Granivore abundance shapes mutualism quality in plant-scatterhoarder interactions.

Conditional mutualisms involve costs and benefits that vary with environmental factors, but mechanisms driving these dynamics remain poorly understood. Scatterhoarder-plant interactions are a prime example of this phenomenon, as scatterhoarders can either increase or reduce plant recruitment depending on the balance between seed dispersal and predation. We explored factors that drive the magnitude of net benefits for plants in this interaction using a mathematical model, with parameter values based on European beech (Fagus sylvatica) and yellow-necked mice (Apodemus flavicollis). We measured benefits as the percentage of germinating seeds, and examined how varying rodent survival (reflecting, e.g. changes in predation pressure), the rate of seed loss to other granivores, the abundance of alternative food resources, and changes in masting patterns affect the quality of mutualism. We found that increasing granivore abundance can degrade the quality of plant-scatterhoarder mutualism due to increased cache pilferage. Scatterhoarders are predicted to respond by increasing immediate consumption of gathered seeds, leading to higher costs and reduced benefits for plants. Thus, biotic changes that are detrimental to rodent populations can be beneficial for tree recruitment due to adaptive behavior of rodents. When scatterhoarder populations decline too drastically (< 5 individuals ha-1 ); however, tree recruitment may also suffer.

Within- and transgenerational stress legacy effects of ocean acidification on red abalone (Haliotis rufescens) growth and survival.

Understanding the mechanisms by which individual organisms respond and populations adapt to global climate change is a critical challenge. The role of plasticity and acclimation, within and across generations, may be essential given the pace of change. We investigated plasticity across generations and life stages in response to ocean acidification (OA), which poses a growing threat to both wild populations and the sustainable aquaculture of shellfish. Most studies of OA on shellfish focus on acute effects, and less is known regarding the longer term carryover effects that may manifest within or across generations. We assessed these longer term effects in red abalone (Haliotis rufescens) using a multi-generational split-brood experiment. We spawned adults raised in ambient conditions to create offspring that we then exposed to high pCO2 (1180 µatm; simulating OA) or low pCO2 (450 µatm; control or ambient conditions) during the first 3 months of life. We then allowed these animals to reach maturity in ambient common garden conditions for 4 years before returning the adults into high or low pCO2 treatments for 11 months and measuring growth and reproductive potential. Early-life exposure to OA in the F1 generation decreased adult growth rate even after 5 years especially when abalone were re-exposed to OA as adults. Adult but not early-life exposure to OA negatively impacted fecundity. We then exposed the F2 offspring to high or low pCO2 treatments for the first 3 months of life in a fully factorial, split-brood design. We found negative transgenerational effects of parental OA exposure on survival and growth of F2 offspring, in addition to significant direct effects of OA on F2 survival. These results show that the negative impacts of OA can last within and across generations, but that buffering against OA conditions at critical life-history windows can mitigate these effects.

Integrating sensory ecology and predator-prey theory to understand animal responses to fire.

Fire regimes are changing dramatically worldwide due to climate change, habitat conversion, and the suppression of Indigenous landscape management. Although there has been extensive work on plant responses to fire, including their adaptations to withstand fire and long-term effects of fire on plant communities, less is known about animal responses to fire. Ecologists lack a conceptual framework for understanding behavioural responses to fire, which can hinder wildlife conservation and management. Here, we integrate cue-response sensory ecology and predator-prey theory to predict and explain variation in if, when and how animals react to approaching fire. Inspired by the literature on prey responses to predation risk, this framework considers both fire-naïve and fire-adapted animals and follows three key steps: vigilance, cue detection and response. We draw from theory on vigilance tradeoffs, signal detection, speed-accuracy tradeoffs, fear generalization, neophobia and adaptive dispersal. We discuss how evolutionary history with fire, but also other selective pressures, such as predation risk, should influence animal behavioural responses to fire. We conclude by providing guidance for empiricists and outlining potential conservation applications.

Evolutionary History Mediates Population Response to Rapid Environmental Change through Within-Generational and Transgenerational Plasticity.

AbstractRapid environmental change is affecting many organisms; some are coping well, but many species are in decline. A key mechanism for facilitating success following environmental change is phenotypic plasticity. Organisms use cues to respond phenotypically to environmental conditions; many incorporate recent information (within-generation plasticity) and information from previous generations (transgenerational plasticity). We extend an existing evolutionary model where organisms utilize within-generational plasticity, transgenerational plasticity, and bet hedging to include changes in environmental regime. We show how when rapid evolution of plasticity is not possible, the effect of environmental change (altering the environment mean, variance, or autocorrelation or cue reliability) on population growth rate depends on the population's evolutionary history and past evolutionary responses to historical environmental conditions. We then evaluate the predictions that populations adapted to highly variable environments or with greater within-generational plasticity are more likely to successfully respond to environmental change. We identify when these predictions fail and show that environmental change is most detrimental when previously reliable cues become unreliable. When multiple cues become unreliable, environmental change can cause deleterious effects regardless of the population's evolutionary history. Overall, this work provides a general framework for understanding the role of plasticity in population responses to rapid environmental change.

Integrating animal behaviour into research on multiple environmental stressors: a conceptual framework.

While a large body of research has focused on the physiological effects of multiple environmental stressors, how behavioural and life-history plasticity mediate multiple-stressor effects remains underexplored. Behavioural plasticity can not only drive organism-level responses to stressors directly but can also mediate physiological responses. Here, we provide a conceptual framework incorporating four fundamental trade-offs that explicitly link animal behaviour to life-history-based pathways for energy allocation, shaping the impact of multiple stressors on fitness. We first address how small-scale behavioural changes can either mediate or drive conflicts between the effects of multiple stressors and alternative physiological responses. We then discuss how animal behaviour gives rise to three additional understudied and interrelated trade-offs: balancing the benefits and risks of obtaining the energy needed to cope with stressors, allocation of energy between life-history traits and stressor responses, and larger-scale escape from stressors in space or time via large-scale movement or dormancy. Finally, we outline how these trade-offs interactively affect fitness and qualitative ecological outcomes resulting from multiple stressors. Our framework suggests that explicitly considering animal behaviour should enrich our mechanistic understanding of stressor effects, help explain extensive context dependence observed in these effects, and highlight promising avenues for future empirical and theoretical research.

Fear generalization and behavioral responses to multiple dangers.

Animals often exhibit consistent-individual differences (CIDs) in boldness/fearfulness, typically studied in the context of predation risk. We focus here on fear generalization, where fear of one danger (e.g., predators) is correlated with fear of other dangers (e.g., humans, pathogens, moving vehicles, or fire). We discuss why fear generalization should be ecologically important, and why we expect fear to correlate across disparate dangers. CIDs in fear are well studied for some dangers in some taxa (e.g., human fear of pathogens), but not well studied for most dangers. Fear of some dangers has been found to correlate with general fearfulness, but some cases where we might expect correlated fears (e.g., between fear of humans, familiar predators, and exotic predators) are surprisingly understudied.

Local adaptation in the transgenerational response to copper pollution in the bryozoan Bugula neritina.

Transgenerational plasticity (TGP)-when a parent or previous generation's environmental experience affects offspring phenotype without involving a genetic change-can be an important mechanism allowing for rapid adaptation. However, despite increasing numbers of empirical examples of TGP, there appears to be considerable variation in its strength and direction, yet limited understanding of what causes this variation. We compared patterns of TGP in response to stress across two populations with high versus low historical levels of stress exposure. Specifically, we expected that exposure to acute stress in the population experiencing historically high levels of stress would result in adaptive TGP or alternatively fixed tolerance (no parental effect), whereas the population with low levels of historical exposure would result in negative parental carryover effects. Using a common sessile marine invertebrate, Bugula neritina, and a split brood design, we exposed parents from both populations to copper or control treatments in the laboratory and then had them brood copper-naïve larvae. We then exposed half of each larval brood to copper and half to control conditions before allowing them to grow to maturity in the field. Maternal copper exposure had a strong negative carryover effect on adult offspring growth and survival in the population without historical exposure, especially when larvae themselves were exposed to copper. We found little to no maternal or offspring treatment effect on adult growth and survival in the population with a history of copper exposure. However, parents from this population produced larger larvae on average and were able to increase the size of their larvae in response to copper exposure, providing a potential mechanism for maintaining fitness and suggesting TGP through maternal provisioning. These results indicate that the ability to adjust offspring phenotype via TGP may be a locally adapted trait and potentially influenced by past patterns of exposure.

Biological invasions as a selective filter driving behavioral divergence.

Biological invasions are a multi-stage process (i.e., transport, introduction, establishment, spread), with each stage potentially acting as a selective filter on traits associated with invasion success. Behavior (e.g., exploration, activity, boldness) plays a key role in facilitating species introductions, but whether invasion acts as a selective filter on such traits is not well known. Here we capitalize on the well-characterized introduction of an invasive lizard (Lampropholis delicata) across three independent lineages throughout the Pacific, and show that invasion shifted behavioral trait means and reduced among-individual variation-two key predictions of the selective filter hypothesis. Moreover, lizards from all three invasive ranges were also more behaviorally plastic (i.e., greater within-individual variation) than their native range counterparts. We provide support for the importance of selective filtering of behavioral traits in a widespread invasion. Given that invasive species are a leading driver of global biodiversity loss, understanding how invasion selects for specific behaviors is critical for improving predictions of the effects of alien species on invaded communities.

Behavioral plasticity can facilitate evolution in urban environments.

Plasticity-led evolution is central to evolutionary theory. Although challenging to study in nature, this process may be particularly apparent in novel environments such as cities. We document abundant evidence of plastic behavioral changes in urban animals, including learning, contextual, developmental, and transgenerational plasticities. Using behavioral drive as a conceptual framework, our analysis of notable case studies suggests that plastic behaviors, such as altered habitat use, migration, diurnal and seasonal activity, and courtship, can have faciliatory and cascading effects on urban evolution via spatial, temporal, and mate-choice mechanisms. Our findings highlight (i) the need to incorporate behavioral plasticity more formally into urban evolutionary research and (ii) the opportunity provided by urban environments to study behavioral mechanisms of plasticity-led processes.

Social context mediates the expression of a personality trait in a gregarious lizard.

The social environment is a key factor that influences behavioural traits across a wide array of species. Yet, when investigating individual differences in behaviour, studies tend to measure animals in isolation from other conspecifics-even in social species. Surprisingly, whether behavioural traits measured in isolation are predictive of individual-level behaviour when in social groups is still poorly understood. Here, we repeatedly measured risk-taking behaviour (i.e. boldness; 741 total trials) in both the presence and absence of conspecifics in a social lizard, the delicate skink (Lampropholis delicata). Further, we manipulated food availability during group trials to test whether the effect of the social environment on risk-taking behaviour was mediated by competition over resources. Using 105 lizards collected from three independent populations, we found that individual risk-taking behaviour was repeatable when measured in either social isolation or within groups both with and without food resources available. However, lizards that were bolder during individual trials were not also bolder when in groups, regardless of resource availability. This was largely driven by individual differences in social behavioural plasticity, whereby individual skinks responded differently to the presence of conspecifics. Together, this resulted in a rank order change of individual behavioural types across the social conditions. Our results highlight the importance of the social environment in mediating animal personality traits across varying levels of resource availability. Further, these findings suggest that behavioural traits when measured in isolation, may not reflect individual variation in behaviour when measured in more ecologically realistic social groups.

Frontiers in quantifying wildlife behavioural responses to chemical pollution.

Animal behaviour is remarkably sensitive to disruption by chemical pollution, with widespread implications for ecological and evolutionary processes in contaminated wildlife populations. However, conventional approaches applied to study the impacts of chemical pollutants on wildlife behaviour seldom address the complexity of natural environments in which contamination occurs. The aim of this review is to guide the rapidly developing field of behavioural ecotoxicology towards increased environmental realism, ecological complexity, and mechanistic understanding. We identify research areas in ecology that to date have been largely overlooked within behavioural ecotoxicology but which promise to yield valuable insights, including within- and among-individual variation, social networks and collective behaviour, and multi-stressor interactions. Further, we feature methodological and technological innovations that enable the collection of data on pollutant-induced behavioural changes at an unprecedented resolution and scale in the laboratory and the field. In an era of rapid environmental change, there is an urgent need to advance our understanding of the real-world impacts of chemical pollution on wildlife behaviour. This review therefore provides a roadmap of the major outstanding questions in behavioural ecotoxicology and highlights the need for increased cross-talk with other disciplines in order to find the answers.

Personality, spatiotemporal ecological variation and resident/explorer movement syndromes in the sleepy lizard.

Individual variation in movement is profoundly important for fitness and offers key insights into the spatial and temporal dynamics of populations and communities. Nonetheless, individual variation in fine-scale movement behaviours is rarely examined even though animal tracking devices offer the long-term, high-resolution, repeatable data in natural conditions that are ideal for studying this variation. Furthermore, of the few studies that consider individual variation in movement, even fewer also consider the internal traits and environmental factors that drive movement behaviour which are necessary for contextualising individual differences in movement patterns. In this study, we GPS tracked a free-ranging population of sleepy lizards Tiliqua rugosa, each Austral spring over 5 years to examine consistent among-individual variation in movement patterns, as well as how these differences were mediated by key internal and ecological factors. We found that individuals consistently differed in a suite of weekly movement traits, and that these traits strongly covaried among-individuals, forming movement syndromes. Lizards fell on a primary movement continuum, from 'residents' that spent extended periods of time residing within smaller core areas of their home range, to 'explorers' that moved greater distances and explored vaster areas of the environment. Importantly, we also found that these consistent differences in lizard movement were related to two ecologically important animal personality traits (boldness and aggression), their sex, key features of the environment (including food availability, and a key water resource), habitat type and seasonal variation (cool/moist vs. hot/drier) in environmental conditions. Broadly, these movement specialisations likely reflect variation in life-history tactics including foraging and mating tactics that ultimately underlie key differences in space use. Such information can be used to connect phenotypic population structure to key ecological and evolutionary processes, for example social networks and disease-transmission pathways, further highlighting the value of examining individual variation in movement behaviour.

Enhancing the ecological realism of evolutionary mismatch theory.

Following rapid environmental change, why do some animals thrive, while others struggle? We present an expanded, cue-response framework for predicting variation in behavioral responses to novel situations. We show how signal detection theory can be used when individuals have three behavioral options (approach, avoid, or ignore). Based on this theory, we outline predictions about which animals are more likely to make mistakes around novel conditions (i.e., fall for a trap or fail to use an undervalued resource) and the intensity of that mismatch (i.e., severe versus moderate). Explicitly considering three options provides a more holistic perspective and allows us to distinguish between severe and moderate traps, which could guide management strategies in a changing world.

Mast seeding promotes evolution of scatter-hoarding.

Many plant species worldwide are dispersed by scatter-hoarding granivores: animals that hide seeds in numerous, small caches for future consumption. Yet, the evolution of scatter-hoarding is difficult to explain because undefended caches are at high risk of pilferage. Previous models have attempted to solve this problem by giving cache owners large advantages in cache recovery, by kin selection, or by introducing reciprocal pilferage of 'shared' seed resources. However, the role of environmental variability has been so far overlooked in this context. One important form of such variability is masting, which is displayed by many plant species dispersed by scatterhoarders. We use a mathematical model to investigate the influence of masting on the evolution of scatter-hoarding. The model accounts for periodically varying annual seed fall, caching and pilfering behaviour, and the demography of scatterhoarders. The parameter values are based mostly on research on European beech (Fagus sylvatica) and yellow-necked mice (Apodemus flavicollis). Starvation of scatterhoarders between mast years decreases the population density that enters masting events, which leads to reduced seed pilferage. Satiation of scatterhoarders during mast events lowers the reproductive cost of caching (i.e. the cost of caching for the future rather than using seeds for current reproduction). These reductions promote the evolution of scatter-hoarding behaviour especially when interannual variation in seed fall and the period between masting events are large. This article is part of the theme issue 'The ecology and evolution of synchronized seed production in plants'.

Andrew Sih.

Interview with Andrew Sih, who studies the evolution and ecological impacts of behavior on population patterns at the University of California, Davis.

Early life experience influences dispersal in coyotes (Canis latrans).

Natal dispersal plays an important role in connecting individual animal behavior with ecological processes at all levels of biological organization. As urban environments are rapidly increasing in extent and intensity, understanding how urbanization influences these long distance movements is critical for predicting the persistence of species and communities. There is considerable variation in the movement responses of individuals within a species, some of which is attributed to behavioral plasticity which interacts with experience to produce interindividual differences in behavior. For natal dispersers, much of this experience occurs in the natal home range. Using data collected from VHF collared coyotes (Canis latrans) in the Chicago Metropolitan Area we explored the relationship between early life experience with urbanization and departure, transience, and settlement behavior. Additionally, we looked at how early life experience with urbanization influenced survival to adulthood and the likelihood of experiencing a vehicle related mortality. We found that coyotes with more developed habitat in their natal home range were more likely to disperse and tended to disperse farther than individuals with more natural habitat in their natal home range. Interestingly, our analysis produced mixed results for the relationship between natal habitat and habitat selection during settlement. Finally, we found no evidence that early life experience with urbanization influenced survival to adulthood or the likelihood of experiencing vehicular mortality. Our study provides evidence that early life exposure influences dispersal behavior; however, it remains unclear how these differences ultimately affect fitness.

Host traits, identity, and ecological conditions predict consistent flea abundance and prevalence on free-living California ground squirrels.

Understanding why some individuals are more prone to carry parasites and spread diseases than others is a key question in biology. Although epidemiologists and disease ecologists increasingly recognize that individuals of the same species can vary tremendously in their relative contributions to the emergence of diseases, very few empirical studies systematically assess consistent individual differences in parasite loads within populations over time. Two species of fleas (Oropsylla montana and Hoplopsyllus anomalous) and their hosts, California ground squirrels (Otospermophilus beecheyi), form a major complex for amplifying epizootic plague in the western United States. Understanding its biology is primarily of major ecological importance and is also relevant to public health. Here, we capitalize on a long-term data set to explain flea incidence on California ground squirrels at Briones Regional Park in Contra Costa County, USA. In a 7 year study, we detected 42,358 fleas from 2,759 live trapping events involving 803 unique squirrels from two free-living populations that differed in the amount of human disturbance in those areas. In general, fleas were most abundant and prevalent on adult males, on heavy squirrels, and at the pristine site, but flea distributions varied among years, with seasonal conditions (e.g., temperature, rainfall, humidity), temporally within summers, and between flea species. Although on-host abundances of the two flea species were positively correlated, each flea species occupied a distinctive ecological niche. The common flea (O. montana) occurred primarily on adults in cool, moist conditions in early summer whereas the rare flea (H. anomalous) was mainly on juveniles in hot, dry conditions in late summer. Beyond this, we uncovered significantly repeatable and persistent effects of host individual identity on flea loads, finding consistent individual differences among hosts in all parasite measures. Taken together, we reveal multiple determinants of parasites on free-living mammals, including the underappreciated potential for host heterogeneity - within populations - to structure the emergence of zoonotic diseases such as bubonic plague.

Bugs scaring bugs: enemy-risk effects in biological control systems.

Enemy-risk effects, often referred to as non-consumptive effects (NCEs), are an important feature of predator-prey ecology, but their significance has had little impact on the conceptual underpinning or practice of biological control. We provide an overview of enemy-risk effects in predator-prey interactions, discuss ways in which risk effects may impact biocontrol programs and suggest avenues for further integration of natural enemy ecology and integrated pest management. Enemy-risk effects can have important influences on different stages of biological control programs, including natural enemy selection, efficacy testing and quantification of non-target impacts. Enemy-risk effects can also shape the interactions of biological control with other pest management practices. Biocontrol systems also provide community ecologists with some of the richest examples of behaviourally mediated trophic cascades and demonstrations of how enemy-risk effects play out among species with no shared evolutionary history, important topics for invasion biology and conservation. We conclude that the longstanding use of ecological theory by biocontrol practitioners should be expanded to incorporate enemy-risk effects, and that community ecologists will find many opportunities to study enemy-risk effects in biocontrol settings.