Separating the effects of prey size and speed on the kinematics of prey capture in the omnivorous lizard Gerrhosaurus major

Feeding behavior is known to be modulated as prey properties change. During prey capture, external prey properties, including size and mobility, are likely some of the most important components in predator–prey interactions. Whereas prey size has been demonstrated to elicit modulation of jaw movements during capture, how prey speed affects the approach and capture of prey remains unknown. We quantified the kinematics associated with movements of both the feeding and locomotor systems during prey capture in a lizard, Gerrhosaurus major, while facing prey differing in size and mobility (newborn mice, grasshoppers, and mealworms). Our data show that the feeding and locomotor systems were recruited differently in response to changes in the size or speed of the prey. The timing of jaw movements and of the positioning of the head are affected by changes in prey size—and speed, to a lesser extent. Changes in prey speed resulted in concomitant changes in the speed of strike and an early and greater elevation of the neck. External prey properties, and prey mobility in particular, are relevant in predator–prey interactions and elicit specific responses in different functional systems.     

The consequences of partially directed search effort

Search effort is undirected when a forager has a stereotypical searching behaviour that results in fixed encounter rates with its prey (e.g. diet choice models), and is directed when the forager can bias its encounter with a ‘chosen’ prey. If the bias is complete, search is totally directed (e.g. habitat selection models). When the bias is incomplete (i.e. search modes are not exclusive to a single prey type), search is partially directed. The inclusion of a prey type in the diet is then the result of two decisions: (1) which prey to search for and (2) which prey to handle. The latter decision is determined by the ratio of energy to handling time and the abundance of the preferred prey. The former decision is a function of the encounter probabilities and densities of all potential prey types in addition to their ratio of energy to handling time. Assuming two prey types, there are three distinct behavioural strategies: (1) search for the preferred prey/forage selectively; (2) search for the preferred prey/forage opportunistically; and (3) search for the non-preferred prey/forage opportunistically. If prey are depletable (i.e. prey occur in resource patches), the forager may switch search modes such that prey are depleted to the point where the marginal values of the search modes are equalized. This revised version was published online in July 2006 with corrections to the Cover Date.     

Should "handled" prey be considered? Some consequences for functional response, predator-prey dynamics and optimal foraging theory

Predator-prey models consider those prey that are free. They assume that once a prey is captured by a predator it leaves the system. A question arises whether in predator-prey population models the variable describing prey population shall consider only those prey which are free, or both free and handled prey together. In the latter case prey leave the system after they have been handled. The classical Holling type II functional response was derived with respect to free prey. In this article we derive a functional response with respect to prey density which considers also handled prey. This functional response depends on predator density, i.e., it accounts naturally for interference. We study consequences of this functional response for stability of a simple predator-prey model and for optimal foraging theory. We show that, qualitatively, the population dynamics are similar regardless of whether we consider only free or free and handled prey. However, the latter case may change predictions in some other cases. We document this for optimal foraging theory where the functional response which considers both free and handled prey leads to partial preferences which are not observed when only free prey are considered.     

The oddity effect drives prey choice but not necessarily attack time

The tendency of predators to preferentially attack phenotypically odd prey in groups (the oddity effect) is a clear example of how predator cognition can impact behaviour and morphology in prey. Through targeting phenotypically odd prey, predators are thought to avoid the cognitive constraints that delay and limit the success of attacks on homogenous prey groups (the confusion effect). In addition to influencing which prey a predator will attack, the confusion and oddity effects would also predict that attacks on odd prey can occur more rapidly than attacking the majority prey type, as odd prey are more easily targeted, but this prediction has yet to be tested. Here, we used kerri tetra fish, Inpaichthys kerri, presented with mixed phenotypic groups of Daphnia dyed red or black to investigate whether odd prey in groups are preferentially attacked and whether these attacks were faster than those on the majority prey type. In agreement with previous work, odd prey were targeted and attacked more often than expected from their frequency in the prey groups, regardless of whether the odd prey was red in a group of black prey or vice versa. However, no difference was found in the time taken to attack odd vs. majority prey items, contrary to our predictions. Our results suggest that the time taken to make an attack is determined by a wider range of factors or is subject to greater variance than the choice of which prey is selectively targeted in a group.     

Foraging performance of diet-induced morphotypes in pumpkinseed sunfish (Lepomis gibbosus) favours resource polymorphism

Morphological plasticity can influence adaptive divergence when it affects fitness components such as foraging performance. We induced morphological variation in pumpkinseed sunfish (Lepomis gibbosus) ecomorphs and tested for effects on foraging performance. Young-of-year pumpkinseed sunfish from littoral and pelagic lake habitats were reared each on a 'specialist diet' representing their native habitat-specific prey, or a 'generalist diet' reflecting a combination of native and non-native prey. Specialist and generalist diets, respectively, induced divergent and intermediate body forms. Specialists had the highest capture success on their native prey whereas generalist forms were inferior. Specialists faced trade-offs across prey types. However, pelagic specialists also had the highest intake rate on both prey types suggesting that foraging trade-offs are relaxed when prey are abundant. This increases the likelihood of a resource polymorphism because the specialized pelagic form can be favoured by directional selection when prey are abundant and by diversifying selection when prey resources are restricted.     

Flexibility in assessment of prey cues: frog-eating bats and frog calls

Predators use cues associated with their prey to assess prey quality and to avoid consuming poisonous prey. Considerable attention has been given to predators' use of aposematic cues to assess prey quality, but little is known about predators that eavesdrop on prey cues that are not intended for them. Here we investigate the prey-cue/prey-quality associations of a predator that eavesdrops on the sexual advertisement signals of its prey. Stability is expected in prey-cue/prey-quality associations when mistakes in prey assessment are lethal. Conversely, flexibility is possible when mistakes are less costly. Predators that must respond to temporal and spatial fluctuations in prey availability should be more flexible in their assessment of prey quality. Given these predictions, we examined flexibility in the ability of wild-caught bats to reverse prey-cue/prey-quality associations for a preferred prey and a poisonous one. We found that the predatory bat, Trachops cirrhosus, has a heretofore undescribed ability to reverse its evaluations of the cues that signal preferred prey.     

Central assumptions of predator-prey models fail in a semi-natural experimental system

The relationship between the encounter rate of predators with prey and the density of this prey is fundamental to models of predator-prey interactions. The relationship determines, among other variables, the rate at which prey patches are depleted, and hence the impact of predator populations on their prey, and the optimal spatial distribution of foraging effort. Two central assumptions that are made in many models are that encounter rate is directly proportional to prey density and that it is independent of the proportion of prey already removed, other than via the decreased density. We show here, using captive great tits searching for winter moth caterpillars in their natural hiding positions, that neither of these assumptions hold. Encounter rate increased less than directly in proportion to prey density, and it depended not only on the current density of prey, but also on the proportion of prey already removed by previous foragers. Both of these effects are likely to have major consequences for the outcome of predator-prey interactions.     

Responses by a generalist predator,the Balearic lizard <Emphasis Type="Italic">Podarcis lilfordi</Emphasis>, to chemical cues from taxonomically diverse prey

Specialist predators may respond strongly to sensory cues from preferred prey, but responses by generalist predators, although predicted to be less specific, are poorly known. Among squamate reptiles, diet and strength of response to chemical prey cues covary geographically in snakes that are specialist predators. There have been no previous studies of correspondence between diet and chemosensory response in lizards that are prey generalists. Actively foraging lizards discriminate between prey chemicals and control substances. It has been speculated that differential responses among prey species are unlikely in typical species that are dietary generalists. We examined this relationship in Podarcis lilfordi, an omnivorous lacertid that consumes a wide variety of animal prey. In experiments in which chemical stimuli were presented on cotton swabs, lizards responded more strongly to chemicals from a broad spectrum of prey types than to deionized water, an odorless control. These findings plus previous data showing that P. lilfordi is capable of prey chemical discrimination suggest that P. lilfordi can identify a wide range of potential prey using chemical cues. However, there was no evidence of differential response to stimuli among prey species, even in comparisons of prey included in the natural diet and potential prey not in the diet. The results, although limited to a single species, are consistent with the hypothesis that lizard species that are prey generalists do not exhibit the differential response strengths to chemical prey cues observed in snakes that have more specialized diets. Received in revised form: 17 July 2001 Electronic Publication     

Intraspecific variation in prey quality: a comparison of nutrient presence in prey and nutrient extraction by predators

Prey quality can have large impacts on the survival, growth and behavior of predators. A number of studies have examined how different species of prey vary in quality. However, far less is known about intraspecific variation in the quality of prey for predators and even less about what nutrients are extracted from prey by predators. We examined how the sex, feeding level and developmental status of prey affected the quantities of nutrients present in prey bodies and the quantities of nutrients that could be extracted from prey by spiders. Female and well‐fed prey were larger and had more nutrients than male and food‐limited prey, respectively. After taking into account differences in prey size, spiders extracted relatively more lipid and less protein from female and well‐fed prey than from male and food‐limited prey, respectively. Mealworms were of higher quality than adult mealworm beetles; spiders were able to extract more lipid, protein and other nutrients from larvae than adults. While lipid present in prey was a good predictor of lipid consumed, protein present in prey was not a reliable predictor of protein consumed. The variation in prey quality that we observed within a single species of prey (i.e. well‐fed vs food‐limited crickets) was as large as variation in quality among the three species of prey used in these experiments. Intraspecific variation in prey quality may be an important factor affecting predatory arthropods, especially in habitats or at times of year when one species of prey is abundant. Further studies are needed to examine the consequences of intraspecific variation in prey quality on the life history and behavior of predators.     

Population dynamical consequences of reduced predator switching at low total prey densities

Several models of rapid switching by a predator in a two-prey environment are analyzed. The goal is to determine how the dynamics of the system and the potential indirect effects between prey are affected by the dependence of switching on total prey density. In exploring this question, the difference between the population-level consequences of switching in stable and cycling predator-prey systems is also examined. We concentrate on reduced switching at low densities, a feature that is likely because of the difficulty of distinguishing between two very low densities. The main findings are: (1) switching in unstable systems can produce positive indirect effects of one prey species on the other; and (2) reduced switching at low densities can greatly alter the dynamics of the system and the indirect effects between prey. Both of the possibilities are only evident in cycling systems. Reduced switching at low total prey densities leads to heavier predation on the slower-growing prey when both prey species are rare. As a consequence, there is a lag in the recovery of the slower-growing prey species after predator densities fall, and the dynamics of the two prey become desynchronized. The net result is increased indirect interactions between prey, and a greater likelihood of exclusion of the slower growing prey. The analysis of these models suggests a need for more empirical work to determine whether switching is reduced by very low total prey densities, and to study the long-term dynamics that occur in systems with switching predators.     

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.     

Prey Responses to Predator Chemical Cues: Disentangling the Importance of the Number and Biomass of Prey Consumed

To effectively balance investment in predator defenses versus other traits, organisms must accurately assess predation risk. Chemical cues caused by predation events are indicators of risk for prey in a wide variety of systems, but the relationship between how prey perceive risk in relation to the amount of prey consumed by predators is poorly understood. While per capita predation rate is often used as the metric of relative risk, studies aimed at quantifying predator-induced defenses commonly control biomass of prey consumed as the metric of risk. However, biomass consumed can change by altering either the number or size of prey consumed. In this study we determine whether phenotypic plasticity to predator chemical cues depends upon prey biomass consumed, prey number consumed, or both. We examine the growth response of red-eyed treefrog tadpoles (Agalychnis callidryas) to cues from a larval dragonfly (Anax amazili). Biomass consumed was manipulated by either increasing the number of prey while holding individual prey size constant, or by holding the number of prey constant and varying individual prey size. We address two questions. (i) Do prey reduce growth rate in response to chemical cues in a dose dependent manner? (ii) Does the magnitude of the response depend on whether prey consumption increases via number or size of prey? We find that the phenotypic response of prey is an asymptotic function of prey biomass consumed. However, the asymptotic response is higher when more prey are consumed. Our findings have important implications for evaluating past studies and how future experiments should be designed. A stronger response to predation cues generated by more individual prey deaths is consistent with models that predict prey sensitivity to per capita risk, providing a more direct link between empirical and theoretical studies which are often focused on changes in population sizes not individual biomass.     

Reversed predator–prey cycles are driven by the amplitude of prey oscillations

Ecoevolutionary feedbacks in predator–prey systems have been shown to qualitatively alter predator–prey dynamics. As a striking example, defense–offense coevolution can reverse predator–prey cycles, so predator peaks precede prey peaks rather than vice versa. However, this has only rarely been shown in either model studies or empirical systems. Here, we investigate whether this rarity is a fundamental feature of reversed cycles by exploring under which conditions they should be found. For this, we first identify potential conditions and parameter ranges most likely to result in reversed cycles by developing a new measure, the effective prey biomass, which combines prey biomass with prey and predator traits, and represents the prey biomass as perceived by the predator. We show that predator dynamics always follow the dynamics of the effective prey biomass with a classic ¼‐phase lag. From this key insight, it follows that in reversed cycles (i.e., ¾‐lag), the dynamics of the actual and the effective prey biomass must be in antiphase with each other, that is, the effective prey biomass must be highest when actual prey biomass is lowest, and vice versa. Based on this, we predict that reversed cycles should be found mainly when oscillations in actual prey biomass are small and thus have limited impact on the dynamics of the effective prey biomass, which are mainly driven by trait changes. We then confirm this prediction using numerical simulations of a coevolutionary predator–prey system, varying the amplitude of the oscillations in prey biomass: Reversed cycles are consistently associated with regions of parameter space leading to small‐amplitude prey oscillations, offering a specific and highly testable prediction for conditions under which reversed cycles should occur in natural systems.     

Incorporating Motion into Investigations of mimicry

During the past thirty years, natural selection due to predation has been investigated with regard to prey motion in three areas that are relevant to the evolution of mimicry: (1) anti-apostatic selection, (2) locomotor mimicry, and (3) escape mimicry. Anti-apostatic selection, or selection against the odd individuals, arises when prey are at very high densities or when prey are Müllerian mimics. When prey are at high densities, motion of the prey increases selection against odd individuals. When the prey are Müllerian mimics, motion may also play an important role in strengthening selection against odd individuals. This may explain locomotor mimicry between Müllerian mimics. Locomotor mimicry arises when two distantly-related prey species appear alike in behaviour, and there is a corresponding suite of morphological, physiological, and biomechanical traits that the prey have in common. Locomotor mimicry has been demonstrated in Müllerian mimics. It is also predicted to occur in Batesian mimics but with important limitations due to selection by the predator for the prey to maintain the ability to escape if detected. Locomotor mimicry may also occur between palatable species that are alike as a result of unprofitable prey (or escape) mimicry. Escape mimicry arises when prey are difficult to capture. By frustration learning, the predator associates the colour of the prey with unprofitability. In all three instances, dis-similarity in colour or motion probably increases selection against the odd individual. In addition, the interaction of colour and motion gives rise to greater reliability of the signals to a specialist predator. However for a generalist predator, multiple component signals of the prey lead to errors in signal perception and greater risk of cheating. This revised version was published online in July 2006 with corrections to the Cover Date.     

Effects of crayfish size,orientation, and movement on the reactive distance of largemouth bass foraging in clear and turbid water

Laboratory experiments were performed in clear and turbid water to determine the effects of prey size, orientation, and movement on the reactive distance of largemouth bass (Micropterus salmoides) when feeding on crayfish (Procambarus acutus). In clear water, the reactive distance increased linearly with an increase in prey size, and prey movement resulted in a significant increase in the reactive distance. Prey orientation (head-on versus perpendicular) did not change the reactive distances. In moderately turbid water, the reactive distance did not increase with increased prey size, and prey movement did not result in any changes in the reactive distance. The absence of any effects of prey orientation in clear water or prey movement in turbid water is inconsistent with results from studies using different species (primarily planktivorous fish). I propose that largemouth bass change their foraging tactics as prey visibility changes. When prey are highly visible (low turbidity), predators attack (react) only after prey recognition, which is based on multiple cues such as prey size (length, width) and movement. When prey are less visible (high turbidity), predators attack immediately upon initial prey sighting, which does not depend on prey size or movement.     

The evolution of warning signals as reliable indicators of prey defense

It is widely argued that defended prey have tended to evolve conspicuous traits because predators more readily learn to avoid defended prey when they are conspicuous. However, a rival theory proposes that defended prey have evolved such characters because it allows them to be distinguished from undefended prey. Here we investigated how the attributes of defended (unprofitable) and undefended (profitable) computer-generated prey species tended to evolve when they were subject to selection by foraging humans. When cryptic forms of defended and undefended species were similar in appearance but their conspicuous forms were not, defended prey became conspicuous while undefended prey remained cryptic. Indeed, in all of our experiments, defended prey invariably evolved any trait that enabled them to be distinguished from undefended prey, even if such traits were cryptic. When conspicuous mutants of defended prey were extremely rare, they frequently overcame their initial disadvantage by chance. When Batesian mimicry of defended species was possible, defended prey evolved unique traits or characteristics that would make undefended prey vulnerable. Overall, our work supports the contention that warning signals are selected for their reliability as indicators of defense rather than to capitalize on any inherent educational biases of predators.     

Morphological limitations, prey size selectivity, and growth response of juvenile atlantic salmon, Salmo salar

The head and jaw movements involved in capture, buccal manipulation, ingestion and rejection of prey were investigated using sequential photography of juvenile Atlantic salmon feeding in a simulated stream environment. The results are described and discussed and mouth breadth and gill raker spacing are proposed as morphometric limitations to the range of prey sizes available which remains constant at 0·06 · fish fork length ( PFR ).
A recirculatory flume tank was used to study prey size selectivity behavior. Simplified downstream-drifting prey items elicited a variety of responses depending on their physical size. One hundred percent of offered prey of PFR 0·025 were ingested, while 90 % of prey at PFR 0·051 and 100% of prey at PFR 0·105 were rejected. It is demonstrated that fish show negative selection for prey sizes smaller than PFR 0·025 and that prey of this size elicits maximum growth response.
The validity of the proposed morphometric limitations on the available prey sizes is demonstrated by reference to selectivity behaviour and prey size related differential growth.     

Coupled predator–prey oscillations in a chaotic food web

Coupling of several predator–prey oscillations can generate intriguing patterns of synchronization and chaos. Theory predicts that prey species will fluctuate in phase if predator–prey cycles are coupled through generalist predators, whereas they will fluctuate in anti-phase if predator–prey cycles are coupled through competition between prey species. Here, we investigate predator–prey oscillations in a long-term experiment with a marine plankton community. Wavelet analysis of the species fluctuations reveals two predator–prey cycles that fluctuate largely in anti-phase. The phase angles point at strong competition between the phytoplankton species, but relatively little prey overlap among the zooplankton species. This food web architecture is consistent with the size structure of the plankton community, and generates highly dynamic food webs. Continued alternations in species dominance enable coexistence of the prey species through a non-equilibrium 'killing-the-winner' mechanism, as the system shifts back and forth between the two predator–prey cycles in a chaotic fashion.     

Keeping the herds healthy and alert: implications of predator control for infectious disease

Predator control programmes are generally implemented in an attempt to increase prey population sizes. However, predator removal could prove harmful to prey populations that are regulated primarily by parasitic infections rather than by predation. We develop models for microparasitic and macroparasitic infection that specify the conditions where predator removal will (a) increase the incidence of parasitic infection, (b) reduce the number of healthy individuals in the prey population and (c) decrease the overall size of the prey population. In general, predator removal is more likely to be harmful when the parasite is highly virulent, macroparasites are highly aggregated in their prey, hosts are long‐lived and the predators select infected prey.     

Prey detection in a cruising copepod

Small cruising zooplankton depend on remote prey detection and active prey capture for efficient feeding. Direct, passive interception of prey is inherently very inefficient at low Reynolds numbers because the viscous boundary layer surrounding the approaching predator will push away potential prey. Yet, direct interception has been proposed to explain how rapidly cruising, blind copepods feed on non-motile phytoplankton prey. Here, we demonstrate a novel mechanism for prey detection in a cruising copepod, and describe how motile and non-motile prey are discovered by hydromechanical and tactile or, likely, chemical cues, respectively.