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

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

Predator–prey naïveté, antipredator behavior,and the ecology of predator invasions

We present a framework for explaining variation in predator invasion success and predator impacts on native prey that integrates information about predator–prey naïveté, predator and prey behavioral responses to each other, consumptive and non‐consumptive effects of predators on prey, and interacting effects of multiple species interactions. We begin with the ‘naïve prey’ hypothesis that posits that naïve, native prey that lack evolutionary history with non‐native predators suffer heavy predation because they exhibit ineffective antipredator responses to novel predators. Not all naïve prey, however, show ineffective antipredator responses to novel predators. To explain variation in prey response to novel predators, we focus on the interaction between prey use of general versus specific cues and responses, and the functional similarity of non‐native and native predators. Effective antipredator responses reduce predation rates (reduce consumptive effects of predators, CEs), but often also carry costs that result in non‐consumptive effects (NCEs) of predators. We contrast expected CEs versus NCEs for non‐native versus native predators, and discuss how differences in the relative magnitudes of CEs and NCEs might influence invasion dynamics. Going beyond the effects of naïve prey, we discuss how the ‘naïve prey’, ‘enemy release’ and ‘evolution of increased competitive ability’ (EICA) hypotheses are inter‐related, and how the importance of all three might be mediated by prey and predator naïveté. These ideas hinge on the notion that non‐native predators enjoy a ‘novelty advantage’ associated with the naïveté of native prey and top predators. However, non‐native predators could instead suffer from a novelty disadvantage because they are also naïve to their new prey and potential predators. We hypothesize that patterns of community similarity and evolution might explain the variation in novelty advantage that can underlie variation in invasion outcomes. Finally, we discuss management implications of our framework, including suggestions for managing invasive predators, predator reintroductions and biological control.     

Effects of perceptual and movement ranges on joint predator–prey distributions

We developed a spatially‐explicit individual‐based model to study how limited perceptual and movement ranges affect spatial predator–prey interactions. Earlier models of ‘predator–prey space games’ were often developed by modifying ideal free distribution models, which are spatially‐implicit and also assume that individuals are omniscient, although some more recent models have relaxed these assumptions. We found that under some conditions, the spatially‐explicit model generated similar predictions to previous models. However, the model showed that limited range in a spatially‐explicit context generated different predictions when 1) predator density and range are both small, and 2) when the predator movement range varied while the prey range was small. The model suggests that the differences were the result of 1) movement range changing the value of information sources and thus changing the behavior of individual predators and prey and 2) movement range limiting the ability of individuals to exploit the environment.     

Dragonfly larvae and tadpole frog space use games in varied light conditions

Predators and prey often engage in a game where predators attemptto be in areas with higher prey densities and prey attempt tobe in areas with lower predator densities. A few models havepredicted the resulting distributions of predators and prey,but little empirical data exist to test these predictions andto examine how abiotic and biotic factors shape the distributions.Thus, we observed how Anax dragonfly nymphs and Pacific treefrog tadpoles (Pseudacris regilla) either together or separatelydistributed themselves in an arena with a high- and a low-preyresource patch. Trials were conducted in high- and low-lightconditions to manipulate predation risk and to view the effectsof this abiotic factor. Counter to the model predictions, wefound that predators were not more abundant in high-resource(HR) patches, and they thus did not force prey toward beinguniformly distributed. Using a model selection approach to assesswhat factors affected predator and prey patch-switching movement,we found that prey more often left patches that had more predatorspresent, but predators surprisingly more often left patcheswith more prey present. Light levels did not affect predationrisk; however, in the dark with the associated reduction invisual information predators preferred HR patches. This causeda lower coincidence of prey and predators in patches. Predatorsalso switched patches less often when they occupied the samepatch as the other predator. This suggests that predator distributions,and indirectly prey distributions, are affected by the riskof intraguild predation.     

Shaped by the past,acting in the present: transgenerational plasticity of anti‐predatory traits

Phenotypic expression can be altered by direct perception of environmental cues (within‐generation phenotypic plasticity) and by the environmental cues experienced by previous generations (transgenerational plasticity). Few studies, however, have investigated how the characteristics of phenotypic traits affect their propensity to exhibit plasticity within and across generations. We tested whether plasticity differed within and across generations between morphological and behavioral anti‐predator traits of Physa acuta, a freshwater snail. We reared 18 maternal lineages of P. acuta snails over two generations using a full factorial design of exposure to predator or control cues and quantified adult F₂ shell size, shape, crush resistance, and anti‐predator behavior – all traits which potentially affect their ability to avoid or survive predation attempts. We found that most morphological traits exhibited transgenerational plasticity, with parental exposure to predator cues resulting in larger and more crush‐resistant offspring, but shell shape demonstrated within‐generation plasticity. In contrast, we found that anti‐predator behavior expressed only within‐generation plasticity such that offspring reared in predator cues responded less to the threat of predation than control offspring. We discuss the consequences of this variation in plasticity for trait evolution and ecological dynamics. Overall, our study suggests that further empirical and theoretical investigation is needed in what types of traits are more likely to be affected by within‐generational and transgenerational plasticity.     

Reproductive decision-making by female peacock wrasses: flexible versus fixed behavioral rules in variable environments

Because environments are temporally variable, animals may oftenestimate the current environmental state to inform their behavioralchoices. However, using experience may cause behavior to lagbehind the current state of the environment, and estimates maysuffer from sampling errors. We used stochastic dynamic modelsto examine the environmental conditions that favor flexible ratherthan fixed estimates and behaviors. The examination was conductedin the context of reproductive decisions made by the femalepeacock wrasse (Symphodus tinca), a nearshore Mediterraneanfish. Female peacock wrasses can choose to spawn in a nest,with males that defend these nests within territories, or outof a nest, with males that defend neither territories nor nests.A female must expend effort and time to find nesting males,and the profitability of this search, relative to spawning with nonnestingmales, changes with the density of nests and relative hatching successof eggs in and out of nests. A female can increase her fitnessby estimating the environment's state and matching her reproductivedecisions to the current environment. These estimates can beflexible and formed by experience, or fixed and formed by selection.We found that flexible estimates based on experience do betterwhen there is variance within and between seasons and when thereis greater uncertainty. The optimal rate for forgetting experiencesis set by the rate of environmental change. Comparisons of predictedfemale behavior using flexible and fixed estimates with observed behaviorsuggest that females use estimates that are updated by experience.     

Predator and Prey Models with Flexible Individual Behavior and Imperfect Information

To begin identifying what behavioral details might be needed to characterize community dynamics and stability, we examined the effect of prey behavioral responses to predation risk on community dynamics and stability. We considered the case of prey altering their foraging effort to trade off energy gain and predation risk. We used state-dependent dynamic optimization to calculate the optimal trade-off for four models of prey behaviorally responding to predation risk. We consider a fixed behavior model in which prey use constant levels of foraging effort and three flexible behavior models in which prey change their foraging effort according to their physiological state and their perceived level of predation risk. Flexible behavior was destabilizing at the community level as evidenced by higher predator-prey oscillations and lower community persistence times. The mechanisms by which prey estimated predation risk also affected community stability. We found that community dynamics resulting from prey with flexible behavior and fixed perception of risk approximated community dynamics resulting from prey with flexible behavior and perfect information about predation risk, however neither approximated the community dynamics resulting from prey with flexible behavior and flexible perception of risk. Thus, whether it might be possible to abstract complex behavior with simpler rules when modeling community dynamics depends on the prey's behavioral mechanisms, which are empirically poorly known.     

Weather Influences Multiple Components of Greater Prairie-Chicken Reproduction

The influence of weather on wildlife populations has been documented for many species; however, much of the current literature has focused on the effects of weather within a season and consists of short-term studies. The use of long-term datasets that cover a variety of environmental conditions will be essential for assessing possible carry-over effects of weather experienced in one season on behavior and fitness in subsequent seasons. In this study, we evaluated the effects of weather variables measured over multiple temporal scales on the reproductive performance and behavior of greater prairie-chickens (Tympanuchus cupido) in Osage County, Oklahoma, USA, from 2011–2019. Considering weather over a range of temporal extents allowed us to determine the relative importance of short-term weather events, such as daily temperature and precipitation, versus more chronic shifts in weather such as persistent drought on the reproductive performance of greater prairie-chickens. We used an information-theoretic model building approach to develop models describing the effects of daily weather variables and drought conditions on daily nest survival, nest incubation start dates, and clutch size. Daily nest survival was primarily influenced by conditions experienced during incubation with daily nest success declining in years with wetter than average springs and during extreme precipitation events. Daily nest survival also declined under higher maximum daily temperatures, especially in years with below-average rainfall. Greater prairie-chickens began nesting earlier and had smaller clutch sizes for initial nests and renests in years with warmer temperatures prior to the nesting season. Additionally, incubation of nests started later in drought years, indicating carry-over effects in greater prairie-chicken reproductive behaviors. Our work shows that if the weather in the Great Plains becomes more variable, with increasing frequency of drought and extreme precipitation events, wildlife species that inhabit these grassland landscapes will likely experience changes in reproduction, potentially influencing future populations. © 2020 The Wildlife Society.     

The effect of predation pressure and predator adaptive foraging on the relative importance of consumptive and non‐consumptive predator net effects in a freshwater model system

An important challenge in community ecology is identifying the functional characteristics capable of predicting the nature and strength of predator effects on food webs. We developed an individual‐based model, based on a shallow lake model system, to evaluate the total, consumptive, and non‐consumptive indirect effect that predators have on basal resources when the predators differ in their foraging types (active adaptive foraging or sedentary foraging). Overall, both predator types caused similar total indirect effects on lower trophic levels. However, the nature net effects of predators diverged between predator foraging types. Active predators caused larger non‐consumptive effects, relative to the total indirect effect, irrespective of predation pressure levels. On the other hand, sedentary predators caused larger non‐consumptive effects for lower predation pressure levels, but consumptive effects became more important as predation pressure increased. Our simulations showed that the reliance on a particular mechanism driving consumer–resource interactions is altered by predator foraging behavior and highlight the importance of both prey and predator foraging behaviors to predict the causes and consequences of cascading effects observed in food webs.     

Assessing the robustness and optimality of alternative decision rules with varying assumptions

Several alternative decision rules have been proposed for how individuals assess and choose options, such as mates and territories. Three of these rules are the threshold rule, where individuals choose the first option that exceeds a preset level of quality, the best-of- n rule, where individuals assess a fixed number of options and then choose the best of those options, and the comparative Bayes rule, where individuals use estimates of options to selectively assess and choose options. It has been previously concluded that the threshold rule produces higher average fitness than the best-of- n rule when assessment costs are not trivial. However, previous comparisons assumed that time and options are infinite, individuals can estimate the distribution of option quality without uncertainty or mistakes, and individuals receive perfect information about the quality of assessed options. I found that the best-of- n rule produces higher average fitness than the threshold rule despite significant assessment costs, when time for choosing an option is limited, when individuals are choosing from a small pool of options, when estimates of the distribution of option quality are error-prone, and when there is uncertainty about the distribution of option quality. I also found that the comparative Bayes rule produces higher average fitness than the threshold and best-of-n rules when time or options are limited and when individuals receive imperfect information about the quality of assessed options. Therefore, the optimality of alternative decision rules depends on more than the size of assessment costs and the previous conclusions of empirical studies that have assumed such need to be re-examined. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.