of NCEs in shaping community dynamics. Further, the results of our laboratory experiments were consistent with observed NCEs in the field, suggesting that data from mesocosm environments can provide insight into field situations where flow and turbulence levels are moderate.     

Trophic cascades in rocky shore tide pools: distinguishing lethal and nonlethal effects

The effects of predators on the density of their prey can have positive indirect effects on the abundance of the preys resource via a trophic cascade. This concept has strongly influenced contemporary views of how communities are structured. However, predators also can transmit indirect effects by inducing changes in prey traits. We show that the mere presence of predator risk cues can initiate a trophic cascade in rocky shore tide pools. In large (mean surface area =9 m²), natural tide pools, we manipulated crab density and their foraging ability to examine the relative importance of lethal (density-mediated) and non-lethal (trait-mediated) predator effects to algal community development. We found that perceived predation risk reduced snail density as much as the direct predation treatment, showing that green crab predation was not an important factor regulating local snail density. Instead, snail emigration away from resident crabs appears to be the most important factor regulating local snail density. As a result, the abundance of ephemeral green algae was similar in the predation risk and direct predation treatments, suggesting that the consumption of snails by crabs plays a minimal role in mediating the trophic cascade. Increased attention to trait-mediated effects that are transmitted by predator-induced changes in prey behavior may change our view of how predators exert their strong influence on community structure.     

Habitat effects on the relative importance of trait- and density-mediated indirect interactions

Classical views of trophic cascades emphasize the primacy of consumptive predator effects on prey populations to the transmission of indirect effects [density-mediated indirect interactions (DMIIs)]. However, trophic cascades can also emerge without changes in the density of interacting species because of non-consumptive predator effects on prey traits such as foraging behaviour [trait-mediated indirect interactions (TMIIs)]. Although ecologists appreciate this point, measurements of the relative importance of each indirect predator effect are rare. Experiments with a three-level, rocky shore food chain containing an invasive predatory crab ( Carcinus maenas ), an intermediate consumer (the snail, Nucella lapillus ) and a basal resource (the barnacle, Semibalanus balanoides ) revealed that the strength of TMIIs is comparable with, or exceeds, that of DMIIs. Moreover, the sign and strength of each indirect predator effect depends on whether it is measured in risky or refuge habitats. Because habitat shifts are often responsible for the emergence of TMIIs, attention to the sign and strength of these interactions in both habitats will improve our understanding of the link between individual behaviour and community dynamics.     

Application of predator-associated cues to control small brown planthoppers: non-consumptive effects of predators suppress the pest population

Predator non-consumptive effects (NCEs) have been well studied in many ecosystems and NCEs can alter the behavior, morphology and life history of prey, producing strong trait-mediated indirect effects (TMIEs) on host plants. However, studies involving the application of NCEs to control pests in the field, and instances of combined laboratory bioassay and field practice are rare. Here, we examine the development, reproduction and behavior of small brown planthoppers, Laodelphax striatellus (Fallén), when exposed to predator cues from caged predators (Paederus fuscipes Curtis), or predator body extracts (in solvents with different polarities) in the laboratory. Field foliage sprays of these extracts were also used to test their effects on the L. striatellus population and rice plant biomass. Nymph development and egg hatch rate in L. striatellus were not influenced, but adult longevity was shorter, and fecundity and weight gain were lower, when nymphs were exposed to the predator cues. Adults exposed to predator cues also gained less weight and laid fewer eggs. The poorer developmental and reproductive performances might result from lower activity levels observed in threatened L. striatellus. The field foliage sprays of predator cues decreased L. striatellus abundance and increased rice plant biomass, suggesting their possible application for pest control. Predator cues extracted using chloroform increased stronger NCEs and TMIEs, indicating their non-polar characteristics. Our studies advance the understanding of how NCEs shape the life history and behavior of L. striatellus and improve rice growth, laying new foundations for future research on novel pest control materials and methods.

     

Predator (<Emphasis Type="Italic">Carcinus maenas</Emphasis>) nonconsumptive limitation of prey (<Emphasis Type="Italic">Nucella lapillus</Emphasis>) feeding depends on prey density and predator cue type

Predators often have nonconsumptive effects (NCEs) on prey. For example, upon detection of predator cues, prey can reduce feeding activities to hamper being detected by predators. Previous research showed that waterborne chemical cues from green crabs (Carcinus maenas, predator) limit the dogwhelk (Nucella lapillus, prey) consumption of barnacles regardless of dogwhelk density, even though individual predation risk for dogwhelks decreases with conspecific density. Such NCEs might disappear with dogwhelk density if dogwhelks feed on mussels, as mussel stands constitute better antipredator refuges than barnacle stands. Through a laboratory experiment, we effectively found that crab chemical cues limit the per-capita consumption of mussels by dogwhelks at low dogwhelk density but not at high density. The combination of tactile and chemical cues from crabs, however, limited the dogwhelk consumption of mussels at both dogwhelk densities. The occurrence of such NCEs at both dogwhelk densities could have resulted from tactile cues indicating a stronger predation risk than chemical cues alone. Overall, the present study reinforces the notions that prey evaluate conspecific density when assessing predation risk and that predator cue type affects their perception of risk.     

Non-consumptive effects of predatory mites on thrips and its host plant

Recent reviews on trait-mediated interactions in food webs suggest that trait-mediated effects are as important in triggering top–down trophic cascades as are density-mediated effects. Trait-mediated interactions between predator and prey result from non-consumptive predator effects changing behavioural and/or life history traits of prey. However, in biological control the occurrence of trait-mediated interactions between predators, prey and plants has been largely ignored. Here, we show that non-consumptive predator effects on prey cascade down to the plant in an agro-ecological food chain. The study system consisted of the predatory mites P. persimilis and N. californicus , the herbivorous non-target prey western flower thrips F. occidentalis and the host plant bean. Irrespective of predator species and risk posed to prey, the presence of predator eggs led to increased ambulation, increased mortality and decreased oviposition of thrips. Furthermore, the presence of predator eggs reduced leaf damage caused by thrips. To our knowledge this is the first experimental evidence suggesting a positive trophic cascade triggered by non-consumptive predator effects on non-target prey in an augmentative biological control system.     

Field evidence of trait-mediated indirect interactions in a rocky intertidal food web

Studies on the implications of food web interactions to community structure have often focused on density-mediated interactions between predators and their prey. This approach emphasizes the importance of predator regulation of prey density via consumption (i.e. lethal effects), which, in turn, leads to cascading effects on the prey's resources. A more recent and contrasting view emphasizes the importance of non-lethal predator effects on prey traits (e.g. behaviour, morphology), or trait-mediated interactions. On rocky intertidal shores in New England, green crab ( Carcinus maenas ) predation is thought to be important to patterns of algal abundance and diversity by regulating the density of herbivorous snails ( Littorina littorea ). We found, however, that risk cues from green crabs can dramatically suppress snail grazing, with large effects on fucoid algal communities. Our results suggest that predator-induced changes in prey behaviour may be an important and under-appreciated component of food web interactions and community dynamics on rocky intertidal shores.     

Predatory fish sounds can alter crab foraging behaviour and influence bivalve abundance

The risk of predation can have large effects on ecological communities via changes in prey behaviour, morphology and reproduction. Although prey can use a variety of sensory signals to detect predation risk, relatively little is known regarding the effects of predator acoustic cues on prey foraging behaviour. Here we show that an ecologically important marine crab species can detect sound across a range of frequencies, probably in response to particle acceleration. Further, crabs suppress their resource consumption in the presence of experimental acoustic stimuli from multiple predatory fish species, and the sign and strength of this response is similar to that elicited by water-borne chemical cues. When acoustic and chemical cues were combined, consumption differed from expectations based on independent cue effects, suggesting redundancies among cue types. These results highlight that predator acoustic cues may influence prey behaviour across a range of vertebrate and invertebrate taxa, with the potential for cascading effects on resource abundance.     

Prey state shapes the effects of temporal variation in predation risk

The ecological impacts of predation risk are influenced by how prey allocate foraging effort across periods of safety and danger. Foraging decisions depend on current danger, but also on the larger temporal, spatial or energetic context in which prey manage their risks of predation and starvation. Using a rocky intertidal food chain, we examined the responses of starved and fed prey (Nucella lapillus dogwhelks) to different temporal patterns of risk from predatory crabs (Carcinus maenas). Prey foraging activity declined during periods of danger, but as dangerous periods became longer, prey state altered the magnitude of risk effects on prey foraging and growth, with likely consequences for community structure (trait-mediated indirect effects on basal resources, Mytilus edulis mussels), prey fitness and trophic energy transfer. Because risk is inherently variable over time and space, our results suggest that non-consumptive predator effects may be most pronounced in productive systems where prey can build energy reserves during periods of safety and then burn these reserves as ‘trophic heat’ during extended periods of danger. Understanding the interaction between behavioural (energy gain) and physiological (energy use) responses to risk may illuminate the context dependency of trait-mediated trophic cascades and help explain variation in food chain length.     

Behavioral plasticity in an invaded system: non-native whelks recognize risk from native crabs

Inducible defenses have the potential to affect both invasion success and the structure of invaded communities. However, little is known about the cues used for risk-recognition that influence the expression of inducible defenses in invasive prey, because they involve a novel threat. In laboratory experiments, we investigated behavioral defenses induced by a native crab on two invasive oyster drills (marine whelks Urosalpinx cinerea and Ocinebrina inornata). Both drills hid more often and reduced their feeding rates when they detected predators consuming conspecific prey. Examination of the responses of U. cinerea to specific cue sources (predator kairomones, conspecific alarm cues) indicated that this species had the strongest responses to cues from injured conspecifics, but that it did recognize the novel crab predator. Our observation of native predator (per se) recognition by an invasive marine prey is novel. In addition, we observed that neither species of drill reduced their defensive behavior to reflect predation risk shared by a group of prey. The lack of density dependence in risk-assessment could cause populations of invasive prey to transmit both quantitatively and qualitatively different community effects over the course of an invasion as abundance changes. Together, these findings demonstrate several ways that the risk-assessment strategies could be important in establishment and post-establishment dynamics of invasive prey.     

Relative strengths of trait-mediated and density-mediated indirect effects of a predator vary with resource levels in a freshwater food chain

Predators can affect the density and traits (e.g. morphology, behavior) of their prey, and either change may influence how prey interact with their resources. Thus, predators can interact indirectly with resource species (i.e. two trophic levels below) through two separate mechanisms. The relative strengths of these two kinds of indirect effects have rarely been compared directly, and how their relative importance varies across environmental gradients is virtually unknown. We investigated the relative strength of trait- and density-mediated indirect effects of the predatory insect Belostoma flumineum on algal communities through predation on the pond snail, Physa gyrina , across a gradient of basal resource abundance. Because prey balance the benefits of foraging against the increased risk of predation while foraging, the availability of the prey's resource should influence the strength of anti-predator behavioral responses and hence the strength of trait-mediated indirect interactions. Belostoma presence had positive indirect effects on resources as expected and total predator effects were constant across the basal resource gradient. At low initial resource levels, trait-mediated indirect effects on algal biomass exceeded density-mediated indirect effects, while at high initial resources the reverse was true. Snails showed similar habitat use across the resource gradient suggesting that the anti-predator response was most likely a depression of activity levels.     

Prey subsidy or predator cue? Direct and indirect effects of caged predators on aquatic consumers and resources

The non-consumptive effects of predators on prey can affect prey phenotypes, potentially having important consequences for communities due to trait-mediated indirect interactions. Predicting non-consumptive effects and their impacts on communities can be difficult because predators can affect resources directly through nutrient cycling and indirectly by altering prey resource use, which can lead to complex interactions among resources and consumers. In this study we examined the effects of caged dragonfly predators on aquatic resources in the presence and absence of two focal herbivores, the tadpoles of Neotropical tree frogs Agalychnis callidryas and Dendropsophus ebraccatus. We crossed the presence/absence of caged dragonflies with four tadpole treatments: no tadpoles, each tadpole species alone, and both species together to examine interactions among tadpole composition, predator presence, and time on tadpole growth, resources, and zooplankton abundances. Predator effects on growth changed through ontogeny and was species-dependent. Predators initially reduced then dramatically increased A. callidryas growth, but had no effect on D. ebraccatus. Predators also increased the abundances of both periphyton and phytoplankton. However, there was no evidence of a trait-mediated trophic cascade (i.e., tadpole by predator interaction). Instead, nutrients from prey carcass subsidies likely played an increasingly important role in facilitating resources, and shaping tadpole growth, competitive interactions, and zooplankton abundances through time. In nutrient-poor aquatic systems the release of nutrients via the consumption of terrestrially derived prey items by aquatic predators may have important impacts on food webs by facilitating resources independent of the role of trait-mediated trophic cascades.     

Predator pheromone elicits a temporally dependent non-consumptive effect in prey

1. The influence of predator cues on the behaviour of prey is well supported in the literature; however, a clear understanding of how predator cues affect prey in variable environmental conditions and over longer time scales is needed to better understand the underlying mechanisms. Here, we measure how predator odors affect herbivore colonization, abundance, oviposition, and plant damage across two growing seasons.
2. The study system consisted of Leptinotarsa decemlineata (Colorado potato beetle) as prey, and the aggregation pheromone of live Podisus maculiventris (spined soldier bug) as the predator cue in a potato field.
3. In 2016, the amount of feeding damage by early beetle colonists was lower in predator odor-treated plots, reducing plant damage by 22%. Larval abundance was also reduced in treated plots in 2016. Beetle abundance and damage in 2017 was similar in the treatment and control plots. Two mechanisms were investigated to better understand why prey response to the predator odor treatment weakened over the first season, including changes in predator odor cue strength and prey habituation. Predator odor cue strength emerged as a likely explanation, as dispensers, which released a synthetic predator pheromone over the entire season, reduced the probability of finding damage more consistently than the live predator treatment.
4. These results suggest that temporal patterns of predator cue release and strength may drive prey response across the season, underscoring the importance of cue release-rate and consistency in both species interactions and for the future application of modifying insect behaviour using non-consumptive effects in agricultural systems.

     

Restricting Prey Dispersal Can Overestimate the Importance of Predation in Trophic Cascades

Predators can affect prey populations and, via trophic cascades, predators can indirectly impact resource populations (2 trophic levels below the predator) through consumption of prey (density-mediated indirect effects; DMIEs) and by inducing predator-avoidance behavior in prey (trait-mediated indirect effects; TMIEs). Prey often employ multiple predator-avoidance behaviors, such as dispersal or reduced foraging activity, but estimates of TMIEs are usually on individual behaviors. We assessed direct and indirect predator effects in a mesocosm experiment using a marine food chain consisting of a predator (toadfish – Opsanus tau), prey (mud crab - Panopeus herbstii) and resource (ribbed mussel – Geukensia demissa). We measured dispersal and foraging activity of prey separately by manipulating both the presence and absence of the predator, and whether prey could or could not disperse into a predator-free area. Consumption of prey was 9 times greater when prey could not disperse, probably because mesocosm boundaries increased predator capture success. Although predator presence did not significantly affect the number of crabs that emigrated, the presence of a predator decreased resource consumption by prey, which resulted in fewer resources consumed for each prey that emigrated in the presence of a predator, and reduced the overall TMIE. When prey were unable to disperse, TMIEs on mussel survival were 3 times higher than the DMIEs. When prey were allowed to disperse, the TMIEs on resource survival increased to 11-times the DMIEs. We found that restricting the ability of prey to disperse, or focusing on only one predator-avoidance behavior, may be underestimating TMIEs. Our results indicate that the relative contribution of behavior and consumption in food chain dynamics will depend on which predator-avoidance behaviors are allowed to occur and measured.     

The context dependence of non‐consumptive predator effects

Non‐consumptive predator effects (NCEs) are now widely recognised for their capacity to shape ecosystem structure and function. Yet, forecasting the propagation of these predator‐induced trait changes through particular communities remains a challenge. Accordingly, focusing on plasticity in prey anti‐predator behaviours, we conceptualise the multi‐stage process by which predators trigger direct and indirect NCEs, review and distil potential drivers of contingencies into three key categories (properties of the prey, predator and setting), and then provide a general framework for predicting both the nature and strength of direct NCEs. Our review underscores the myriad factors that can generate NCE contingencies while guiding how research might better anticipate and account for them. Moreover, our synthesis highlights the value of mapping both habitat domains and prey‐specific patterns of evasion success (‘evasion landscapes’) as the basis for predicting how direct NCEs are likely to manifest in any particular community. Looking ahead, we highlight two key knowledge gaps that continue to impede a comprehensive understanding of non‐consumptive predator–prey interactions and their ecosystem consequences; namely, insufficient empirical exploration of (1) context‐dependent indirect NCEs and (2) the ways in which direct and indirect NCEs are shaped interactively by multiple drivers of context dependence.     

Human activity helps prey win the predator-prey space race

Predator-prey interactions, including between large mammalian wildlife species, can be represented as a "space race", where prey try to minimize and predators maximize spatial overlap. Human activity can also influence the distribution of wildlife species. In particular, high-human disturbance can displace large carnivore predators, a trait-mediated direct effect. Predator displacement by humans could then indirectly benefit prey species by reducing predation risk, a trait-mediated indirect effect of humans that spatially decouples predators from prey. The purpose of this research was to test the hypothesis that high-human activity was displacing predators and thus indirectly creating spatial refuge for prey species, helping prey win the "space race". We measured the occurrence of eleven large mammal species (including humans and cattle) at 43 camera traps deployed on roads and trails in southwest Alberta, Canada. We tested species co-occurrence at camera sites using hierarchical cluster and nonmetric multidimensional scaling (NMS) analyses; and tested whether human activity, food and/or habitat influenced predator and prey species counts at camera sites using regression tree analysis. Cluster and NMS analysis indicated that at camera sites humans co-occurred with prey species more than predator species and predator species had relatively low co-occurrence with prey species. Regression tree analysis indicated that prey species were three times more abundant on roads and trails with >32 humans/day. However, predators were less abundant on roads and trails that exceeded 18 humans/day. Our results support the hypothesis that high-human activity displaced predators but not prey species, creating spatial refuge from predation. High-human activity on roads and trails (i.e., >18 humans/day) has the potential to interfere with predator-prey interactions via trait-mediated direct and indirect effects. We urge scientist and managers to carefully consider and quantify the trait-mediated indirect effects of humans, in addition to direct effects, when assessing human impacts on wildlife and ecosystems.     

Fear of predation alters soil carbon dioxide flux and nitrogen content

Predators are known to have both consumptive and non-consumptive effects (NCEs) on their prey that can cascade to affect lower trophic levels. Non-consumptive interactions often drive these effects, though the majority of studies have been conducted in aquatic- or herbivory-based systems. Here, we use a laboratory study to examine how linkages between an above-ground predator and a detritivore influence below-ground properties. We demonstrate that predators can depress soil metabolism (i.e. CO₂ flux) and soil nutrient content via both consumptive and non-consumptive interactions with detritivores, and that the strength of isolated NCEs is comparable to changes resulting from predation. Changes in detritivore abundance and activity in response to predators and the fear of predation likely mediate interactions with the soil microbe community. Our results underscore the need to explore these mechanisms at large scales, considering the disproportionate extinction risk faced by predators and the importance of soils in the global carbon cycle.     

A meta‐analysis of non‐consumptive predator effects in arthropods: the influence of organismal and environmental characteristics

Non‐consumptive effects (NCEs) – changes in prey behavior or physiology in response to predator threat – are common and can be as strong as consumptive effects. However, our knowledge of NCEs in arthropod systems is lacking. Factors related to study organism and environment have the potential to influence the occurrence and magnitude of NCEs in arthropod systems. While factors such as coevolutionary history of natural enemies and their prey, predator cue, predator or prey feeding mode, and refuge availability have been theoretically and empirically examined, no trends have been proposed for arthropods. We compiled 62 studies, yielding 128 predator–prey interactions, which explicitly examined NCEs in experiments where arthropods were identified to species, using a previously published database of papers from 1990 to 2005 and a new database of papers published from 2006 to 2015. Using these data, we conducted a meta‐analysis to explore the influence of organismal and environmental characteristics on the magnitude of predator NCEs. Our analysis addressed the following three questions. 1) Does predator–prey coevolution give rise to stronger NCEs than when predator and prey species did not coevolve? 2) What influence does habitat type and refuge availability have on NCEs? 3) How do predator characteristics (cue type, hunting mode and life stage) and prey characteristics (mobility, life stage, specialization, gregariousness and feeding mode) influence NCEs? We found that while NCEs were similar across most measured characteristics, NCEs on prey activity were significantly stronger when predator and prey shared an evolutionary history. Our results support growing evidence that NCEs have a negative effect on prey traits and that behavioral NCEs are stronger than physiological ones. Additional studies are needed to be confident in any emerging patterns, therefore we identify key gaps in the literature on NCEs in arthropod systems and discuss ideas for moving forward.     

Mesopredator suppression by an apex predator alleviates the risk of predation perceived by small prey

Predators can impact their prey via consumptive effects that occur through direct killing, and via non-consumptive effects that arise when the behaviour and phenotypes of prey shift in response to the risk of predation. Although predators'' consumptive effects can have cascading population-level effects on species at lower trophic levels there is less evidence that predators'' non-consumptive effects propagate through ecosystems. Here we provide evidence that suppression of abundance and activity of a mesopredator (the feral cat) by an apex predator (the dingo) has positive effects on both abundance and foraging efficiency of a desert rodent. Then by manipulating predators'' access to food patches we further the idea that apex predators provide small prey with refuge from predation by showing that rodents increased their habitat breadth and use of ‘risky′ food patches where an apex predator was common but mesopredators rare. Our study suggests that apex predators'' suppressive effects on mesopredators extend to alleviate both mesopredators'' consumptive and non-consumptive effects on prey.