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.     

Spatial processes can determine the relationship between prey encounter rate and prey density

Theoretical models frequently assume that the rate at which a searching predator encounters prey increases linearly with prey density. In a recent experiment using great tits searching for winter moth caterpillars, the time to find the first prey item did not decline as quickly with density as the standard theory assumes. Using a spatial simulation model, we show that prey aggregation and/or spatially correlated searching behaviour by the predator can generate a range of relationships, including results that are qualitatively similar to those found in the great tit experiment. We suggest that further experiments are required to determine whether the explanation proposed here is correct, and that theoretical work is needed to determine how this behaviour is likely to influence the ecological and evolutionary dynamics of predator-prey communities.     

Explicit model for searching behavior of predator

The authors present an approach for explicit modeling of spatio-temporal dynamics of predator-prey community. This approach is based on a reaction-diffusion-adjection PD (prey dependent) system. Local kinetics of population is determined by logistic reproduction function of prey, constant natural mortality of predator and Holling type 2 trophic function. Searching behavior of predator is described by the advective term in predator balance equation assuming the predator acceleration to be proportional to the prey density gradient. The model was studied with zero-flux boundary conditions. The influence of predator searching activity on the community dynamics, in particular, on the emergence of spatial heterogeneity, has been investigated by linear analysis and numerical simulations. It has been shown how searching activity may effect the persistence of species, stabilizing predator-prey interactions at very low level of pest density. It has been demonstrated that obtaining of such dynamic regimes does not require the use of complex trophic functions.     

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.     

ORGANIZATION OF PREDATOR-PREY COMMUNITIES AS AN EVOLUTIONARY GAME

We consider a simple predator-prey model of coevolution. By allowing coevolution both within and between trophic levels the model breaks the traditional dichotomy between coevolution among competitors and coevolution between a prey and its predator. By allowing the diversity of prey and predator species to emerge as a property of the evolutionarily stable strategies (ESS), the model breaks another constraint of most approaches to coevolution that consider as fixed the number of coevolving species. The number of species comprising the ESS is influenced by a parameter that determines the predator's niche breadth. Depending upon the parameter's value the ESS may contain: 1) one prey and one predator species, 2) two prey and one predator, 3) two prey and two predators, 4) three prey and two predators, 5) three prey and three predators, etc. Evolutionarily, these different ESSs all emerge from the same model. Ecologically, however, these ESSs result in very different patterns of community organization. In some communities the predator species are ecologically keystone in that their removal results in extinctions among the prey species. In others, the removal of a predator species has no significant impact on the prey community. These varied ecological roles for the predator species contrasts sharply with the essential evolutionary role of the predators in promoting prey species diversity. The ghost of predation past in which a predator's insignificant ecological role obscures its essential evolutionary role may be a frequent property of communities of predator and prey.     

How predator incursions affect critical patch size: the role of the functional response

Understanding the impact of habitat edges provides a key to deciphering how community dynamics change as functions of habitat structure and spatial scale. Motivated by studies of predation on bird nests in forest fragments and other cases of "cross-boundary subsidies," we present results from a partial differential equation model in which a patch-resident prey species suffers incidental mortality from a generalist predator species residing in the surrounding matrix habitat. We demonstrate that predator intrusions have the potential to induce critical patch size effects for the prey species, even when the prey's dynamics would otherwise preclude such effects. We also demonstrate that the existence of critical patch size effects depends on the functional response of the predator, with Lotka-Volterra and Type II functional responses generating the effect (but not Type III). We conclude by discussing how predator-induced critical patch size effects can influence opportunities for regionwide persistence of the prey by altering the fraction and spatial distribution of meaningful patches within a metapopulation.     

Behavioral responses to prey density by three acarine predator species with different degrees of polyphagy

Behavioral responses by three acarine predators, Phytoseiulus persimilis, Typhlodromus occidentalis, and Amblyseius andersoni (Acari: Phytoseiidae), to different egg and webbing densities of the spider mite Tetranychus urticae (Acari: Tetranychidae) on rose leaflets were studied in the laboratory. Prey patches were delineated by T. urticae webbing and associated kairomones, which elicit turning back responses in predators near the patch edge. Only the presence of webbing affected predator behavior; increased webbing density did not increase patch time. Patch time increased with increased T. urticae egg density in the oligophagous P. persimilis, but was density independent in the polyphagous species T. occidentalis and A. andersoni. Patch time in all three species was more strongly correlated with the number of prey encounters and attacks than with the actual prey number present in the patch. Patch time was determined by (a) the turning back response near the patch edge; this response decayed through time and eventually led to the abandonment of the patch, and (b) encounters with, and attacks upon, prey eggs; these prolonged patch time by both an increment of time spent in handling or rejecting prey and an increment of time spent searching between two successive prey encounters or attacks. Although searching efficiency was independent of prey density in all three species, the predation rate by P. persimilis decreased with prey density because its searching activity (i.e. proportion of total patch time spent in searching) decreased with prey density. Predation rates by T. occidentalis and A. andersoni decreased with prey density because their searching activity and success ratio both decreased with prey density. The data were tested against models of predator foraging responses to prey density. The effects of the degree of polyphagy on predator foraging behavior were also discussed.     

Influence of intra‐ and interspecific variation in predator–prey body size ratios on trophic interaction strengths

1. Predation is a pervasive force that structures food webs and directly influences ecosystem functioning. The relative body sizes of predators and prey may be an important determinant of interaction strengths. However, studies quantifying the combined influence of intra‐ and interspecific variation in predator–prey body size ratios are lacking.
2. We use a comparative functional response approach to examine interaction strengths between three size classes of invasive bluegill and largemouth bass toward three scaled size classes of their tilapia prey. We then quantify the influence of intra‐ and interspecific predator–prey body mass ratios on the scaling of attack rates and handling times.
3. Type II functional responses were displayed by both predators across all predator and prey size classes. Largemouth bass consumed more than bluegill at small and intermediate predator size classes, while large predators of both species were more similar. Small prey were most vulnerable overall; however, differential attack rates among prey were emergent across predator sizes. For both bluegill and largemouth bass, small predators exhibited higher attack rates toward small and intermediate prey sizes, while larger predators exhibited greater attack rates toward large prey. Conversely, handling times increased with prey size, with small bluegill exhibiting particularly low feeding rates toward medium–large prey types. Attack rates for both predators peaked unimodally at intermediate predator–prey body mass ratios, while handling times generally shortened across increasing body mass ratios.
4. We thus demonstrate effects of body size ratios on predator–prey interaction strengths between key fish species, with attack rates and handling times dependent on the relative sizes of predator–prey participants.
5. Considerations for intra‐ and interspecific body size ratio effects are critical for predicting the strengths of interactions within ecosystems and may drive differential ecological impacts among invasive species as size ratios shift.

     

Warning signals and predator-prey coevolution

Theories of the evolution of warning signals are typically expressed using analytic and computational models, most of which attribute aspects of predator psychology as the key factors facilitating the evolution of warning signals. Sherratt provides a novel and promising perspective with a model that considers the coevolution of predator and prey populations, showing how predators may develop a bias towards attacking cryptic prey in preference to conspicuous prey. Here, we replicate the model as an individual-based simulation and find, in accordance with Sherratt, that predators evolve a bias towards attacking cryptic prey. We then use a Monte Carlo simulation to calculate the relative survivorships of cryptic and conspicuous prey and stress that, as it stands, the model does not predict the evolution or stability of warning signals. We extend the model by giving predators continuous attack strategies and by allowing the evolution of prey conspicuousness: results are robust to the first modification but, in all cases, cryptic prey always enjoy a higher survivorship than conspicuous prey. When conspicuousness is allowed to evolve, prey quickly evolve towards crypsis, even when runaway coevolution is enabled. Sherratt's approach is promising, but other aspects of predator psychology, besides their innate response, remain vital to our understanding of warning signals.     

Depletion models can predict shorebird distribution at different spatial scales

Predicting the impact of habitat change on populations requires an understanding of the number of animals that a given area can support. Depletion models enable predictions of the numbers of individuals an area can support from prey density and predator searching efficiency and handling time. Depletion models have been successfully employed to predict patterns of abundance over small spatial scales, but most environmental change occurs over large spatial scales. We test the ability of depletion models to predict abundance at a range of scales with black-tailed godwits, Limosa limosa islandica. From the type II functional response of godwits to their prey, we calculated the handling time and searching efficiency associated with these prey. These were incorporated in a depletion model, together with the density of available prey determined from surveys, in order to predict godwit abundance. Tests of these predictions with Wetland Bird Survey data from the British Trust for Ornithology showed significant correlations between predicted and observed densities at three scales: within mudflats, within estuaries and between estuaries. Depletion models can thus be powerful tools for predicting the population size that can be supported on sites at a range of scales. This greatly enhances our confidence in predictions of the consequences of environmental change.     

Evaluating the effects of large marine predators on mobile prey behavior across subtropical reef ecosystems

The indirect effect of predators on prey behavior, recruitment, and spatial relationships continues to attract considerable attention. However, top predators like sharks or large, mobile teleosts, which can have substantial top–down effects in ecosystems, are often difficult to study due to their large size and mobility. This has created a knowledge gap in understanding how they affect their prey through nonconsumptive effects. Here, we investigated how different functional groups of predators affected potential prey fish populations across various habitats within Biscayne Bay, FL. Using baited remote underwater videos (BRUVs), we quantified predator abundance and activity as a rough proxy for predation risk and analyzed key prey behaviors across coral reef, sea fan, seagrass, and sandy habitats. Both predator abundance and prey arrival times to the bait were strongly influenced by habitat type, with open homogenous habitats receiving faster arrival times by prey. Other prey behaviors, such as residency and risk‐associated behaviors, were potentially driven by predator interaction. Our data suggest that small predators across functional groups do not have large controlling effects on prey behavior or stress responses over short temporal scales; however, habitats where predators are more unpredictable in their occurrence (i.e., open areas) may trigger risk‐associated behaviors such as avoidance and vigilance. Our data shed new light on the importance of habitat and context for understanding how marine predators may influence prey behaviors in marine ecosystems.     

Contemporary evolution and genetic change of prey as a response to predator removal

The ecological effects of predator removal and its consequence on prey behavior have been investigated widely; however, predator removal can also cause contemporary evolution of prey resulting in prey genetic change. Here we tested the role of predator removal on the contemporary evolution of prey traits such as movement, reproduction and foraging. We use EcoSim simulation which allows complex intra- and inter-specific interactions, based on individual evolving behavioral models, as well as complex predator–prey dynamics and coevolution in spatially homogenous and heterogeneous worlds. We model organisms' behavior using fuzzy cognitive maps (FCM) that are coded in their genomes which has a clear semantics making reasoning about causality of any evolved behavior possible. We show that the contemporary evolution of prey behavior owing to predator removal is also accompanied by prey genetic change. We employed machine learning methods, now recognized as holding great promise for the advancement of our understanding and prediction of ecological phenomena. A classification algorithm was used to demonstrate the difference between genomes belonging to prey coevolving with predators and prey evolving in the absence of predation pressure. We argue that predator introductions to naive prey might be destabilizing if prey have evolved and adapted to the absence of predators. Our results suggest that both predator introductions and predator removal from an ecosystem have widespread effects on the survival and evolution of prey by altering their genomes and behavior, even after relatively short time intervals. Our study highlights the need to consider both ecological and evolutionary time scales, as well as the complex interplay of behaviors between trophic levels, in determining the outcomes of predator–prey interactions.     

Consequences of refuge for the functional response of Dermestes ater (Coleoptera: Dermestidae) to Musca domestica (Diptera: Muscidae)

It is well known that a predator has the potential to regulate a prey population only if the predator responds to increases in prey density and inflicts greater mortality rates. Predators may cause such density-dependent mortality depending on the nature of the functional and numerical responses. Yet, few studies have examined the relationship between the addition of refuges and the characteristic of functional response fits. We investigated whether addition of a refuge changed the type of functional response exhibited by Dermestes ater on Musca domestica, comparing the inherent ability of D. ater to kill houseflies in the absence and in the presence of refuge. An additional laboratory experiment was also carried out to assess handling and searching times exhibited by D. ater. Logistic regression analyses revealed a type III functional response for predator–prey interaction without refuge, and results were described by the random predator equation. The mean number of prey killed did not differ between experimental habitats, indicating that the addition of refuge did not inhibit predation. However, predators that interacted with prey without refuge spent less time searching for prey at higher densities, increasing predatory interaction. We concluded that this interaction may be weak, because data from experiments with refuge fitted poorly to models. However, the high variability and the nonsignificance of the data from the experiment with refuge show the importance of refuge for promoting spatial heterogeneity, which may prevent prey extinction.     

Spatial extinction or persistence: landscape‐temperature interactions perturb predator–prey dynamics

Recognising that species interact across a range of spatial scales, we explore how landscape structure interacts with temperature to influence persistence. Specifically, we recognise that few studies indicate thermal shifts as the proximal cause of species extinctions; rather, species interactions exacerbated by temperature result in extinctions. Using microcosm‐based experiments, as models of larger landscape processes, we test hypotheses that would be problematic to address through field work. A text‐book predator–prey system (the ciliates Didinium and Paramecium) was used to compare three landscapes: an unfragmented landscape subjected to uniform temperatures (10, 20, 30°C); a fragmented landscape (potentially hosting metapopulations) subjected to these three temperatures; and a fragmented landscape subjected to a spatial temperature gradient (～ 10 to 30°C) – despite the prevalence of natural temperature ecoclines this is the first time such an analysis has been conducted. Initial thermal response‐analysis (growth, mortality, and movement measured between 10 and 30°C) suggested that as temperature increased, the predator might drive the prey to extinction. Thermal preferences (measured at 5 temperatures between 10 and 30°C), indicated that both predator and prey preferred warmer temperatures, with the predator exhibiting the stronger preference, suggesting that cooler regions might act as a prey‐refuge. The landscape level observations, however, did not entirely support the predictions. First, in the unfragmented landscape, increased temperature led to extinctions, but at the highest temperature (where the predator growth can be reduced) the prey survived. Second, at high temperatures the fragmented landscape failed to host metapopulations that would allow predator–prey persistence. Third, the thermal ecocline did not provide heterogeneity that improved stability; rather it forced both species to occupy a smaller realized space, leading toward extinctions. These findings reveal that temperature‐impacted rates and temperature preferences combine to drive predator–prey dynamics and persistence across landscapes.     

Coevolution-driven predator-prey cycles: predicting the characteristics of eco-coevolutionary cycles using fast-slow dynamical systems theory

Eco-coevolutionary theory predicts that predator-prey coevolution occurring on the time scale of ecological dynamics (e.g., changes in population abundances) can drive novel kinds of predator-prey cycles, e.g., cryptic cycles where one species cycles while the other remains effectively constant and clockwise cycles where peaks in predator density precede peaks in prey density. However, because this body of theory has focused on particular models and studied the different cycle types in isolation, it is unclear what biological characteristics (e.g., costs for offense or defense) determine when a particular cycle type will arise. In this study, I explore the kinds of predator-prey cycles that arise in a general eco-coevolutionary model where there is disruptive selection and the coevolutionary dynamics are fast relative to the ecological dynamics of the system. With a graphical tool created using the theory of fast-slow dynamical systems, I predict what kinds of cycles can arise in the model and how cycle type depends on the costs for prey defense and predator offense. Fast-slow dynamical systems theory requires a separation of time scales between the ecological and evolutionary processes; however, numerical simulations show that this tool can help predict how coevolution drives populations cycles in systems where the speeds of ecological and evolutionary dynamics are comparable. Thus, this work is a step forward in building a general eco-coevolutionary theory.     

Consequences of food distribution for optimal searching behavior: an evolutionary model

Resource distribution can vary greatly in space and time. Consequently, animals should adjust their searching tactics to such spatio–temporal patterns in accordance with their innate capabilities, or alternatively, they should use a genetically fixed searching tactic that has been evolved in response to the specific pattern of the food they experience. Using a simulation model and a genetic algorithm, we show how optimal searching tactics change as a function of food spatial pattern. Searching tactics for hidden prey can be approximated using the following three components: (1) Extensive search mode (ESM), the type of movement before encountering a food item; (2) Intensive search mode (ISM), the type of movement after encountering a food item; and (3) ISM duration. Both ESM and ISM are characterized by movement tortuosity. We show that searching behavior adaptively changes as a function of food pattern. When food is distributed in a regular pattern, ISM is more directional than ESM, but under a clumped food pattern, ISM is much more tortuous than ESM. It may suggest that animals with larger spectra of searching tactics should experience greater variance or seasonal changes in their food pattern than animals with narrow spectra of searching tactics. Increased forager attack radius diminishes the differences between ESM and ISM, and thus the use of these three components to model searching in animals with higher attack radii is not appropriate. Increased handling time, which is a surrogate of reducing habitat profitability results in longer patch residency time as expected by optimal foraging theory. To conclude, we suggest that using such a combined approach of simulation models and genetic algorithms may improve our understanding of how extrinsic and intrinsic factors interact to influence searching behavior.     

Predator–prey interactions in a ladybeetle–aphid system depend on spatial scale

The outcome of species interactions may manifest differently at different spatial scales; therefore, our interpretation of observed interactions will depend on the scale at which observations are made. For example, in ladybeetle–aphid systems, the results from small‐scale cage experiments usually cannot be extrapolated to landscape‐scale field observations. To understand how ladybeetle–aphid interactions change across spatial scales, we evaluated predator–prey interactions in an experimental system. The experimental habitat consisted of 81 potted plants and was manipulated to facilitate analysis across four spatial scales. We also simulated a spatially explicit metacommunity model parallel to the experiment. In the experiment, we found that the negative effect of ladybeetles on aphids decreased with increasing spatial scales. This pattern can be explained by ladybeetles strongly suppressing aphids at small scales, but not colonizing distant patches fast enough to suppress aphids at larger scales. In the experiment, the positive effects of aphids on ladybeetles were strongest at three‐plant scale. In a model scenario where predators did not have demographic dynamics, we found, consistent with the experiment, that both the effects of ladybeetles on aphids and the effects of aphids on ladybeetles decreased with increasing spatial scales. These patterns suggest that dispersal was the primary cause of ladybeetle population dynamics in our experiment: aphids increased ladybeetle numbers at smaller scales because ladybeetles stayed in a patch longer and performed area‐restricted searches after encountering aphids; these behaviors did not affect ladybeetle numbers at larger spatial scales. The parallel experimental and model results illustrate how predator–prey interactions can change across spatial scales, suggesting that our interpretation of observed predator–prey dynamics would differ if observations were made at different scales. This study demonstrates how studying ecological interactions at a range of scales can help link the results of small‐scale ecological experiments to landscape‐scale ecological problems.     

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

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

The functional response of Toxorhynchites rutilus rutilus to changes in the population density of its prey Aedes aegypti

We present an analysis of the functional response of the predator Toxorhynchites rutilus rutilus (Coquillett) to changes in the density of the larvae of Aedes aegypti (L.) (Diptera: Culicidae). The experiment was replicated for five different ages, and at three different densities of the predator. The data were fitted to Rogers' (1972) random predator equation by non-linear least-squares in order to estimate searching efficiency and handling time for each experimental treatment. The data show that estimated searching efficiencies are highest at intermediate ages of the predator for all predator densities tested. Handling time declines exponentially with increasing predator age. There is a marked interference effect; searching efficiency decreases with increased predator density, and this is most pronounced at intermediate prey ages. Estimated handling times increase with predator density at a rate which declines with increasing predator age.     

Effects of prey-size and predator-instar on the predation of Daphnia by Notonecta

Abstract. 1. Attack rates and handling times are measured by a series of separate functional response experiments for each instar of Notonecta glauca attacking four size classes of Daphnia magna as prey. The resulting attack rate and handling time surfaces are complex, with maximum attack rates for small predators attacking small prey, and large predators attacking large prey. Adult Notonecta have lower attack rates than the two previous juvenile instars (4 and 5).
2. The literature on attack rates and handling times in other predator—prey interactions that involve a series of different predator and prey size or age classes is reviewed in the context of the Notonecta-Daphnia results. The data suggest that small predator instars will usually compete with large instars for food, unless there is spatial or temporal separation between them.
3. Complex attack rate and handling time surfaces are to be expected wherever a wide range of prey and predator sizes is involved.
4. Size related changes in attack rates and handling times can introduce very complex dynamics into predator-prey interactions.