The influence of temporally variable predation risk on indirect interactions in an aquatic food chain

We know little about how temporally variable predation risk influences prey behavior. The risk allocation hypothesis predicts that prey facing more frequent risk should show weak anti-predator responses, and should be particularly active foragers during rare periods of safety, compared to prey facing infrequent risk. Several studies offer support for the risk allocation hypothesis, but how these responses might propagate through the larger ecological community remains largely unknown. We experimentally investigated the relative strength of trait- and density-mediated indirect effects of a predator on its prey’s resource across predation treatments that varied the lethality (caged or free-swimming predators) and temporal variability (always, often, or sometimes present) of predation. We performed this experiment in pond mesocosms using a giant water bug predator (Belostoma lutarium), an herbivorous pond snail (Physa gyrina), and algae as the basal resource. Snails greatly reduced the abundance of their algal resource when in the absence of predation. Lethal predation at low and medium intensities had significant positive indirect effects on the abundance of algae, mostly by reducing snail density. Snails responded behaviorally to high levels of deadly predation by foraging more and hiding less than in other situations, as predicted by the risk allocation hypothesis, and thus ameliorated the density-mediated indirect effects of predators on algae. Behavioral responses to caged predators, and the subsequent trait-mediated indirect effects, were negligible regardless of predation intensity. Our previous work has demonstrated that trait-mediated indirect effects are weak when resources are abundant, as they were in this experiment. This work demonstrates that temporal variation in predation intensity plays a key role in determining the relative strength of TMIIs and DMIIs in an aquatic food chain.     

Seasonal Trophic Niche Shift and Cascading Effect of a Generalist Predator Fish

Few studies have examined how foraging niche shift of a predator over time cascade down to local prey communities. Here we examine patterns of temporal foraging niche shifts of a generalist predator (yellow catfish, Pelteobagrus fulvidraco) and the abundance of prey communities in a subtropical lake. We predicted that the nature of these interactions would have implications for patterns in diet shifts and growth of the predator. Our results show significant decreases in planktivory and benthivory from late spring to summer and autumn, whereas piscivory increased significantly from mid-summer until late autumn and also increased steadily with predator body length. The temporal dynamics in predator/prey ratios indicate that the predation pressure on zooplankton and zoobenthos decreased when the predation pressure on the prey fish and shrimps was high. Yellow catfish adjusted their foraging strategies to temporal changes in food availability, which is in agreement with optimal foraging theory. Meanwhile the decrease in planktivory and benthivory of yellow catfish enabled primary consumers, such as zooplankton and benthic invertebrates, to develop under low grazing pressure via trophic cascading effects in the local food web. Thus, yellow catfish shifts its foraging niche to intermediate consumers in the food web to benefit the energetic demand on growth and reproduction during summer, which in turn indirectly facilitate the primary consumers. In complex food webs, trophic interactions are usually expected to reduce the strength and penetrance of trophic cascades. However, our study demonstrates strong associations between foraging niche of piscivorous fish and abundance of prey. This relationship appeared to be an important factor in producing top-down effects on both benthic and planktonic food webs.     

Does Temporal Variation in Predation Risk Influence the Intensity of Antipredator Responses? A Test of the Risk Allocation Hypothesis

Temporal variation in predation risk may fundamentally influence antipredator responses of prey animals. To maximize lifetime fitness, prey must be able to optimize energy gain and minimize predation risk, and responses to current levels of risk may be influenced by background levels of risk. A ‘risk allocation’ model has recently been proposed to predict the intensity of antipredator responses that should occur as predation risk varies over time. Prey animals from high‐risk environments should respond to predators with relatively low intensities of antipredator behaviour because long periods of antipredator behaviour may result in unacceptable decreases in levels of foraging activity. Moreover, animals that are under frequent risk should devote more energy to foraging during brief pulses of safety compared with animals under infrequent attack. In this study, we experimentally tested the risk allocation hypothesis. We exposed juvenile rainbow trout, Oncorhynchus mykiss, to three levels of risk (high, moderate and low) crossed with two levels of temporal variation (exposed to risk three times a day and once a day). In accordance with the model, we found that trout exposed to risky situations more frequently responded with significantly less intense antipredator behaviour than trout exposed to risk infrequently. The intensity of response of trout exposed to moderate risk three times a day decreased to levels similar to situations of no risk. However, in contrast to the second prediction of the model, animals under frequent risk were not more active during periods of safety compared with animals under infrequent risk. Although behaviour in the face of predation risk was dependent on the broader temporal context in which risk varied, the specific predictions of the risk allocation model were only partly supported.     

Resource levels and prey state influence antipredator behavior and the strength of nonconsumptive predator effects

The risk of predation can drive trophic cascades by causing prey to engage in antipredator behavior (e.g. reduced feeding), but these behaviors can be energetically costly for prey. The effects of predation risk on prey (nonconsumptive effects, NCEs) and emergent indirect effects on basal resources should therefore depend on the ecological context (e.g. resource abundance, prey state) in which prey manage growth/predation risk tradeoffs. Despite an abundance of behavioral research and theory examining state‐dependent responses to risk, there is a lack of empirical data on state‐dependent NCEs and their impact on community‐level processes. We used a rocky intertidal food chain to test model predictions for how resources levels and prey state (age/size) shape the magnitude of NCEs. Risk cues from predatory crabs Carcinus maenas caused juvenile and sub‐adult snails Nucella lapillus to increase their use of refuge habitats and decrease their growth and per capita foraging rates on barnacles Semibalanus balanoides. Increasing resource levels (high barnacle density) and prey state (sub‐adults) enhanced the strength of NCEs. Our results support predictions that NCEs will be stronger in resource‐rich systems that enhance prey state and suggest that the demographic composition of prey populations will influence the role of NCEs in trophic cascades. Contrary to theory, however, we found that resources and prey state had little to no effect on snails in the presence of predation risk. Rather, increases in NCE strength arose because of the strong positive effects of resources and prey state on prey foraging rates in the absence of risk. Hence, a common approach to estimating NCE strength – integrating measurements of prey traits with and without predation risk into a single metric – may mask the underlying mechanisms driving variation in the strength and relative importance of NCEs in ecological communities.     

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.     

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.     

Climate change enhances the negative effects of predation risk on an intermediate consumer

Predators are a major source of stress in natural systems because their prey must balance the benefits of feeding with the risk of being eaten. Although this ‘fear’ of being eaten often drives the organization and dynamics of many natural systems, we know little about how such risk effects will be altered by climate change. Here, we examined the interactive consequences of predator avoidance and projected climate warming in a three‐level rocky intertidal food chain. We found that both predation risk and increased air and sea temperatures suppressed the foraging of prey in the middle trophic level, suggesting that warming may further enhance the top‐down control of predators on communities. Prey growth efficiency, which measures the efficiency of energy transfer between trophic levels, became negative when prey were subjected to predation risk and warming. Thus, the combined effects of these stressors may represent an important tipping point for individual fitness and the efficiency of energy transfer in natural food chains. In contrast, we detected no adverse effects of warming on the top predator and the basal resources. Hence, the consequences of projected warming may be particularly challenging for intermediate consumers residing in food chains where risk dominates predator‐prey interactions.     

Semi‐intensive shrimp farms as experimental arenas for the study of predation risk from falcons to shorebirds

Varying environmental conditions and energetic demands can affect habitat use by predators and their prey. Anthropogenic habitats provide an opportunity to document both predation events and foraging activity by prey and therefore enable an empirical evaluation of how prey cope with trade‐offs between starvation and predation risk in environments of variable foraging opportunities and predation danger. Here, we use seven years of observational data of peregrine falcons Falco peregrinus and shorebirds at a semi‐intensive shrimp farm to determine how starvation and predation risk vary for shorebirds under a predictable variation in foraging opportunities. Attack rate (mean 0.1 attacks/hr, equating 1 attack every ten hours) was positively associated with the total foraging area available for shorebirds at the shrimp farm throughout the harvesting period, with tidal amplitude at the adjacent mudflat having a strong nonlinear (quadratic) effect. Hunt success (mean 14%) was higher during low tides and declined as the target flocks became larger. Finally, individual shorebird vigilance behaviors were more frequent when birds foraged in smaller flocks at ponds with poorer conditions. Our results provide empirical evidence of a risk threshold modulated by tidal conditions at the adjacent wetlands, where shorebirds trade‐off risk and rewards to decide to avoid or forage at the shrimp farm (a potentially dangerous habitat) depending on their need to meet daily energy requirements. We propose that semi‐intensive shrimp farms serve as ideal “arenas” for studying predator–prey dynamics of shorebirds and falcons, because harvest operations and regular tidal cycles create a mosaic of foraging patches with predictable food supply. In addition, the relatively low hunt success suggests that indirect effects associated with enhanced starvation risk are important in shorebird life‐history decisions.     

Fixed vs. Random Temporal Predictability of Predation Risk: An Extension of the Risk Allocation Hypothesis

Predation is a strong selective force acting on prey animals. Predation is by nature highly variable in time; however, this aspect of predation risk has traditionally been overlooked by behavioural ecologists. Lima and Bednekoff proposed the predation risk allocation hypothesis (RAH), predicting how temporal variation in predation risk drives prey antipredator behaviours. This model is based on the concept that prey adaptively allocate their foraging and antipredator efforts across high‐ and low‐risk situations, depending on the duration of high‐ vs. low‐risk situations and the relative risk associated with each of them. An unstudied extension of the RAH is the effect of predictability of predation risk. A predictable risk should lead to prey displaying minimal vigilance behaviours during predictable low‐risk periods and the strongest antipredator behaviours during risky periods. Conversely, an unpredictable predation risk should result in prey displaying constant vigilance behaviour, with suboptimal foraging rates during periods of safety but antipredator behaviours of lower intensity during periods of risk. We tested this extension of the RAH using convict cichlids exposed to high‐risk alarm cues at two frequencies of risk (1× vs. 3×) per day, on either a fixed or random schedule for 5 d. We then tested the fish for a response to high‐risk cues (alarm cues) and to low‐risk cues (disturbance resulting from the introduction of distilled water). Our study supports previous results on the effects of risk frequency and cue intensity on cichlid behaviour. We failed to show an effect of risk predictability on the behavioural responses of cichlids to high‐risk alarm cues, but predictability did influence responses to low‐risk cues. We encourage further studies to test the effect of predictability in other systems.     

Patch use in time and space for a meso-predator in a risky world

Predator–prey studies often assume a three trophic level system where predators forage free from any risk of predation. Since meso-predators themselves are also prospective prey, they too need to trade-off between food and safety. We applied foraging theory to study patch use and habitat selection by a meso-predator, the red fox. We present evidence that foxes use a quitting harvest rate rule when deciding whether or not to abandon a foraging patch, and experience diminishing returns when foraging from a depletable food patch. Furthermore, our data suggest that patch use decisions of red foxes are influenced not just by the availability of food, but also by their perceived risk of predation. Fox behavior was affected by moonlight, with foxes depleting food resources more thoroughly (lower giving-up density) on darker nights compared to moonlit nights. Foxes reduced risk from hyenas by being more active where and when hyena activity was low. While hyenas were least active during moon, and most active during full moon nights, the reverse was true for foxes. Foxes showed twice as much activity during new moon compared to full moon nights, suggesting different costs of predation. Interestingly, resources in patches with cues of another predator (scat of wolf) were depleted to significantly lower levels compared to patches without. Our results emphasize the need for considering risk of predation for intermediate predators, and also shows how patch use theory and experimental food patches can be used for a predator. Taken together, these results may help us better understand trophic interactions.     

Predator identity and time of day interact to shape the risk–reward trade-off for herbivorous coral reef fishes

Non-consumptive effects (NCEs) of predators occur as prey alters their habitat use and foraging decisions to avoid predation. Although NCEs are recognized as being important across disparate ecosystems, the factors influencing their strength and importance remain poorly understood. Ecological context, such as time of day, predator identity, and prey condition, may modify how prey species perceive and respond to risk, thereby altering NCEs. To investigate how predator identity affects foraging of herbivorous coral reef fishes, we simulated predation risk using fiberglass models of two predator species (grouper Mycteroperca bonaci and barracuda Sphyraena barracuda) with different hunting modes. We quantified how predation risk alters herbivory rates across space (distance from predator) and time (dawn, mid-day, and dusk) to examine how prey reconciles the conflicting demands of avoiding predation vs. foraging. When we averaged the effect of both predators across space and time, they suppressed herbivory similarly. Yet, they altered feeding differently depending on time of day and distance from the model. Although feeding increased strongly with increasing distance from the predators particularly during dawn, we found that the barracuda model suppressed herbivory more strongly than the grouper model during mid-day. We suggest that prey hunger level and differences in predator hunting modes could influence these patterns. Understanding how context mediates NCEs provides insight into the emergent effects of predator–prey interactions on food webs. These insights have broad implications for understanding how anthropogenic alterations to predator abundances can affect the spatial and temporal dynamics of important ecosystem processes.     

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.     

捕食风险及其对动物觅食行为的影响

对捕食风险的涵义及其对猎物动物觅食行为的影响、猎物动物面对捕食风险时的反应进行了论述。捕食风险可以简单地理解为一定时间内猎物动物被杀死的概率。当捕食风险存在时 ,动物会选择相对安全但觅食效益较低的地点觅食 ;由于死亡率和消化方面的限制 ,一般都会产生食谱收缩 ;觅食活动方式的时间格局也会因捕食风险而发生改变 ,如水生动物的昼夜垂直迁移、某些陆生动物昼行性与夜行性活动的转换、月光回避等。在与捕食者发生遭遇时 ,猎物动物的主要反应是 :①发出某些信号以阻止捕食者的追捕 ;②靠近并注视捕食者 ;③逃逸 ;④在一定的时间恢复觅食活动。在以往的研究中 ,对捕食者种类已经有了较多的了解 ,而对猎物如何判断捕食者丰富度信息、估计风险程度等方面则知之甚少 ;同时 ,对捕食风险水平的调控、对多种因素的综合分析也较少涉及。在今后的研究中 ,还应该考虑研究的尺度问题 ,因为在不同尺度的环境条件下 ,猎物动物对于捕食风险的反应可能大相径庭。     

How climate change might influence the starvation–predation risk trade-off response

Climate change within the UK will affect winter starvation risk because higher temperatures reduce energy budgets and are likely to increase the quality of the foraging environment. Mass regulation in birds is a consequence of the starvation–predation risk trade-off: decreasing starvation risk because of climate change should decrease mass, but this will be countered by the effects of predation risk, because high predation risk has a negative effect on mass when foraging conditions are poor and a positive effect on mass when foraging conditions are good. We tested whether mass regulation in great tits (Parus major) across the UK was related to temporal changes in starvation risk (winter temperature 1995–2005) and spatial changes in predation risk (sparrowhawk Accipiter nisus abundance). As predicted, great tits carried less mass during later, warmer, winters, demonstrating that starvation risk overall has decreased. Also, the effects of predation risk interacted with the effects of temperature (as an index of foraging conditions), so that in colder winters higher sparrowhawk abundance led to lower mass, whereas in warmer, later, winters higher sparrowhawk abundance led to higher mass. Mass regulation in a small bird species may therefore provide an index of how environmental change is affecting the foraging environment.     

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.     

Hazardous duty pay and the foraging cost of predation

We review the concepts and research associated with measuring fear and its consequences for foraging. When foraging, animals should and do demand hazardous duty pay. They assess a foraging cost of predation to compensate for the risk of predation or the risk of catastrophic injury. Similarly, in weighing foraging options, animals tradeoff food and safety. The foraging cost of predation can be modelled, and it can be quantitatively and qualitatively measured using risk titrations. Giving‐up densities (GUDs) in depletable food patches and the distribution of foragers across safe and risky feeding opportunities are two frequent experimental tools for titrating food and safety. A growing body of literature shows that: (i) the cost of predation can be big and comprise the forager's largest foraging cost, (ii) seemingly small changes in habitat or microhabitat characteristics can lead to large changes in the cost of predation, and (iii) a forager's cost of predation rises with risk of mortality, the forager's energy state and a decrease in its marginal value of energy. In titrating for the cost of predation, researchers have investigated spatial and temporal variation in risk, scale‐dependent variation in risk, and the role of predation risk in a forager's ecology. A risk titration from a feeding animal often provides a more accurate behavioural indicator of predation risk than direct observations of predator‐inflicted mortality. Titrating for fear responses in foragers has some well‐established applications and holds promise for novel methodologies, concepts and applications. Future directions for expanding conceptual and empirical tools include: what are the consequences of foraging costs arising from interference behaviours and other sources of catastrophic loss? Are there alternative routes by which organisms can respond to tradeoffs of food and safety? What does an animal's landscape of fear look like as a spatially explicit map, and how do various environmental factors affect it? Behavioural titrations will help to illuminate these issues and more.     

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.     

Indirect risk effects reduce feeding efficiency of ducks during spring

Indirect risk effects of predators on prey behavior can have more of an impact on prey populations than direct consumptive effects. Predation risk can elicit more vigilance behavior in prey, reducing the amount of time available for other activities, such as foraging, which could potentially reduce foraging efficiency. Understanding the conditions associated with predation risk and the specific effects predation risk have on prey behavior is important because it has direct influences on the profitability of food items found under various conditions and states of the forager. The goals of this study were to assess how ducks perceived predation risk in various habitat types and how strongly perceived risk versus energetic demand affected foraging behavior. We manipulated food abundance in different wetland types in Illinois, USA to reduce confounding between food abundance and vegetation structure. We conducted focal‐animal behavioral samples on five duck species in treatment and control plots and used generalized linear mixed‐effects models to compare the effects of vegetation structure versus other factors on the intensity with which ducks fed and the duration of feeding stints. Mallards fed more intensively and, along with blue‐winged teal, used longer feeding stints in open habitats, consistent with the hypothesis that limited visibility was perceived to have a greater predation risk than unlimited visibility. The species temporally nearest to nesting, wood ducks, were willing to take more risks for a greater food reward, consistent with an increase in a marginal value of energy as they approached nesting. Our results indicate that some duck species value energy differently based on the surrounding vegetation structure and density. Furthermore, increases in the marginal value of energy can be more influential than perceived risk in shaping foraging behavior patterns. Based on these findings, we conclude that the value of various food items is not solely determined by energy contained in the item but by conditions in which it is found and the state of the forager.     

Herbivore release through cascading risk effects

Predators influence prey through consumption, and through trait-mediated effects such as emigration in response to predation risk (risk effects). We studied top-down effects of (sub-) adult wolf spiders (Lycosidae) on arthropods in a meadow. We compared risk effects with the overall top-down effect (including consumption) by gluing the chelicers of wolf spiders to prevent them from killing the prey. In a field experiment, we created three treatments that included either: (i) intact (‘predation’) wolf spiders; (ii) wolf spiders with glued chelicers (‘risk spiders’); or (iii) no (sub-) adult wolf spiders. Young wolf spiders were reduced by their (sub-) adult congeners. Densities of sheetweb spiders (Linyphiidae), a known intraguild prey of wolf spiders, were equally reduced by the presence of risk and predation wolf spiders. Plant- and leafhoppers (Auchenorrhyncha) showed the inverse pattern of higher densities in the presence of both risk and predation wolf spiders. We conclude that (sub-) adult wolf spiders acted as top predators, which reduced densities of intermediate predators and thereby enhanced herbivores. Complementary to earlier studies that found trait-mediated herbivore suppression, our results demonstrate that herbivores can be enhanced through cascading risk effects by top predators.     

Predation-risk effects of predator identity on the foraging behaviors of frugivorous bats

Predators directly and indirectly affect the density and the behavior of prey. These effects may potentially cascade down to lower trophic levels. In this study, we tested the effects of predator calls (playbacks of bird vocalizations: Tyto alba, Speotyto cunicularia, and Vanellus chilensis), predator visual stimuli (stuffed birds) and interactions of visual and auditory cues, on the behavior of frugivore phyllostomid bats in the field. In addition, we tested if the effects of predation risk cascade down to other trophic levels by measuring rates of seed dispersal of the tree Muntingia calabura. Using video recording, we found that bats significantly decreased the foraging frequency on trees when a visual cue of T. alba was present. However, no stimuli of potential predatory birds, including vocalization of T. alba, affected bat foraging frequency. There was a change in bat behavior during 7 min, but then their frequency of activity gradually increased. Consequently, the presence of T. alba decreased by up to ten times the rate of seed removal. These results indicate that risk sensitivity of frugivorous phyllostomid bats depends on predator identity and presence. Among the predators used in this study, only T. alba is an effective bat predator in the Neotropics. Sound stimuli of T. alba seem not to be a cue of predation risk, possibly because their vocalizations are used only for intraspecific communication. This study emphasizes the importance of evaluating different predator stimuli on the behavior of vertebrates, as well as the effects of these stimuli on trait-mediated trophic cascades.