The rules of engagement: how to defend against combinations of predators

Studies of inducible defenses have traditionally examined prey responses to one predator at a time. However, prey in nature encounter combinations of predators that should force them to produce phenotypic compromises. We examined how snails (Helisoma trivolvis) alter their phenotype in the presence of three different predator species that were presented alone and in pairwise combinations. When snails were exposed to each predator alone, they formed predator-specific defenses that reflected the differences in each predator’s foraging mode. When snails were exposed to pairwise combinations of predators, their phenotype was dependent on their ability to detect each predator, the risk posed by each predator, and the effectiveness of a given defense against each predator. Consequently, responses to combined predators were typically biased towards one of the predators in the pair. This suggests that prey facing combined predators do not form simple intermediate defenses and, as a result, may experience enhanced mortality risk when they encounter natural predator regimes.     

COEVOLUTION OF PHENOTYPIC PLASTICITY IN PREDATOR AND PREY: WHY ARE INDUCIBLE OFFENSES RARER THAN INDUCIBLE DEFENSES?

Inducible defenses of prey and inducible offenses of predators are drastic phenotypic changes activated by the interaction between a prey and predator. Inducible defenses occur in many taxa and occur more frequently than inducible offenses. Recent empirical studies have reported reciprocal phenotypic changes in both predator and prey. Here, we model the coevolution of inducible plasticity in both prey and predator, and examine how the evolutionary dynamics of inducible plasticity affect the population dynamics of a predator-prey system. Under a broad range of parameter values, the proportion of predators with an offensive phenotype is smaller than the proportion of prey with a defensive phenotype, and the offense level is relatively lower than the defense level at evolutionary end points. Our model also predicts that inducible plasticity evolves in both species when predation success depends sensitively on the difference in the inducible trait value between the two species. Reciprocal phenotypic plasticity may be widespread in nature but may have been overlooked by field studies because offensive phenotypes are rare and inconspicuous.     

Predators as drivers of insect defenses

Insects have evolved various types of antipredator defenses. For example, many insects have evolved crypsis, and exhibit cryptic body colors and shapes for hiding from predators. Other insects produce toxins as a form of chemical defense against predators, and some toxic insects are aposematic, with conspicuous body colors for advertising their toxins. Insects can also develop hairs, spines or hard exoskeletons as morphological defenses to protect themselves from predation. In addition, insects can evolve behavioral defenses, in which insects exhibit autotomy or dropping, or feign death. This study investigated which predator types evoke these types of defenses, through a review of the effectiveness of antipredator defenses in insects against carnivorous animals that are commonly used as model predators in studies. These predators include other insects, spiders, fish, frogs, lizards, birds and mammals. The results provide the first step for clarifying the evolutionary drivers of antipredator defenses in insects. The following aspects should be considered for future studies: multiple predator species and sufficient replication, alternative prey and predator models, and tolerance to predators in insects.     

The influence of vigilance on intraguild predation

Theoretical work on intraguild predation suggests that if a top predator and an intermediate predator share prey, the system will be stable only if the intermediate predator is better at exploiting the prey, and the top predator gains significantly from consuming the intermediate predator. In mammalian carnivore systems, however, there are examples of top predator species that attack intermediate predator species, but rarely or never consume the intermediate predator. We suggest that top predators attacking intermediate predators without consuming them may not only reduce competition with the intermediate predators, but may also increase the vigilance of the intermediate predators or alter the vigilance of their shared prey, and that this behavioral response may help to maintain the stability of the system. We examine two models of intraguild predation, one that incorporates prey vigilance, and a second that incorporates intermediate predator vigilance. We find that stable coexistence can occur when the top predator has a very low consumption rate on the intermediate predator, as long as the attack rate on the intermediate predator is relatively large. However, the system is stable when the top predator never consumes the intermediate predator only if the two predators share more than one prey species. If the predators do share two prey species, and those prey are vigilant, increasing top predator attack rates on the intermediate predator reduces competition with the intermediate predator and reduces vigilance by the prey, thereby leading to higher top predator densities. These results suggest that predator and prey behavior may play an important dynamical role in systems with intraguild predation.     

Prey and predator density‐dependent interactions under different water volumes

Predation is a critical ecological process that directly and indirectly mediates population stabilities, as well as ecosystem structure and function. The strength of interactions between predators and prey may be mediated by multiple density dependences concerning numbers of predators and prey. In temporary wetland ecosystems in particular, fluctuating water volumes may alter predation rates through differing search space and prey encounter rates. Using a functional response approach, we examined the influence of predator and prey densities on interaction strengths of the temporary pond specialist copepod Lovenula raynerae preying on cladoceran prey, Daphnia pulex, under contrasting water volumes. Further, using a population dynamic modeling approach, we quantified multiple predator effects across differences in prey density and water volume. Predators exhibited type II functional responses under both water volumes, with significant antagonistic multiple predator effects (i.e., antagonisms) exhibited overall. The strengths of antagonistic interactions were, however, enhanced under reduced water volumes and at intermediate prey densities. These findings indicate important biotic and abiotic contexts that mediate predator–prey dynamics, whereby multiple predator effects are contingent on both prey density and search area characteristics. In particular, reduced search areas (i.e., water volumes) under intermediate prey densities could enhance antagonisms by heightening predator–predator interference effects.     

Opportunistic predator prefers habitat complexity that exposes prey while reducing cannibalism and intraguild encounters

Structural features of habitat are known to affect the density of predators and prey, and it is generally accepted that complexity provides some protection from the environment and predators but may also reduce foraging success. A next step in understanding these interactions is to decouple the impacts of both spatial and trophic ingredients of complexity to explicitly explore the trade-offs between the habitat, its effects on foraging success, and the competition that ensues as predator densities increase. We quantified the accumulation of spiders and their prey in habitat islands with different habitat complexities created in the field using natural plants, plant debris and plastic plant mimics. Spiders were observed at higher densities in the complex habitat structure composed of both live plants and thatch. However, the numerically dominant predator in the system, the wolf spider Pardosa milvina, was observed at high densities in habitat islands containing plastic mimics of plants and thatch. In a laboratory experiment, we examined the interactive effects of conspecific density and habitat on the prey capture of P. milvina. Thatch, with or without vertical plant structure, reduced prey capture, but the plastic fiber did not. Pairwise interactions among spiders reduced prey capture, but this effect was moderated by thatch. Taken together, these experiments highlight the flexibility of one important predator in the food web, where multiple environmental cues intersect to explain the role of habitat complexity in determining generalist predator accumulation.     

Cue reliability, risk sensitivity and inducible morphological defense in a marine snail

Reliable cues that communicate current or future environmental conditions are a requirement for the evolution of adaptive phenotypic plasticity, yet we often do not know which cues are responsible for the induction of particular plastic phenotypes. I examined the single and combined effects of cues from damaged prey and predator cues on the induction of plastic shell defenses and somatic growth in the marine snail Nucella lamellosa. Snails were exposed to chemical risk cues from a factorial combination of damaged prey presented in isolation or consumed by predatory crabs (Cancer productus). Water-borne cues from damaged conspecific and heterospecific snails did not affect plastic shell defenses (shell mass, shell thickness and apertural teeth) or somatic growth in N. lamellosa. Cues released by feeding crabs, independent of prey cue, had significant effects on shell mass and somatic growth, but only crabs consuming conspecific snails induced the full suite of plastic shell defenses in N. lamellosa and induced the greatest response in all shell traits and somatic growth. Thus the relationship between risk cue and inducible morphological defense is dependent on which cues and which morphological traits are examined. Results indicate that cues from damaged conspecifics alone do not trigger a response, but, in combination with predator cues, act to signal predation risk and trigger inducible defenses in this species. This ability to “label” predators as dangerous may decrease predator avoidance costs and highlights the importance of the feeding habits of predators on the expression of inducible defenses.     

Experimental evolution of a microbial predator's ability to find prey

Foraging theory seeks to explain how the distribution and abundance of prey influence the evolution of predatory behaviour, including the allocation of effort to searching for prey and handling them after they are found. While experiments have shown that many predators alter their behaviour phenotypically within individual lifetimes, few have examined the actual evolution of predatory behaviour in light of this theory. Here, we test the effects of prey density on the evolution of a predator's searching and handling behaviours using a bacterial predator, Myxococcus xanthus. Sixteen predator populations evolved for almost a year on agar surfaces containing patches of Escherichia coli prey at low or high density. Improvements in searching rate were significantly greater in those predators that evolved at low prey density. Handling performance also improved in some predator populations, but prey density did not significantly affect the magnitude of these gains. As the predators evolved greater foraging proficiency, their capacity diminished to produce fruiting bodies that enable them to survive prolonged periods of starvation. More generally, these results demonstrate that predators evolve behaviours that reflect at least some of the opportunities and limitations imposed by the distribution and abundance of their prey.     

Interactions between adult and larval bluegill sunfish: positive and negative effects

Adult fish may affect the growth and survival of conspecific larvae through a variety of pathways, including negative interactions via competition for shared limiting resources or via predation (i.e., cannibalism), and positive interactions due to the consumption of larval predators and via resource enhancement (i.e., presence of adults increases availability of larval prey). To examine the overall effect of adult bluegill sunfish (Lepomis macrochirus) on larval bluegill, we conducted a field experiment in which we manipulated adult densities and quantified larval growth and survival, prey abundance, invertebrate predator abundance, and cannibalism. The presence of adult bluegill had a negative effect on final larval mass. This response was consistent with competition for zooplankton prey. Adult bluegill reduced the abundance of large zooplankton (e.g., Chaoborus and Daphnia), which were the dominant prey of bluegill larvae in the absence of adults. Larvae in the no-adult treatment also had significantly more prey in their stomachs compared to larvae in the presence of adults. Larval survival was maximized at intermediate adult densities and the overall production of larvae peaked at intermediate adult densities. The higher larval survival at intermediate adult densities is attributed to a reduction in invertebrate predators in treatments with adult bluegill; invertebrate predators experienced an 80% reduction in the presence of adult fish. Decreased larval survival at the highest adult density was not due to resource limitation and may be due to cannibalism, which was not directly observed in our study, but has been observed in other studies.     

Poor phenotypic integration of blue mussel inducible defenses in environments with multiple predators

Aquatic prey encounter an array of threat cues from multiple predators and killed conspecifics, yet the vast majority of induced defenses are investigated using cues from single predator species. In most cases, it is unclear if odors from multiple predators will disrupt defenses observed in single-predator induction experiments. We experimentally compared the inducible defenses of the common marine mussel Mytilus edulis to waterborne odor from pairwise combinations of three predators representing two attack strategies. Predators included the sea star, Asterias vulgaris (= Asterias rubens ), and the crabs Carcinus maenas and Cancer irroratus . The mussels increased adductor muscle mass in response to cues from unfed Asterias (a predatory seastar that pulls mussel shells open) and increased shell thickness in response to unfed Carcinus, a predatory crab that crushes or peels shells. However, the mussels did not express either predator specific response when exposed to the combined cues of Asterias and Carcinus , and mussels did not increase shell thickness when exposed to cues from Cancer alone or any pairwise combination of the three predators. Shell closure or 'clamming up' did not occur in response to any predator combination. These results suggest that predator-specific responses to the Asterias and Carcinus are poorly integrated and cannot be expressed simultaneously. Simultaneous cues from multiple predators affect the integration of predator specific defenses and predator odors from functionally similar predators do not necessarily initiate similar defenses. Ultimately, the degree that prey can integrate potentially disparate defenses in a multiple predator environment may have ecological ramifications and represent a seldom explored facet of the evolution of inducible defenses.     

Density-dependent effects of prey defences

In this study, we show that the protective advantage of a defence depends on prey density. For our investigations, we used the predator-prey model system Chaoborus-Daphnia pulex. The prey, D. pulex, forms neckteeth as an inducible defence against chaoborid predators. This morphological response effectively reduces predator attack efficiency, i.e. number of successful attacks divided by total number of attacks. We found that neckteeth-defended prey suffered a distinctly lower predation rate (prey uptake per unit time) at low prey densities. The advantage of this defence decreased with increasing prey density. We expect this pattern to be general when a defence reduces predator success rate, i.e. when a defence reduces encounter rate, probability of detection, probability of attack, or efficiency of attack. In addition, we experimentally simulated the effects of defences which increase predator digestion time by using different sizes of Daphnia with equal vulnerabilities. This type of defence had opposite density-dependent effects: here, the relative advantage of defended prey increased with prey density. We expect this pattern to be general for defences which increase predator handling time, i.e. defences which increase attacking time, eating time, or digestion time. Many defences will have effects on both predator success rate and handling time. For these defences, the predator’s functional response should be decreased over the whole range of prey densities. Received: 15 September 1999 / Accepted: 23 December 1999     

Evolutionary consequences of a search image

Many predators are able to become better at spotting cryptic prey by recognising specific clues, but by concentrating on one prey type they will become worse at spotting other prey types. This phenomenon is known as the formation of a search image for a certain prey by a predator and is related to apostatic selection. Here, we study the evolution of a search image in the predator by formulating and analysing a mathematical model. The predator forages for two prey types and is able to form an independent search image for both prey. The results show that the evolutionary dynamics can be divided into two parts: a fast and a slow part. At first selection pressure will be strong towards a stable ratio of prey, which is the same as the ratio found for the unbeatable prey choice for predators with a Holling type II functional response. Following this, the slow dynamics will keep this ratio constant independent of the trait values, but the predator will slowly evolve towards a stronger search image and ultimately become a specialist predator or slowly evolve towards generalist with a weak search image. In conclusion, the formation of a search image causes the predator to control the prey densities such that the ratio of available prey is kept constant by the predator.     

Algal defenses,population stability,and the risk of herbivore extinctions: a chemostat model and experiment

The effects of inducible defenses and constitutive defenses on population dynamics were investigated in a freshwater plankton system with rotifers as predators and different algal strains as prey. We made predictions for these systems using a chemostat predator–prey model and focused on population stability and predator persistence as a function of flow-through rate. The model exhibits three major types of behavior at a high nutrient concentration: (1) at high dilution rates, only algae exist; (2) at intermediate dilution rates, algae and rotifers show stable coexistence; (3) at low dilution rates, large population fluctuations occur, with low minimum densities entailing a risk of stochastic rotifer extinctions. The size and location of the corresponding areas in parameter space critically depend on the type of algal defense strategy. In an 83-day high-nutrient chemostat experiment we changed the dilution rate every 3 weeks, from 0.7 to 0.5 to 0.3 to 0.1 per day. Within this range of dilution rates, rotifers and algae coexisted, and population fluctuations of algae clearly increased as dilution rates decreased. The CV of herbivore densities was highest at the end of the experiment, when the dilution rate was low. On day 80, herbivorous rotifers had become undetectable in all three chemostats with permanently defended algae (where rotifer densities had already been low) and in two out of three chemostats where rotifers had been feeding on algae with inducible defenses (that represented more edible food). We interpret our results in relation to the paradox of enrichment.     

Influence of cruising and ambush predators on 3-dimensional habitat use in age 0 juvenile Atlantic cod Gadus morhua

Predators and prey often co-exist at high densities within the same habitat, yet the behavioural and spatial dynamics underlying this co-existence are not well known. To better understand small-scale, predator-prey co-occurrence, the spatial patterns and behaviour of age 0 juvenile cod Gadus morhua 75-88 mm SL and two of their known predators, age 2+ cod and short-horn sculpin Myoxocephalus scorpinus, were examined in two habitats (i.e., sand and eelgrass) using three-dimensional video analysis. Both habitat and predator type interacted to result in unique spatial patterns of prey. Spatial overlap between predators and prey was highest in open habitat in the presence of the cruising predator but lowest in the presence of sculpin in the same habitat. In eelgrass, age 0 cod avoided predators primarily along the vertical axis (i.e., distance off bottom). Age 0 cod stayed above eelgrass in the presence of sculpin but lowered themselves into the eelgrass while in the presence of predator cod. Anti-predator behaviour (i.e., predator-prey distance, prey cohesion and freezing) was significantly reduced over eelgrass compared to sand, suggesting eelgrass has lower ‘inherent risk’ than open habitats. However, predator consumption was similar across all treatments, suggesting that, 1) complex habitat also impairs the visual cues needed for anti-predator behaviour (e.g., schooling) and assessing the location of predators, and 2) predators change their behaviour with habitat to enhance their opportunities for finding and capturing prey.     

Mixed encounters, limited perception and optimal foraging

This article demonstrates how perceptual constraints of predators and the possibility that predators encounter prey both sequentially (one prey type at a time) and simultaneously (two or more prey types at a time) may influence the predator attack decisions, diet composition and functional response of a behavioural predator-prey system. Individuals of a predator species are assumed to forage optimally on two prey types and to have exact knowledge of prey population numbers (or densities) only in a neighbourhood of their actual spatial location. The system characteristics are inspected by means of a discrete-time, discrete-space, individual-based model of the one-predator-two-prey interaction. Model predictions are compared with ones that have been obtained by assuming only sequential encounters of predators with prey and/or omniscient predators aware of prey population densities in the whole environment. It is shown that the zero-one prey choice rule, optimal for sequential encounters and omniscient predators, shifts to abruptly changing partial preferences for both prey types in the case of omniscient predators faced with both types of prey encounters. The latter, in turn, become gradually changing partial preferences when predator omniscience is considered only local.     

Effects of prey availability, facultative plant feeding, and plant defenses on a generalist insect predator

This study examined the effects of feeding interval, access to host plants (thus, a source of sap), and plant defenses on the predatory insect, Podisus maculiventris Say (Hemiptera: Pentatomidae). The experiment consisted of a 2 × 2 design with two feeding intervals (1 day or 5 days) and predators living on either tomato plants or plastic plants. Females fed every day had greater body weights and egg hatch rates than females fed every five days. Females on tomato plants lived longer than females on plastic plants. However, access to plants did not alleviate the effects of low prey level on predator weight or reproductive output. In a second experiment, third instar nymphs were placed on either tomato plants or plastic plants for four days to examine the effects of tomato trichome defenses on these predators. Nymphs on tomato plants experienced 50% mortality compared to 15% mortality for nymphs on plastic plants. Some nymphs living on tomato plants were trapped by the hairy trichomes of the plant; others had gummed up legs from the exudates of the plants’ glandular trichomes, which inhibited their movement and ability to feed on prey. Although predators appeared to benefit from feeding on tomato plants, their ability to live on the plants was negatively affected by the defensive features of the plants. The potential effects of trichome defenses on predator survival and population dynamics must be considered when evaluating the benefits of plants on insect predator life histories and efficacy as biological control agents.     

Predator induced phenotypic plasticity in the pinewoods tree frog,<Emphasis Type="Italic"> Hyla femoralis</Emphasis>: necessary cues and the cost of development

Predator-induced defenses can result from non-contact cues associated with the presence of a feeding predator; however, the nature of the predator cue has not been determined. We tested the role of two non-contact cues, metabolites of digestion of conspecific prey released by the predator and alarm pheromones released by attacked conspecific prey, in the development of inducible defenses by exposing pinewoods tree frog (Hyla femoralis) tadpoles to non-lethal dragonfly (Anax junius) larvae fed either inside experimental bins or removed from the bins for feeding to eliminate alarm pheromones. The costs associated with the development of the induced morphology were also investigated by providing the tadpoles with two food levels intended to provide adequate or growth limiting resources. The generalized morphological response of H. femoralis tadpoles to predators included the development of bodies and tails that were both deeper and shorter, smaller overall body size, and increased orange tail fin coloration and black tail outline. Metabolites of digestion were sufficient to initiate development of inducible defenses; however, the combination of metabolites and alarm cue resulted in a greater response. Furthermore, growth and development were slowed in tadpoles that expressed the induced morphology; however, this growth cost was insufficient to preclude the development of the induced morphology when food resources were low. These results indicate that two aspects of the indirect predator cue work together to trigger a morphological anti-predator response.     

The long‐term impacts of predators on prey: inducible defenses,population dynamics,and indirect effects

Despite the amount of research on the inducible defenses of prey against predators, our understanding of the long‐term significance of non‐lethal predators on prey phenotypes, prey population dynamics, and community structure has rarely been explored. Our objectives were to assess the effects of predators on prey defenses, prey population dynamics, and the relative magnitude of density‐ versus trait‐mediated indirect interactions (DMIIs and TMIIs) over multiple prey generations. Using a freshwater snail and three common snail predators, we constructed a series of community treatments with pond mesocosms that manipulated trophic structure, the identity of the top predator, and whether predators were caged or uncaged. We quantified snail phenotypes, snail population size, and resource abundance over multiple snail generations. We found that snails were expressing inducible defenses in our system although the magnitude of the responses varied over time and across predator species. Despite the expression of inducible defenses, caged predators did not reduce snail population size. There also was no evidence of TMIIs throughout the experiment suggesting that TMIIs have a minimal role in the long‐term structure of our communities. The absence of TMIIs was largely driven by the lack of predator‐induced reductions in resource consumption and the lack of consistent reductions in population size with predator cues. In contrast, we detected strong DMIIs associated with lethal predators suggesting that DMIIs are the dominant long‐term mechanism influencing community structure. Our results demonstrate that although predators can have significant effects on prey phenotypes and sometimes cause short‐term TMIIs, there may be few long‐term consequences of these responses on population dynamics and indirect interactions, at least within simple food webs. Research directed towards addressing the long‐term consequences of predator–prey interactions within communities will help to reveal whether the conclusions and predictions generated from short‐term experiments are applicable over ecological and evolutionary timescales.     

The optimal sampling strategy for unfamiliar prey

Precisely how predators solve the problem of sampling unfamiliar prey types is central to our understanding of the evolution of a variety of antipredator defenses, ranging from Müllerian mimicry to polymorphism. When predators encounter a novel prey item then they must decide whether to take a risk and attack it, thereby gaining a potential meal and valuable information, or avoid such prey altogether. Moreover, if predators initially attack the unfamiliar prey, then at some point(s) they should decide to cease sampling if evidence mounts that the type is on average unprofitable to attack. Here, I cast this problem as a "two-armed bandit," the standard metaphor for exploration-exploitation trade-offs. I assume that as predators encounter and attack unfamiliar prey they use Bayesian inference to update both their beliefs as to the likelihood that individuals of this type are chemically defended, and the probability of seeing the prey type in the future. I concurrently use dynamic programming to identify the critical informational states at which predator should cease sampling. The model explains why predators sample more unprofitable prey before complete rejection when the prey type is common and explains why predators exhibit neophobia when the unfamiliar prey type is perceived to be rare.     

Predator avoidance behavior in the pea aphid: costs,frequency, and population consequences

Induced prey defenses can be costly. These costs have the potential to reduce prey survival or reproduction and, therefore, prey population growth. I estimated the potential for predators to suppress populations of pea aphids (Acyrthosiphon pisum) in alfalfa fields through the induction of pea aphid predator avoidance behavior. I quantified (1) the period of non-feeding activity that follows a disturbance event, (2) the effect of frequent disturbance on aphid reproduction, and (3) the frequency at which aphids are disturbed by predators. In combination, these three values predict that the disturbances induced by predators can substantially reduce aphid population growth. This result stems from the high frequency of predator-induced disturbance, and the observation that even brief disturbances reduce aphid reproduction. The potential for predators to suppress prey populations through induction of prey defenses may be strongest in systems where (1) predators frequently induce prey defensive responses, and (2) prey defenses incur acute survival or reproductive costs. Electronic supplementary material Supplementary material is available in the online version of this article at and is accessible for authorized users.