Collective signalling is shaped by feedbacks between signaller variation, receiver perception and acoustic environment in a simulated communication network.

Communication takes place within a network of multiple signallers and receivers. Social network analysis provides tools to quantify how an individual's social positioning affects group dynamics and the subsequent biological consequences. However, network analysis is rarely applied to animal communication, likely due to the logistical difficulties of monitoring natural communication networks. We generated a simulated communication network to investigate how variation in individual communication behaviours generates network effects, and how this communication network's structure feeds back to affect future signalling interactions. We simulated competitive acoustic signalling interactions among chorusing individuals and varied several parameters related to communication and chorus size to examine their effects on calling output and social connections. Larger choruses had higher noise levels, and this reduced network density and altered the relationships between individual traits and communication network position. Hearing sensitivity interacted with chorus size to affect both individuals' positions in the network and the acoustic output of the chorus. Physical proximity to competitors influenced signalling, but a distinctive communication network structure emerged when signal active space was limited. Our model raises novel predictions about communication networks that could be tested experimentally and identifies aspects of information processing in complex environments that remain to be investigated. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Maternal effects, paternal effects, and their interactions in the freshwater snail Physa acuta.

Individuals exposed to predation risk can produce offspring with altered phenotypes. Most work on predation-induced parental effects has focused on maternal effects or on generalized parental effects where both parents are exposed to risk. We conducted an experiment to measure and compare maternal and paternal effects on offspring phenotypes and test for interactions in those effects. We exposed 82 snails from 22 lines to control or predator cues and created line dyads with the four possible mating pairings of control and predator cue exposed individuals. We measured the resulting body masses, shell masses, shell shapes, and anti-predator behaviors of the offspring. We found some evidence that offspring were larger and heavier when the mother was exposed to predation cues, but that this effect was negated when the father was also exposed. The mass of offspring shells relative to their total mass was unaffected by parental treatments. Shell shape was marginally affected by maternal treatment, but not paternal treatment. Behavioral responses to cues were not affected by maternal or paternal treatments. Our results suggest potential conflict between male and female parental effects and highlight the importance of examining the interactions of maternal and paternal effects.

Bison movements change with weather: Implications for their continued conservation in the Anthropocene.

Animal movement patterns are affected by complex interactions between biotic and abiotic landscape conditions, and these patterns are being altered by weather variability associated with a changing climate. Some animals, like the American plains bison (Bison bison L.; hereafter, plains bison), are considered keystone species, thus their response to weather variability may alter ecosystem structure and biodiversity patterns. Many movement studies of plains bison and other ungulates have focused on point-pattern analyses (e.g., resource-selection) that have provided information about where these animals move, but information about when or why these animals move is limited. For example, information surrounding the influence of weather on plains bison movement in response to weather is limited but has important implications for their conservation in a changing climate. To explore how movement distance is affected by weather patterns and drought, we utilized 12-min GPS data from two of the largest plains bison herds in North America to model their response to weather and drought parameters using generalized additive mixed models. Distance moved was best predicted by air temperature, wind speed, and rainfall. However, air temperature best explained the variation in distance moved compared to any other single parameter we measured, predicting a 48% decrease in movement rates above 28°C. Moreover, severe drought (as indicated by 25-cm depth soil moisture) better predicted movement distance than moderate drought. The strong influence of weather and drought on plains bison movements observed in our study suggest that shifting climate and weather will likely affect plains bison movement patterns, further complicating conservation efforts for this wide-ranging keystone species. Moreover, changes in plains bison movement patterns may have cascading effects for grassland ecosystem structure, function, and biodiversity. Plains bison and grassland conservation efforts need to be proactive and adaptive when considering the implications of a changing climate on bison movement patterns.

Optimal hormonal regulation when stressor cues are imperfect.

The endocrine system uses information about the environment and the individual's state to regulate circulating concentrations of hormones, and then those hormones, through receptor binding, cause changes in the phenotype. How quickly individuals can up- and down-regulate their hormones can affect baseline and elevated hormone levels and presumably affects how successfully individuals can cope with a varying environment. To respond to environmental change, individuals first need to perceive and process cues about the state of the environment. Individuals may receive imperfect cues about the environment due to perceptual errors, variation in cues, or inexperience with novel stressors. In this paper we use a mathematical model to ask how these imperfect cues should affect how individuals regulate their glucocorticoid concentrations. We find imperfect cues can lead to changes in hormone regulation with individuals generally having higher baseline and lower elevated hormone levels as environmental cues become less reliable. Informational constraints and physiological constraints appear to have generally additive effects, with informational constraints having less of an impact as physiological constraints increase. Our results highlight the different means by which imperfect information can affect hormone regulation. We find that mistakes caused by imperfect cues are commonly responsible for changes in average hormone levels, but imperfect cues also cause individuals to be slower and less certain in their updated estimates of the environmental state, which affects hormone regulation. We also demonstrate the separate effects of false positive and false negative cues and how these are shaped by the relative fitness consequences of baseline and stress-induced hormone levels. Our model shows how given our assumptions imperfect stressor cues should affect endocrine flexibility and regulation, and we hope provides a piece for future conversations and models of endocrine regulation.

Integrating theoretical and empirical approaches for a robust understanding of endocrine flexibility.

There is growing interest in studying hormones beyond single 'snapshot' measurements, as recognition that individual variation in the endocrine response to environmental change may underlie many rapid, coordinated phenotypic changes. Repeated measures of hormone levels in individuals provide additional insight into individual variation in endocrine flexibility - that is, how individuals modulate hormone levels in response to the environment. The ability to quickly and appropriately modify phenotype is predicted to be favored by selection, especially in unpredictable environments. The need for repeated samples from individuals can make empirical studies of endocrine flexibility logistically challenging, but methods based in mathematical modeling can provide insights that circumvent these challenges. Our Review introduces and defines endocrine flexibility, reviews existing studies, makes suggestions for future empirical work, and recommends mathematical modeling approaches to complement empirical work and significantly advance our understanding. Mathematical modeling is not yet widely employed in endocrinology, but can be used to identify innovative areas for future research and generate novel predictions for empirical testing.

Mathematical modeling reveals how the speed of endocrine regulation should affect baseline and stress-induced glucocorticoid levels.

Unpredictable environmental changes displace individuals from homeostasis and elicit a stress response. In vertebrates, the stress response is mediated mainly by glucocorticoids (GCs) which initiate physiological changes while minimizing allostatic overload. Individuals and species vary consistently in baseline and stress-induced GC levels and the speed with which GC levels can be upregulated or downregulated, but the extent to which variation in hormone regulation influences baseline and stress-induced GC levels is unclear. Using mathematical modeling, we tested how GC regulation rate, frequencies and durations of acute stressors, fitness functions, and allostatic overload affect GC levels during control and acute stress periods. As GC regulation rate slows, baseline and acute stress-induced GC levels become more similar. When the speed of up- and downregulation decreased, hormone levels became more linked to anticipated future conditions to avoid fitness costs of mismatching a new environmental state. More frequent acute stressors caused baseline and acute stress-induced GC levels to converge. When fitness was more tightly linked to hormone levels during acute stress periods than during control states, the speed of upregulation influenced optimal hormone levels more than the downregulation rate. With allostatic overload costs included, predicted GC levels were lower and more dependent on the frequency of past acute stressors. Our results show the value of optimality modeling to study the hormonal response to stressors and suggest GC levels depend on past and anticipated future environmental states as well as individual differences in hormone regulation.

Stress hormone-mediated antipredator morphology improves escape performance in amphibian tadpoles.

Complete functional descriptions of the induction sequences of phenotypically plastic traits (perception to physiological regulation to response to outcome) should help us to clarify how plastic responses develop and operate. Ranid tadpoles express several plastic antipredator traits mediated by the stress hormone corticosterone, but how they influence outcomes remains uncertain. We investigated how predator-induced changes in the tail morphology of wood frog (Rana sylvatica) tadpoles influenced their escape performance over a sequence of time points when attacked by larval dragonflies (Anax junius). Tadpoles were raised with no predator exposure, chemical cues of dragonflies added once per day, or constant exposure to caged dragonflies crossed with no exogenous hormone added (vehicle control only), exogenous corticosterone, or metyrapone (a corticosteroid synthesis inhibitor). During predation trials, we detected no differences after four days, but after eight days, tadpoles exposed to larval dragonflies and exogenous corticosterone had developed deeper tail muscles and exhibited improved escape performance compared to controls. Treatment with metyrapone blocked the development of a deeper tail muscle and resulted in no difference in escape success. Our findings further link the predator-induced physiological stress response of ranid tadpoles to the development of an antipredator tail morphology that confers performance benefits.

Effects of pyric herbivory on prairie-chicken (Tympanuchus spp) habitat.

The reduction and simplification of grasslands has led to the decline of numerous species of grassland fauna, particularly grassland-obligate birds. Prairie-chickens (Tympanuchus spp.) are an example of obligate grassland birds that have declined throughout most of their distribution and are species of conservation concern. Pyric herbivory has been suggested as a land management strategy for enhancing prairie-chicken habitat and stabilizing declining population trends. We assessed differences in vegetation structure created by pyric herbivory compared to fire-only treatments to determine whether pyric herbivory increased habitat heterogeneity for prairie-chickens, spatially or temporally. Our study was performed at four sites in the southern Great Plains, all within the current or historic distribution of either lesser (T. pallidicinctus), greater (T. cupido), or Attwater's (T. cupido attwateri) prairie-chickens. Key vegetation characteristics of grass cover and vegetation height in pyric herbivory and fire-only treatments were within the recommended range of values for prairie-chickens during their distinct life history stages. However, patches managed via pyric herbivory provided approximately 5% more forb cover than fire-only treatments for almost 30 months post-fire. Additionally, pyric herbivory extended the length of time bare ground was present after fires. Pyric herbivory also reduced vegetation height and biomass, with mean vegetation height in pyric herbivory treatments lagging behind fire-only treatments by approximately 15 months. Canopy cover in fire-only treatments exceeded levels recommended for prairie-chicken young within 12 months post-fire. However, canopy cover in pyric herbivory treatments never exceeded the maximum recommended levels. Overall, it appears that pyric herbivory improves vegetation characteristics reported as critical to prairie-chicken reproduction. Based on our results, we suggest pyric herbivory as a viable management technique to promote prairie-chicken habitat in the southern Great Plains, while still accommodating livestock production.

Safety Cues Can Give Prey More Valuable Information Than Danger Cues.

The ability of prey to assess predation risk is fundamental to their success. It is routinely assumed that predator cues do not vary in reliability across levels of predation risk. We propose that cues can differ in how precisely they indicate different levels of predation risk. What we call danger cues precisely indicate high risk levels, while safety cues precisely indicate low risk levels. Using optimality modeling, we find that prey fitness is increased when prey pay more attention to safety cues than to danger cues. This fitness advantage is greater when prey need to protect assets, predators are more dangerous, or predation risk increases at an accelerating rate with prey foraging efforts. Each of these conditions lead to prey foraging less when estimated predation risk is higher. Danger cues have less value than safety cues because they give precise information about risk when it is high, but prey behavior varies little when risk is high. Safety cues give precise information about levels of risk where prey behavior varies. These results highlight how our fascination with predators may have biased the way that we study predator-prey interactions and focused too exclusively on cues that clearly indicate the presence of predator rather than cues that clearly indicate their absence.

Transgenerational Plasticity in Human-Altered Environments.

Our ability to predict how species will respond to human-induced rapid environmental change (HIREC) may depend upon our understanding of transgenerational plasticity (TGP), which occurs when environments experienced by previous generations influence phenotypes of subsequent generations. TGP evolved to help organisms cope with environmental stressors when parental environments are highly predictive of offspring environments. HIREC can alter conditions that favored TGP in historical environments by reducing parents' ability to detect environmental conditions, disrupting previous correlations between parental and offspring environments, and interfering with the transmission of parental cues to offspring. Because of the propensity to produce errors in these processes, TGP will likely generate negative fitness outcomes in response to HIREC, though beneficial fitness outcomes may occur in some cases.

Allometry and morphometrics of clypeal membrane size and shape in Nicrophorus (Coleoptera: Silphidae).

Contests between same-sex opponents over resources necessary for reproduction, as well interactions used to discern mate quality, often involve exaggerated traits wherein large individuals have disproportionately larger traits. This positive allometric scaling of weapons or signals facilitates communication during social interactions by accentuating body size differences between individuals. Typically, males carry these exaggerated traits, as males must compete over limited female gametes. However, in Nicrophorus beetles both males and females engage in physical contests over the vertebrate carcasses they need to provision and raise offspring. Male and female Nicrophorus beetles have extended clypeal membranes directly above their mandibles, which could serve as signals. We investigated the scaling relationships between clypeal membrane size and shape and body size for five species of North American burying beetle to determine whether clypeal membranes contain exaggerated body size information. We found that clypeal membranes for both sexes of all species scaled positively with body size (slope > 1). Three of the five species also displayed sexual dimorphism in aspects of clypeal membrane size and shape allometry despite lack of dimorphism in body size. In two dimorphic species, small male clypeal membranes were statistically indistinguishable from the female form. We conclude that colored clypeal membranes in Nicrophorus beetles do contain exaggerated body size information. Observed patterns of dimorphism suggest that males sometimes experience stronger selection on marking size and shape, which might be explained by life history differences among species.

Re-examining the Causes and Meaning of the Risk Allocation Hypothesis.

The risk allocation hypothesis has inspired numerous studies seeking to understand how temporal variation in predation risk affects prey foraging behavior, but there has been debate about its generality and causes. I examined how imperfect information affects its predictions and sought to clarify the causes of the predicted patterns. I first confirmed that my modeling approach-given a threshold or linear fitness function-produced the risk allocation prediction that prey increase their foraging efforts during low and high risk as the proportion of high-risk periods increases. However, the causes of this result and its robustness differed for the two fitness functions. When prey that had evolved to use perfect information received imperfect information, risk allocation was reduced. However, prey that evolved to use imperfect information in some cases reversed the risk allocation prediction. The model also showed that risk allocation occurs even when prey have no knowledge that the proportions of low- and high-risk periods have changed. I conclude that risk allocation is largely not driven by prey expectations about future states of the environment but rather by the prey's current energetic state and time remaining. I discuss the consequences for experimental design and explanations for empirical results.

Comparisons of discrete and integrative sampling accuracy in estimating pulsed aquatic exposures.

Most current-use pesticides have short half-lives in the water column and thus the most relevant exposure scenarios for many aquatic organisms are pulsed exposures. Quantifying exposure using discrete water samples may not be accurate as few studies are able to sample frequently enough to accurately determine time-weighted average (TWA) concentrations of short aquatic exposures. Integrative sampling methods that continuously sample freely dissolved contaminants over time intervals (such as integrative passive samplers) have been demonstrated to be a promising measurement technique. We conducted several modeling scenarios to test the assumption that integrative methods may require many less samples for accurate estimation of peak 96-h TWA concentrations. We compared the accuracies of discrete point samples and integrative samples while varying sampling frequencies and a range of contaminant water half-lives (t50 = 0.5, 2, and 8 d). Differences the predictive accuracy of discrete point samples and integrative samples were greatest at low sampling frequencies. For example, when the half-life was 0.5 d, discrete point samples required 7 sampling events to ensure median values > 50% and no sampling events reporting highly inaccurate results (defined as < 10% of the true 96-h TWA). Across all water half-lives investigated, integrative sampling only required two samples to prevent highly inaccurate results and measurements resulting in median values > 50% of the true concentration. Regardless, the need for integrative sampling diminished as water half-life increased. For an 8-d water half-life, two discrete samples produced accurate estimates and median values greater than those obtained for two integrative samples. Overall, integrative methods are the more accurate method for monitoring contaminants with short water half-lives due to reduced frequency of extreme values, especially with uncertainties around the timing of pulsed events. However, the acceptability of discrete sampling methods for providing accurate concentration measurements increases with increasing aquatic half-lives.

How the informational environment shapes how prey estimate predation risk and the resulting indirect effects of predators.

Prey often behaviorally respond to changes in the intensity of predation risk, and these responses can often significantly shape community dynamics, but flexible responses to changes in predation risk require that prey have accurate and timely estimates of predation risk. We present a model of how a prey's environment should shape the cognitive rules they use to assess predation risk and present how these rules shape the effects predators have on prey and the prey's resources. In the model, prey can rely on a combination of a fixed estimate of predation risk and a flexible estimate of predation risk shaped by their recent experience. Prey relied more on their experience to estimate predation risk when predator cues were more reliable and when predator densities were lower. In addition, when the prey cognitive rules favored a greater use of their experience to estimate predation risk, the presence of predators caused larger nonconsumptive effects and generally smaller consumptive effects on prey and the prey's resources. These differences in prey cognition also altered the effects that alterations of cue reliability and predator densities had on prey and their resources.

The effects of variable predation risk on foraging and growth: less risk is not necessarily better.

There is strong evidence that the way prey respond to predation risk can be fundamentally important to the structuring and functioning of natural ecosystems. The majority of work on such nonconsumptive predator effects (NCEs) has examined prey responses under constant risk or constant safety. Hence, the importance of temporal variation in predation risk, which is ubiquitous in natural systems, has received limited empirical attention. In addition, tests of theory (e.g., the risk allocation hypothesis) on how prey allocate risk have relied almost exclusively on the behavioral responses of prey to variation in risk. In this study, we examined how temporal variation in predation risk affected NCEs on prey foraging and growth. We found that high risk, when predictable, was just as energetically favorable to prey as safe environments that are occasionally pulsed by risk. This pattern emerged because even episodic pulses of risk in otherwise safe environments led to strong NCEs on both foraging and growth. However, NCEs more strongly affected growth than foraging, and we suggest that such effects on growth are most important to how prey ultimately allocate risk. Hence, exclusive focus on behavioral responses to risk will likely provide an incomplete understanding of how NCEs shape individual fitness and the dynamics of ecological communities.

Risk, resources and state-dependent adaptive behavioural syndromes.

Many animals exhibit behavioural syndromes-consistent individual differences in behaviour across two or more contexts or situations. Here, we present adaptive, state-dependent mathematical models for analysing issues about behavioural syndromes. We find that asset protection (where individuals with more 'assets' tend be more cautious) and starvation avoidance, two state-dependent mechanisms, can explain short-term behavioural consistency, but not long-term stable behavioural types (BTs). These negative-feedback mechanisms tend to produce convergence in state and behaviour over time. In contrast, a positive-feedback mechanism, state-dependent safety (where individuals with higher energy reserves, size, condition or vigour are better at coping with predators), can explain stable differences in personality over the long term. The relative importance of negative- and positive-feedback mechanisms in governing behavioural consistency depends on environmental conditions (predation risk and resource availability). Behavioural syndromes emerge more readily in conditions of intermediate ecological favourability (e.g. medium risk and medium resources, or high risk and resources, or low risk and resources). Under these conditions, individuals with higher initial state maintain a tendency to be bolder than individuals that start with low initial state; i.e. later BT is determined by state during an early 'developmental window'. In contrast, when conditions are highly favourable (low risk, high resources) or highly unfavourable (high risk, low resources), individuals converge to be all relatively bold or all relatively cautious, respectively. In those circumstances, initial differences in BT are not maintained over the long term, and there is no early developmental window where initial state governs later BT. The exact range of ecological conditions favouring behavioural syndromes depends also on the strength of state-dependent safety.

Effects of survival on the attractiveness of cues to natal dispersers.

Habitat selection by natal dispersers is one of several contexts in which preexisting biases interact with experience to affect the attractiveness of cues from biologically significant items. Here we use a Bayesian approach to explore the conditions that favor this phenomenon. We demonstrate that the simplest possible type of natal experience--namely, survival to the age/stage of dispersal--can increase the attractiveness of cues from an individual's natal habitat relative to the attractiveness of those same cues to naive individuals. The effects of survivorship on cue attractiveness are strongest when the quality of the habitat that produces that cue varies widely across large spatial or temporal scales, when that type of habitat is rarely of high quality, and when offspring survivorship provides a reliable indication of the quality of that type of habitat at the current time and locality. More generally, the framework outlined here may also apply to other situations in which extended exposure to cues early in life increases the attractiveness of those cues later in life.

Revisiting the classics: considering nonconsumptive effects in textbook examples of predator-prey interactions.

Predator effects on prey dynamics are conventionally studied by measuring changes in prey abundance attributed to consumption by predators. We revisit four classic examples of predator-prey systems often cited in textbooks and incorporate subsequent studies of nonconsumptive effects of predators (NCE), defined as changes in prey traits (e.g., behavior, growth, development) measured on an ecological time scale. Our review revealed that NCE were integral to explaining lynx-hare population dynamics in boreal forests, cascading effects of top predators in Wisconsin lakes, and cascading effects of killer whales and sea otters on kelp forests in nearshore marine habitats. The relative roles of consumption and NCE of wolves on moose and consequent indirect effects on plant communities of Isle Royale depended on climate oscillations. Nonconsumptive effects have not been explicitly tested to explain the link between planktonic alewives and the size structure of the zooplankton, nor have they been invoked to attribute keystone predator status in intertidal communities or elsewhere. We argue that both consumption and intimidation contribute to the total effects of keystone predators, and that characteristics of keystone consumers may differ from those of predators having predominantly NCE. Nonconsumptive effects are often considered as an afterthought to explain observations inconsistent with consumption-based theory. Consequently, NCE with the same sign as consumptive effects may be overlooked, even though they can affect the magnitude, rate, or scale of a prey response to predation and can have important management or conservation implications. Nonconsumptive effects may underlie other classic paradigms in ecology, such as delayed density dependence and predator-mediated prey coexistence. Revisiting classic studies enriches our understanding of predator-prey dynamics and provides compelling rationale for ramping up efforts to consider how NCE affect traditional predator-prey models based on consumption, and to compare the relative magnitude of consumptive and NCE of predators.

Evolution of animal personalities.

Wolf et al. propose a model to explain the existence of animal personalities, consistent with behavioural differences among individuals in various contexts--their explanation is counter-intuitive and cogent. However, all models have their limits, and the particular life-history requirements of this one may be unclear. Here we analyse their model and clarify its organismal scope.

Predator and prey space use: dragonflies and tadpoles in an interactive game.

Predator and prey spatial distributions have important population and community level consequences. However, little is known either theoretically or empirically about behavioral mechanisms that underlie the spatial patterns that emerge when predators and prey freely interact. We examined the joint space use and behavioral rules governing movement of freely interacting groups of odonate (dragonfly) predators and two size classes of anuran (tadpole) prey in arenas containing two patches with different levels of the prey's resource. Predator and prey movement and space use was quantified both when they were apart and together. When apart from predators, large tadpoles strongly preferred the high resource patch. When apart from prey, dragonflies weakly preferred the high resource patch. When together, large prey shifted to a uniform distribution, while predators strongly preferred the high resource patch. These patterns qualitatively fit the predictions of several three trophic level, ideal free distribution models. In contrast, the space use of small prey and predators did not deviate from uniform. Three measures of joint space use (spatial correlations, overlap, and co-occurrence) concurred in suggesting that prey avoidance of predators was more important than predator attraction to prey in determining overall spatial patterns. To gain additional insight into behavioral mechanisms, we used a model selection approach to identify behavioral movement rules that can potentially explain the observed, emergent patterns of space use. Prey were more likely to leave patches with more predators and more conspecific competitors; resources had relatively weak effects on prey movements. In contrast, predators were more likely to leave patches with low resources (that they do not consume) and more competing predators; prey had relatively little effect on predator movements. These results highlight the importance of investigating freely interacting predators and prey, the potential for simple game theory models to predict joint spatial distributions, and the utility of using model choice methods to identify potential key factors that govern movement.