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.

Wild animals suppress the spread of socially transmitted misinformation.

Understanding the mechanisms by which information and misinformation spread through groups of individual actors is essential to the prediction of phenomena ranging from coordinated group behaviors to misinformation epidemics. Transmission of information through groups depends on the rules that individuals use to transform the perceived actions of others into their own behaviors. Because it is often not possible to directly infer decision-making strategies in situ, most studies of behavioral spread assume that individuals make decisions by pooling or averaging the actions or behavioral states of neighbors. However, whether individuals may instead adopt more sophisticated strategies that exploit socially transmitted information, while remaining robust to misinformation, is unknown. Here, we study the relationship between individual decision-making and misinformation spread in groups of wild coral reef fish, where misinformation occurs in the form of false alarms that can spread contagiously through groups. Using automated visual field reconstruction of wild animals, we infer the precise sequences of socially transmitted visual stimuli perceived by individuals during decision-making. Our analysis reveals a feature of decision-making essential for controlling misinformation spread: dynamic adjustments in sensitivity to socially transmitted cues. This form of dynamic gain control can be achieved by a simple and biologically widespread decision-making circuit, and it renders individual behavior robust to natural fluctuations in misinformation exposure.

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.

Belonging in STEM: an interactive, iterative approach to create and maintain a diverse learning community.

Diversity is a key driver of scientific innovation, yet fields in science, technology, engineering, and mathematics (STEM) have struggled to retain diverse communities. Research suggests that fostering a sense of belonging is critical for retaining diversity. We propose an iterative process that aims to improve sense of belonging among laboratory (lab) members through self-reflection and community collective action.

Fast behavioral feedbacks make ecosystems sensitive to pace and not just magnitude of anthropogenic environmental change.

Anthropogenic environmental change is altering the behavior of animals in ecosystems around the world. Although behavior typically occurs on much faster timescales than demography, it can nevertheless influence demographic processes. Here, we use detailed data on behavior and empirical estimates of demography from a coral reef ecosystem to develop a coupled behavioral-demographic ecosystem model. Analysis of the model reveals that behavior and demography feed back on one another to determine how the ecosystem responds to anthropogenic forcing. In particular, an empirically observed feedback between the density and foraging behavior of herbivorous fish leads to alternative stable ecosystem states of coral population persistence or collapse (and complete algal dominance). This feedback makes the ecosystem more prone to coral collapse under fishing pressure but also more prone to recovery as fishing is reduced. Moreover, because of the behavioral feedback, the response of the ecosystem to changes in fishing pressure depends not only on the magnitude of changes in fishing but also on the pace at which changes are imposed. For example, quickly increasing fishing to a given level can collapse an ecosystem that would persist under more gradual change. Our results reveal conditions under which the pace and not just the magnitude of external forcing can dictate the response of ecosystems to environmental change. More generally, our multiscale behavioral-demographic framework demonstrates how high-resolution behavioral data can be incorporated into ecological models to better understand how ecosystems will respond to perturbations.

Mobility and its sensitivity to fitness differences determine consumer-resource distributions.

An animal's movement rate (mobility) and its ability to perceive fitness gradients (fitness sensitivity) determine how well it can exploit resources. Previous models have examined mobility and fitness sensitivity separately and found that mobility, modelled as random movement, prevents animals from staying in high-quality patches, leading to a departure from an ideal free distribution (IFD). However, empirical work shows that animals with higher mobility can more effectively collect environmental information and better sense patch quality, especially when the environment is frequently changed by human activities. Here, we model, for the first time, this positive correlation between mobility and fitness sensitivity and measure its consequences for the populations of a consumer and its resource. In the absence of consumer demography, mobility alone had no effect on system equilibria, but a positive correlation between mobility and fitness sensitivity could produce an IFD. In the presence of consumer demography, lower levels of mobility prevented the system from approaching an IFD due to the mixing of consumers between patches. However, when positively correlated with fitness sensitivity, high mobility led to an IFD. Our study demonstrates that the expected covariation of animal movement attributes can drive broadly theorized consumer-resource patterns across space and time and could underlie the role of consumers in driving spatial heterogeneity in resource abundance.

Odors from marine plastic debris elicit foraging behavior in sea turtles.

Pfaller et al. report that sea turtles respond to odors from biofouled plastic debris with the same behavior that is elicited by food odors, providing a possible unifying explanation for why sea turtles interact with marine plastic.

Conserved behavioral circuits govern high-speed decision-making in wild fish shoals.

To evade their predators, animals must quickly detect potential threats, gauge risk, and mount a response. Putative neural circuits responsible for these tasks have been isolated in laboratory studies. However, it is unclear whether and how these circuits combine to generate the flexible, dynamic sequences of evasion behavior exhibited by wild, freely moving animals. Here, we report that evasion behavior of wild fish on a coral reef is generated through a sequence of well-defined decision rules that convert visual sensory input into behavioral actions. Using an automated system to present visual threat stimuli to fish in situ, we show that individuals initiate escape maneuvers in response to the perceived size and expansion rate of an oncoming threat using a decision rule that matches dynamics of known loom-sensitive neural circuits. After initiating an evasion maneuver, fish adjust their trajectories using a control rule based on visual feedback to steer away from the threat and toward shelter. These decision rules accurately describe evasion behavior of fish from phylogenetically distant families, illustrating the conserved nature of escape decision-making. Our results reveal how the flexible behavioral responses required for survival can emerge from relatively simple, conserved decision-making mechanisms.

Social Information Links Individual Behavior to Population and Community Dynamics.

When individual animals make decisions, they routinely use information produced intentionally or unintentionally by other individuals. Despite its prevalence and established fitness consequences, the effects of such social information on ecological dynamics remain poorly understood. Here, we synthesize results from ecology, evolutionary biology, and animal behavior to show how the use of social information can profoundly influence the dynamics of populations and communities. We combine recent theoretical and empirical results and introduce simple population models to illustrate how social information use can drive positive density-dependent growth of populations and communities (Allee effects). Furthermore, social information can shift the nature and strength of species interactions, change the outcome of competition, and potentially increase extinction risk in harvested populations and communities.

Social interactions among grazing reef fish drive material flux in a coral reef ecosystem.

In human financial and social systems, exchanges of information among individuals cause speculative bubbles, behavioral cascades, and other correlated actions that profoundly influence system-level function. Exchanges of information are also widespread in ecological systems, but their effects on ecosystem-level processes are largely unknown. Herbivory is a critical ecological process in coral reefs, where diverse assemblages of fish maintain reef health by controlling the abundance of algae. Here, we show that social interactions have a major effect on fish grazing rates in a reef ecosystem. We combined a system for observing and manipulating large foraging areas in a coral reef with a class of dynamical decision-making models to reveal that reef fish use information about the density and actions of nearby fish to decide when to feed on algae and when to flee foraging areas. This "behavioral coupling" causes bursts of feeding activity that account for up to 68% of the fish community's consumption of algae. Moreover, correlations in fish behavior induce a feedback, whereby each fish spends less time feeding when fewer fish are present, suggesting that reducing fish stocks may not only reduce total algal consumption but could decrease the amount of algae each remaining fish consumes. Our results demonstrate that social interactions among consumers can have a dominant effect on the flux of energy and materials through ecosystems, and our methodology paves the way for rigorous in situ measurements of the behavioral rules that underlie ecological rates in other natural systems.

When environmental factors become stressors: interactive effects of vermetid gastropods and sedimentation on corals.

Environmental stressors often interact, but most studies of multiple stressors have focused on combinations of abiotic stressors. Here we examined the potential interaction between a biotic stressor, the vermetid snail Ceraesignum maximum, and an abiotic stressor, high sedimentation, on the growth of reef-building corals. In a field experiment, we subjected juvenile massive Porites corals to four treatments: (i) neither stressor, (ii) sedimentation, (iii) vermetids or (iv) both stressors. Unexpectedly, we found no effect of either stressor in isolation, but a significant decrease in coral growth in the presence of both stressors. Additionally, seven times more sediment remained on corals in the presence (versus absence) of vermetids, likely owing to adhesion of sediments to corals via vermetid mucus. Thus, vermetid snails and high sedimentation can interact to drive deleterious effects on reef-building corals. More generally, our study illustrates that environmental factors can combine to have negative interactive effects even when individual effects are not detectable. Such 'ecological surprises' may be easily overlooked, leading to environmental degradation that cannot be anticipated through the study of isolated factors.

Social Information on Fear and Food Drives Animal Grouping and Fitness.

Empirical studies in select systems suggest that social information-the incidental or deliberate information produced by animals and available to other animals-can fundamentally shape animal grouping behavior. However, to understand the role of social information in animal behavior and fitness, we must establish general theory that quantifies effects of social information across ecological contexts and generates expectations that can be applied across systems. Here we used dynamic state variable modeling to isolate effects of social information about food and predators on grouping behavior and fitness. We characterized optimal behavior from a set of strategies that included grouping with different numbers of conspecifics or heterospecifics and the option to forage or be vigilant over the course of a day. We show that the use of social information alone increases grouping behavior but constrains group size to limit competition, ultimately increasing individual fitness substantially across various ecological contexts. We also found that across various contexts, foraging in mixed-species groups is generally better than foraging in conspecific groups, supporting recent theory on competition-information quality trade-offs. Our findings suggest that multiple forms of social information shape animal grouping and fitness, which are sensitive to resource availability and predation pressure that determine information usefulness.

Context-dependent landscape of fear: algal density elicits risky herbivory in a coral reef.

Foraging theory posits that isolation from refuge habitat within a landscape increases perceived predation risk and, thus, suppresses the foraging behavior of prey species. However, these effects may depend fundamentally on resource availability, which could affect prey boldness and can change considerably through bottom-up processes. We conducted a field survey and experiment in a coral reef to test the effects of isolation from refuge habitat (i.e., reef structure) on herbivory by reef fishes and whether these effects depend on resource density. By fitting continuous-time, pure death Markov processes to our data, we found that at both the local and landscape scale distance from refuge habitat reduced herbivory in attractive resource patches of palatable benthic algae. However, our field experiment revealed that higher initial resource densities weakened negative effects of distance from refuge habitat on herbivory. Furthermore, we observed higher bite rates and greater total lengths of herbivorous fishes with greater distance from refuge habitat-responses consistent with higher perceived predation risk. Our results suggest that while the loss or fragmentation of refuge habitat reduces consumer control of resources, greater resource densities can partially counteract this effect by altering landscapes of fear of consumer species. Our findings emphasize the importance of considering the spatial context of species interactions that structure communities.

Sea turtle symbiosis facilitates social monogamy in oceanic crabs via refuge size.

The capacity for resource monopolization by individuals often dictates the size and composition of animal groups, and ultimately, the adoption of mating strategies. For refuge-dwelling animals, the ability (or inability) of individuals to monopolize refuges should depend on the relative size of the refuge. In theory, groups should be larger and more inclusive when refuges are large, and smaller and more exclusive when refuges are small, regardless of refuge type. We test this prediction by comparing the size and composition of groups of oceanic crabs (Planes minutus) living on plastic flotsam and loggerhead sea turtles. We found that (i) surface area of refuges (barnacle colonies on flotsam and supracaudal space on turtles) is a better predictor of crab number than total surface area and (ii) flotsam and turtles with similar refuge surface area host a similar number (1-2) and composition (adult male-female pairs) of crabs. These results indicate that group size and composition of refuge-dwelling animals are modulated by refuge size and the capacity for refuge monopolization. Moreover, these results suggest that sea turtle symbiosis facilitates social monogamy in oceanic crabs, providing insights into how symbiosis can promote specific mating strategies.

Oceanic barnacles act as foundation species on plastic debris: implications for marine dispersal.

Plastic has emerged as an abundant, stable substratum for oceanic dispersal of organisms via rafting. However, the ecological mechanisms underlying community diversity on plastic debris remain poorly understood. On a cruise from California to Hawai'i, we surveyed plastic debris, some likely originating from the 2011 Tohoku tsunami, to examine the relationship between rafting community diversity and both habitat area and stalked barnacle (Lepas spp.) abundance. For sessile taxa richness, we observed an interaction in which the positive effect of debris area weakened the negative effect of barnacle cover. In contrast, for mobile taxa richness, including cohabiting species from opposite sides of the Pacific Ocean, barnacle abundance had a positive effect that was strongest at smaller debris sizes. These findings suggest that barnacles, through interactions with habitat area, have trait-dependent effects on other species, serving as both foundation species and competitors, mediating the diversity and dispersal potential of marine organisms on plastic debris.

Enrichment scale determines herbivore control of primary producers.

Anthropogenic nutrient enrichment stimulates primary production and threatens natural communities worldwide. Herbivores may counteract deleterious effects of enrichment by increasing their consumption of primary producers. However, field tests of herbivore control are often done by adding nutrients at small (e.g., sub-meter) scales, while enrichment in real systems often occurs at much larger scales (e.g., kilometers). Therefore, experimental results may be driven by processes that are not relevant at larger scales. Using a mathematical model, we show that herbivores can control primary producer biomass in experiments by concentrating their foraging in small enriched plots; however, at larger, realistic scales, the same mechanism may not lead to herbivore control of primary producers. Instead, other demographic mechanisms are required, but these are not examined in most field studies (and may not operate in many systems). This mismatch between experiments and natural processes suggests that many ecosystems may be less resilient to degradation via enrichment than previously believed.

Unity through nonlinearity: a unimodal coral-nutrient interaction.

The magnitude and direction of biological effects of environmental disturbances can vary considerably, especially among studies that use presence/absence manipulations. Because nonlinearities (e.g., humped relationships) are common in biological systems, this heterogeneity in effects may arise if systems are similar in their responses but specific studies use few (e.g., two) levels, or a narrow range, of a factor. To test whether nonlinearity can explain heterogeneous responses to a common environmental disturbance, I examined the effect of nutrient enrichment on coral growth, which has been previously shown using simple (e.g., two-level) manipulations to yield positive, negative, or neutral responses. I subjected corals (Porites) to a nutrient gradient in situ for 28 days. Coral growth rate increased (2.4-fold) then decreased (2.7-fold) with enrichment, returning to near-ambient values at the highest nutrient levels. This unimodal response could explain disparities among past findings and provides a compelling case for using regression designs to understand heterogeneity within ecological interactions.

Housekeeping mutualisms: do more symbionts facilitate host performance?

Mutualisms often involve one host supporting multiple symbionts, whose identity, density and intraguild interactions can influence the nature of the mutualism and performance of the host. However, the implications of multiple co-occurring symbionts on services to a host have rarely been quantified. In this study, we quantified effects of decapod symbionts on removal of sediment from their coral host. Our field survey showed that all common symbionts typically occur as pairs and never at greater abundances. Two species, the crab Trapezia serenei and the shrimp Alpheus lottini, were most common and co-occurred more often than expected by chance. We conducted a mesocosm experiment to test for effects of decapod identity and density on sediment removal. Alone, corals removed 10% of sediment, but removal increased to 30% and 48% with the presence of two and four symbionts, respectively. Per-capita effects of symbionts were independent of density and identity. Our results suggest that symbiont density is restricted by intraspecific competition. Thus, increased sediment removal from a coral host can only be achieved by increasing the number of species of symbionts on that coral, even though these species are functionally equivalent. Symbiont diversity plays a key role, not through added functionality but by overcoming density limitation likely imposed by intraspecific mating systems.