Dying from the lesser of three evils: facilitation and non‐consumptive effects emerge in a model with multiple predators

Prey modify their behaviour to avoid predation, but dilemmas arise when predators vary in hunting style. Behaviours that successfully evade one predator sometimes facilitate exposure to another predator, forcing the prey to choose the lesser of two evils. In such cases, we need to quantify behavioural strategies in a mix of predators. We model optimal behaviour of Atlantic cod Gadus morhua larvae in a water column, and find the minimal vulnerability from three common predator groups with different hunting modes; 1) ambush predators that sit‐and‐wait for approaching fish larvae; 2) cruising invertebrates that eat larvae in their path; and 3) fish which are visually hunting predators. We use a state‐dependent model to find optimal behaviours (vertical position and swimming speed over a diel light cycle) under any given exposure to the three distinct modes of predation. We then vary abundance of each predator and quantify direct and indirect effects of predation. The nature and strength of direct and indirect effects varied with predator type and abundance. Larvae escaped about half the mortality from fish by swimming deeper to avoid light, but their activity level and cumulative predation from ambush predators increased. When ambush invertebrates dominated, it was optimal to be less active but in more lit habitats, and predation from fish increased. Against cruising predators, there was no remedy. In all cases, the shift in behaviour allowed growth to remain almost the same, while total predation were cut by one third. In early life stages with high and size‐dependent mortality rates, growth rate can be a poor measure of the importance of behavioural strategies.     

Predator hunting modes and predator–prey space games

Predators and prey are often engaged in a game where their expected fitnesses are affected by their relative spatial distributions. Game models generally predict that when predators and prey move at similar temporal and spatial scales that predators should distribute themselves to match the distribution of the prey's resources and that prey should be relatively uniformly distributed. These predictions should better apply to sit-and-pursue and sit-and-wait predators, who must anticipate the spatial distributions of their prey, than active predators that search for their prey. We test this with an experiment observing the spatial distributions and estimating the causes of movements between patches for Pacific tree frog tadpoles (Pseudacris regilla), a sit-and-pursue dragonfly larvae predator (Rhionaeschna multicolor), and an active salamander larval predator (Ambystoma tigrinum mavortium) when a single species was in the arena and when the prey was with one of the predators. We find that the sit-and-pursue predator favors patches with more of the prey's algae resources when the prey is not in the experimental arena and that the prey, when in the arena with this predator, do not favor patches with more resources. We also find that the active predator does not favor patches with more algae and that prey, when with an active predator, continue to favor these higher resource patches. These results suggest that the hunting modes of predators impact their spatial distributions and the spatial distributions of their prey, which has potential to have cascading effects on lower trophic levels.     

Rethinking trophic niches: Speed and body mass colimit prey space of mammalian predators

1. Realized trophic niches of predators are often characterized along a one‐dimensional range in predator–prey body mass ratios. This prey range is constrained by an “energy limit” and a “subdue limit” toward small and large prey, respectively. Besides these body mass ratios, maximum speed is an additional key component in most predator–prey interactions.
2. Here, we extend the concept of a one‐dimensional prey range to a two‐dimensional prey space by incorporating a hump‐shaped speed‐body mass relation. This new “speed limit” additionally constrains trophic niches of predators toward fast prey.
3. To test this concept of two‐dimensional prey spaces for different hunting strategies (pursuit, group, and ambush predation), we synthesized data on 63 terrestrial mammalian predator–prey interactions, their body masses, and maximum speeds.
4. We found that pursuit predators hunt smaller and slower prey, whereas group hunters focus on larger but mostly slower prey and ambushers are more flexible. Group hunters and ambushers have evolved different strategies to occupy a similar trophic niche that avoids competition with pursuit predators. Moreover, our concept suggests energetic optima of these hunting strategies along a body mass axis and thereby provides mechanistic explanations for why there are no small group hunters (referred to as “micro‐lions”) or mega‐carnivores (referred to as “mega‐cheetahs”).
5. Our results demonstrate that advancing the concept of prey ranges to prey spaces by adding the new dimension of speed will foster a new and mechanistic understanding of predator trophic niches and improve our predictions of predator–prey interactions, food web structure, and ecosystem functions.

     

Autotomy and its Effects on Wolf Spider Foraging Success

Few studies have attempted to determine how physical injury affects predators. One of the ways that physical injury can be expressed is by autotomy or the voluntary loss of a body part. Here, we examined whether the loss of specific legs affects the foraging success of the wolf spider Rabidosa santrita (predator) on another species, Pardosa valens (prey). We also wanted to identify whether the loss of legs in both the predator and prey would impact the outcome of a predation event. Both predator and prey were collected from a creek bed at Portal, AZ, in 2012. Predators were randomly assigned groups where all prey items were intact or all prey had one randomly chosen leg IV removed. Within these groups, predators were organized into a control, leg I autotomy, or leg IV autotomy treatment. All predators had their pre‐ and post‐foraging running speed determined. Predators were introduced into chambers with five prey items and allowed to forage for 1 h. The leg position autotomized or the comparison of pre‐ and post‐foraging trials had no effect on predator running speed. Additionally, there was no significant effect of either predator or prey leg treatment on the total proportion of prey items captured by the end of the foraging trials. Survival analyses indicated that intact prey items tended to have a higher survival rate when predators were missing a leg IV than when predators were intact. When both the predator and prey were missing legs, no significant difference in prey survival rates was detected. We suggest that for predators that inhabit complex, heterogeneous habitats and are classified as ambush predators, the loss of a limb may affect prey capture success, especially when the prey is intact, but that increased sample size is necessary to determine whether this trend is significant.     

Indirect cues in selecting a hunting site in a sit‐and‐wait predator

Sit‐and‐wait predators use relatively simple rules for their decisions to choose and leave a patch, such as using the direct presence of prey to select a hunting site. However, the direct presence of prey can only be used when there is a highly visited patch in the proximity of the predator. Therefore, it is plausible that sit‐and‐wait predators also exploit indirect cues of prey presence and, consequently, use associative learning to select a hunting site. The present study tests for the role of associative learning in a sit‐and‐wait predator species for which the ecology is well understood: Misumena vatia Clerck crab spiders. An ecologically relevant scenario is used by selecting flower colour as the conditioned stimulus and prey presence as the unconditioned stimulus. The results provide no evidence that M. vatia crab spiders use the association between flower colour and food presence for selecting a hunting site. After a training phase of being exposed to a colourful artificial flower highly visited by bees, spiders select a hunting site independently of its colour during the testing phase. Investigations of similar scope and ecological relevance are required with other sit‐and‐wait predators to identify the conditions promoting the use of associative learning for foraging site selection when animals face an unpredictable food supply.     

Influence of sprint speed and body size on predator avoidance in New Mexican spadefoot toads (<Emphasis Type="Italic">Spea multiplicata</Emphasis>)

Predator–prey interactions play an important role in community dynamics and may be important for promoting genetic diversification. Diversification may be especially important when prey species have multiple anti-predator strategies available, but these strategies conflict with each other. For example, rapid sprint speed and large size are both thought to decrease vulnerability to many predators. A physiological trade-off between swimming speed and growth rate has been documented in many aquatic species and, as a result, individual genotypes may employ one strategy or the other, but not both. Although rapid sprint speed is often assumed to decrease vulnerability to predators, this has only rarely been tested. Here I provide evidence that both rapid sprint speed and large size in tadpoles of the New Mexico spadefoot toad (Spea multiplicata) decreases predation risk from carnivore morphs of its congener the Great Plains spadefoot toad (Spea bombifrons). Such conflicts, coupled with spatio-temporal variation in predation pressure, may be important in maintaining genetic variation for trade-offs.     

Effect of temperature extremes on the spatial dynamics of predator–prey interactions: A case study with dragonfly nymphs and newt larvae

Theory predicts that predators are more vulnerable to increasing temperature than prey. Despite huge variations in the magnitude and duration of thermally-extreme episodes in nature, most empirical studies on predator–prey interactions consider conditions induced by a climatic shift in mean temperature. We asked whether the increased vulnerability of predators holds under daily thermal extremes occurring during heat waves, using dragonfly nymphs and newt larvae as the predator–prey model system. Direct exposure of predator to prey in heated and non-heated aquaria under semi-natural conditions revealed that predator movements increased with rising temperature, whereas prey activity decreased. In contrast to the theory of predator–prey space use, the spatial co-occurrence of predator and prey individuals increased with temperature, while predation rates diminished. We conclude that daily thermal extremes affect trophic interactions in the same way, i.e. through the increased vulnerability of predators, as do long-term shifts in mean environmental temperature. Our results highlight the importance of behavioral studies for understanding mechanisms mediating the effect of extreme thermal events on species interactions.     

Predator hunting mode influences patterns of prey use from grazing and epigeic food webs

Multichannel omnivory by generalist predators, especially the use of both grazing and epigeic prey, has the potential to increase predator abundance and decrease herbivore populations. However, predator use of the epigeic web (soil surface detritus/microbe/algae consumers) varies considerably for reasons that are poorly understood. We therefore used a stable isotope approach to determine whether prey availability and predator hunting style (active hunting vs. passive web-building) impacted the degree of multichannel omnivory by the two most abundant predators on an intertidal salt marsh, both spiders. We found that carbon isotopic values of herbivores remained constant during the growing season, while values for epigeic feeders became dramatically more enriched such that values for the two webs converged in August. Carbon isotopic values for both spider species remained midway between the two webs as values for epigeic feeders shifted, indicating substantial use of prey from both food webs by both spider species. As the season progressed, prey abundance in the grazing food web increased while prey abundance in the epigeic web remained constant or declined. In response, prey consumption by the web-building spider shifted toward the grazing web to a much greater extent than did consumption by the hunting spider, possibly because passive web-capture is more responsive to changes in prey availability. Although both generalist predator species engaged in multichannel omnivory, hunting mode influenced the extent to which these predators used prey from the grazing and epigeic food webs, and could thereby influence the strength of trophic cascades in both food webs.     

Cooperative hunting in a discrete predator–prey system II

ABSTRACT

We investigate a discrete-time predator–prey system with cooperative hunting in the predators proposed by Chow et al. by determining local stability of the interior steady states analytically in certain parameter regimes. The system can have either zero, one or two interior steady states. We provide criteria for the stability of interior steady states when the system has either one or two interior steady states. Numerical examples are presented to confirm our analytical findings. It is concluded that cooperative hunting of the predators can promote predator persistence but may also drive the predator to a sudden extinction.     

Mechanisms of group-hunting in vertebrates

Group-hunting is ubiquitous across animal taxa and has received considerable attention in the context of its functions. By contrast much less is known about the mechanisms by which grouping predators hunt their prey. This is primarily due to a lack of experimental manipulation alongside logistical difficulties quantifying the behaviour of multiple predators at high spatiotemporal resolution as they search, select, and capture wild prey. However, the use of new remote-sensing technologies and a broadening of the focal taxa beyond apex predators provides researchers with a great opportunity to discern accurately how multiple predators hunt together and not just whether doing so provides hunters with a per capita benefit. We incorporate many ideas from collective behaviour and locomotion throughout this review to make testable predictions for future researchers and pay particular attention to the role that computer simulation can play in a feedback loop with empirical data collection. Our review of the literature showed that the breadth of predator:prey size ratios among the taxa that can be considered to hunt as a group is very large (<10⁰ to >10²). We therefore synthesised the literature with respect to these predator:prey ratios and found that they promoted different hunting mechanisms. Additionally, these different hunting mechanisms are also related to particular stages of the hunt (search, selection, capture) and thus we structure our review in accordance with these two factors (stage of the hunt and predator:prey size ratio). We identify several novel group-hunting mechanisms which are largely untested, particularly under field conditions, and we also highlight a range of potential study organisms that are amenable to experimental testing of these mechanisms in connection with tracking technology. We believe that a combination of new hypotheses, study systems and methodological approaches should help push the field of group-hunting in new directions.     

Living and dying in a multi‐predator landscape of fear: roe deer are squeezed by contrasting pattern of predation risk imposed by lynx and humans

The theory of predation risk effects predicts behavioral responses in prey when risk of predation is not homogenous in space and time. Prey species are often faced with a tradeoff between food and safety in situations where food availability and predation risk peak in the same habitat type. Determining the optimal strategy becomes more complex if predators with different hunting mode create contrasting landscapes of risk, but this has rarely been documented in vertebrates. Roe deer in southeastern Norway face predation risk from lynx, as well as hunting by humans. These two predators differ greatly in their hunting methods. The predation risk from lynx, an efficient stalk‐and‐ambush predator is expected to be higher in areas with dense understory vegetation, while predation risk from human hunters is expected to be higher where visual sight lines are longer. Based on field observations and airborne LiDAR data from 71 lynx predation sites, 53 human hunting sites, 132 locations from 15 GPS‐marked roe deer, and 36 roe deer pellet locations from a regional survey, we investigated how predation risk was related to terrain attributes and vegetation classes/structure. As predicted, we found that increasing cover resulted in a contrasting lower predation risk from humans and higher predation risk from lynx. Greater terrain ruggedness increased the predation risk from both predators. Hence, multiple predators may create areas of contrasting risk as well as double risk in the same landscape. Our study highlights the complexity of predator–prey relationship in a multiple predator setting. Synthesis In this study of risk effects in a multi‐predator context, LiDAR data were used to quantify cover in the habitat and relate it to vulnerability to predation in a boreal forest. We found that lynx and human hunters superimpose generally contrasting landscapes of fear on a common prey species, but also identified double‐risk zones. Since the benefit of anti‐predator responses depends on the combined risk from all predators, it is necessary to consider complete predator assemblages to understand the potential for and occurrence of risk effects across study systems.     

Sacrificial males: the potential role of copulation and predation in contributing to copepod sex‐skewed ratios

Predation is thought to play a selective role in the emergence of behavioural traits in prey. Differences in behaviour between prey demographics may, therefore, be driven by predation with select components of the population being less vulnerable to predators. While under controlled conditions prey demography has been shown to have consequences for predation success, investigations linking these implications to natural prey population demographics are scarce. Here we assess predator–prey dynamics between notonectid predators (backswimmers) and Lovenula raynerae (Copepoda), key faunal groups in temperate ephemeral pond ecosystems. Using a combination of field and experimental approaches we test for the development and mechanism of predation‐induced sex‐skewed ratios. A natural population of L. raynerae was tracked over time in relation to their predator (notonectid) and prey (Cladocera) numbers. In the laboratory, L. raynerae sex ratios were also assessed over time but in the absence of predation pressure. Predation success and prey performance experiments evaluating differences between L. raynerae male, female, gravid female and copulating pairs exposed to notonectid predation were then examined. Under natural conditions, a female dominated copepod population developed over time and was correlated to predation pressure, while under predator‐free conditions non sex‐skewed prey population demographics persisted. Predator–prey laboratory trials showed no difference in vulnerability and escape performance for male, female and gravid female copepods, but pairs in copula were significantly more vulnerable to predation. This vulnerability was not shared by both sexes, with only female copepods ultimately escaping from successful predation on a mating pair. These results suggest that contact periods during copula may contribute to the development of sex‐skewed copepod ratios over time in ecosystems dominated by hexapod predators. This is discussed within the context of vertebrate and invertebrate predation and how these dissimilar types of predation are likely to have acted as selective pressures for copepod mating systems.     

Interspecific infanticide deters predators

It is well known that young, small predator stages are vulnerable to predation by conspecifics, intra-guild competitors or hyperpredators. It is less known that prey can also kill vulnerable predator stages that present no danger to the prey. Since adult predators are expected to avoid places where their offspring would run a high predation risk, this opens the way for potential prey to deter dangerous predator stages by killing vulnerable predator stages. We present an example of such a complex predator–prey interaction. We show that (1) the vulnerable stage of an omnivorous arthropod prey discriminates between eggs of a harmless predator species and eggs of a dangerous species, killing more eggs of the latter; (2) prey suffer a minor predation risk from newly hatched predators; (3) adult predators avoid ovipositing near killed predator eggs, and (4) vulnerable prey near killed predator eggs experience an almost fourfold reduction of predation. Hence, by attacking the vulnerable stage of their predator, prey deter adult predators and thus reduce their own predation risk. This provides a novel explanation for the killing of vulnerable stages of predators by prey and adds a new dimension to anti-predator behaviour.     

Hunting‐mediated predator facilitation and superadditive mortality in a European ungulate

Predator‐prey theory predicts that in the presence of multiple types of predators using a common prey, predator facilitation may result as a consequence of contrasting prey defense mechanisms, where reducing the risk from one predator increases the risk from the other. While predator facilitation is well established in natural predator‐prey systems, little attention has been paid to situations where human hunters compete with natural predators for the same prey. Here, we investigate hunting‐mediated predator facilitation in a hunter‐predator‐prey system. We found that hunter avoidance by roe deer (Capreolus capreolus) exposed them to increase predation risk by Eurasian lynx (Lynx lynx). Lynx responded by increasing their activity and predation on deer, providing evidence that superadditive hunting mortality may be occurring through predator facilitation. Our results reveal a new pathway through which human hunters, in their role as top predators, may affect species interactions at lower trophic levels and thus drive ecosystem processes.     

Estimating predation risk in zooplankton communities: the importance of vertical overlap

In order to estimate predation risk in nature, two basic components of predation need to be quantified: prey vulnerability, and density risk. Prey vulnerability can be estimated from clearance rates obtained from enclosure experiments with and without predators. Density risk is a function of predator density, and the spatial and temporal overlap of the predator and prey populations. In the current study we examine the importance of the vertical component of overlap in making accurate estimates of predation risk from the invertebrate predator Mesocyclops edax on rotifer versus crustacean prey. The results indicate that assumptions of uniform predator and prey densities cause a significant underestimation of predation risk for many crustacean prey due to the coincident vertical migration of these prey with the predator. The assumption of uniformity is more reasonable for estimating predation risk for most rotifer prey.     

Sensory-based niche partitioning in a multiple predator–multiple prey community

Many predators and parasites eavesdrop on the communication signals of their prey. Eavesdropping is typically studied as dyadic predator–prey species interactions; yet in nature, most predators target multiple prey species and most prey must evade multiple predator species. The impact of predator communities on prey signal evolution is not well understood. Predators could converge in their preferences for conspicuous signal properties, generating competition among predators and natural selection on particular prey signal features. Alternatively, predator species could vary in their preferences for prey signal properties, resulting in sensory-based niche partitioning of prey resources. In the Neotropics, many substrate-gleaning bats use the mate-attraction songs of male katydids to locate them as prey. We studied mechanisms of niche partitioning in four substrate-gleaning bat species and found they are similar in morphology, echolocation signal design and prey-handling ability, but each species preferred different acoustic features of male song in 12 sympatric katydid species. This divergence in predator preference probably contributes to the coexistence of many substrate-gleaning bat species in the Neotropics, and the substantial diversity in the mate-attraction signals of katydids. Our results provide insight into how multiple eavesdropping predator species might influence prey signal evolution through sensory-based niche partitioning.     

Naïveté in novel ecological interactions: lessons from theory and experimental evidence

The invasion of alien species into areas beyond their native ranges is having profound effects on ecosystems around the world. In particular, novel alien predators are causing rapid extinctions or declines in many native prey species, and these impacts are generally attributed to ecological naïveté or the failure to recognise a novel enemy and respond appropriately due to a lack of experience. Despite a large body of research concerning the recognition of alien predation risk by native prey, the literature lacks an extensive review of naïveté theory that specifically asks how naïveté between novel pairings of alien predators and native prey disrupts our classical understanding of predator–prey ecological theory. Here we critically review both classic and current theory relating to predator–prey interactions between both predators and prey with shared evolutionary histories, and those that are ecologically ‘mismatched’ through the outcomes of biological invasions. The review is structured around the multiple levels of naïveté framework of Banks & Dickman (2007), and concepts and examples are discussed as they relate to each stage in the process from failure to recognise a novel predator (Level 1 naïveté), through to appropriate (Level 2) and effective (Level 3) antipredator responses. We discuss the relative contributions of recognition, cue types and the implied risk of cues used by novel alien and familiar native predators, to the probability that prey will recognise a novel predator. We then cover the antipredator response types available to prey and the factors that predict whether these responses will be appropriate or effective against novel alien and familiar native predators. In general, the level of naïveté of native prey can be predicted by the degree of novelty (in terms of appearance, behaviour or habitat use) of the alien predator compared to native predators with which prey are experienced. Appearance in this sense includes cue types, spatial distribution and implied risk of cues, whilst behaviour and habitat use include hunting modes and the habitat domain of the predator. Finally, we discuss whether the antipredator response can occur without recognition per se, for example in the case of morphological defences, and then consider a potential extension of the multiple levels of naïveté framework. The review concludes with recommendations for the design and execution of naïveté experiments incorporating the key concepts and issues covered here. This review aims to critique and combine classic ideas about predator–prey interactions with current naïveté theory, to further develop the multiple levels of naïveté framework, and to suggest the most fruitful avenues for future research.     

Faced with a choice, sparrowhawks more often attack the more vulnerable prey group

Whether predators always attack the most vulnerable prey or simply attack prey that exceeds a minimum vulnerability level is an important question to answer in furthering our understanding of predator and antipredation behaviour. Predators may attack any reasonably vulnerable prey rather than waste time identifying the most vulnerable prey, particularly when prey can respond quickly to alter their vulnerability in response to a predator. We tested whether sparrowhawks always choose to attack the group of prey that maximises their capture probability, or whether they simply attack any group above a minimum vulnerability. We modelled sparrowhawk attack success when hunting redshanks using data from three winters and found that probability of capture increased when group size or distance to predator-concealing cover decreased. We then used this model to predict the relative vulnerability to capture of redshank groups occurring in pairs in a fourth winter and found that sparrowhawks attacked the most vulnerable prey group twice as often as not (66% n=59 pairs). When sparrowhawks attacked the less vulnerable group, there was no tendency for both groups to be particularly vulnerable or for the difference in the vulnerability between the two groups to be relatively small. This suggests that, while sparrowhawks do on average attack the most vulnerable group available, they consider other factors that affect vulnerability or that additional factors lead them to also attack opportunistically. This suggests that there will be selection for the predator to monitor a large number of prey individuals and groups and for prey to have the ability to monitor the behaviour of conspecifics in the same and different groups so that they can assess relative vulnerability.     

The dynamics of prey choice in fish: the importance of prey size and satiation

Over a number of decades the process of prey choice has been investigated using fishes as model predators. Using fishes for the model has allowed the proximate factors that determine how a mobile predator finds and chooses to eat the prey encountered within a variable 3‐D environment to be estimated. During prey choice a number of constraints exist, in particular most fish predators will eat their prey whole thus their jaws and gut create functional limitations once a prey has been attacked. By considering the relationship between the size of the prey and the predator's feeding apparatus and feeding motivation this study explores the link between mechanistic studies and theoretical, optimal foraging based predictions. How the prediction of prey choices made by the fish following prey encounter can be reconciled with what is likely to be found in the fish's stomach is discussed. This study uses a progression of empirical examples to illustrate how the limits of functional constraints and prey choice at different stages of motivation to feed can be taken into account to improve predictions of predator prey choice.     

Managing predators: The influence of kangaroo rat antipredator displays on sidewinder rattlesnake hunting behavior

Upon sensing predators in their vicinity, many prey species perform antipredator displays that are thought to provide information to the predator that deters it from attacking (predator‐deterrent signals). These displays can be complex, incorporating a variety of signaling elements as well as direct physical harassment of the predator. Although the display behaviors in these communication systems are often well characterized, evidence of the efficacy of these displays in deterring predators is limited due to the challenges associated with studying free‐ranging predators. Here, we examine how the anti‐snake signals of the desert kangaroo rat (Dipodomys deserti) influence the ambush hunting behaviors of sidewinder rattlesnakes (Crotalus cerastes). We found that, although desert kangaroo rats incorporate a number of signal elements into their antipredator display, only sand kicking behavior was a significant factor in motivating sidewinder rattlesnakes to cease hunting: high rates of sand kicking led to early abandonment of ambush coils. These results indicate that anti‐snake displays of small mammals may be especially effective at mitigating the threat posed by rattlesnakes when those displays incorporate physical harassment as well as signaling.