Prey responses to disturbance cues: Effects of familiarity, kinship, and past experience with risk

Prey can acquire information about predators by eavesdropping on conspecific cues, but these cues are not always reliable. In aquatic systems, disturbance cues are pulses of urea or ammonia that are often released by prey while fleeing a predator; nearby individuals typically display antipredator responses after detecting these cues. Despite the importance of disturbance cues to aquatic prey survival, they remain largely understudied in terms of their function and evolution. Here, I sought to test whether disturbance cues might function as an antipredator signal. Using a series of experiments, I assessed how familiarity and relatedness with individuals releasing the cues affects the antipredator response of the receiver, and whether background risk levels for the cue releaser and receiver play a role in the response exhibited by the receiver. If prey rely more on disturbance cues from familiar, related, or high predation risk background conspecifics, then I expect to see a heightened fright response to these cues. To test this, I raised wood frog (Lithobates sylvaticus) egg clutches and obtained disturbance cues from groups of tadpoles by simulating a predator chase. Counter to expectation, tadpoles exposed to disturbance cues from unfamiliar individuals displayed a fright response, whereas disturbance cues from familiar individuals were ignored, possibly because these cues became unreliable after being detected repeatedly in the absence of a true threat. Tadpoles responded similarly to the disturbance cues of related and unrelated individuals, suggesting that related individuals did not provide more reliable information. When manipulating background predation risk, high-risk receivers but not low-risk receivers responded to disturbance cues from low-risk donors, suggesting a lower response threshold in high risk prey. Disturbance cues from high-risk donors also elicited more of a fright response in both high- and low-risk receivers. This suggests that high risk prey release more, or more potent disturbance cues. Taken together, these experiments provide strong evidence that tadpoles detect variation in disturbance cues and may be capable of modulating their disturbance cues as antipredator signals. These findings are of important consideration for conservationists studying how Allee effects manifest in threatened aquatic species such as anuran tadpoles

Demographic and evolutionary responses of reef-building corals to climate change

Kevin Bairos-Novak studied coral responses to climate change across the Great Barrier Reef. He modelled coral evolution across future climates and found that coral evolution may keep pace with climate change if carbon emissions are substantially reduced and if healthy corals continue to produce enough new coral recruits

Coral adaptation to climate change: meta-analysis reveals high heritability across multiple traits

Anthropogenic climate change is a rapidly intensifying selection pressure on biodiversity across the globe and, particularly, on the world's coral reefs. The rate of adaptation to climate change is proportional to the amount of phenotypic variation that can be inherited by subsequent generations (i.e., narrow-sense heritability, h2). Thus, traits that have higher heritability (e.g., h2 > 0.5) are likely to adapt to future conditions faster than traits with lower heritability (e.g., h2 0.50) for metrics related to survival and immune responses. Some of these values are higher than typically observed in other taxa, such as survival and growth, while others were more comparable, such as gene expression and photochemistry. There was no detectable effect of temperature on heritability, but narrow-sense heritability estimates were generally lower than broad-sense estimates, indicative of significant non-additive genetic variation across traits. Trait heritability also varied depending on coral life stage, with bleaching and growth in juveniles generally having lower heritability compared to bleaching and growth in larvae and adults. These differences may be the result of previous stabilizing selection on juveniles or may be due to constrained evolution resulting from genetic trade-offs or genetic correlations between growth and thermotolerance. While we find no evidence that heritability decreases under temperature stress, explicit tests of the heritability of thermal tolerance itself—such as coral thermal reaction norm shape—are lacking. Nevertheless, our findings overall reveal high trait heritability for the majority of coral traits, suggesting corals may have a greater potential to adapt to climate change than has been assumed in recent evolutionary models

Impacts of ocean warming on echinoderms: A meta‐analysis

Rising ocean temperatures are threatening marine species and populations worldwide, and ectothermic taxa are particularly vulnerable. Echinoderms are an ecologically important phylum of marine ectotherms and shifts in their population dynamics can have profound impacts on the marine environment. The effects of warming on echinoderms are highly variable across controlled laboratory-based studies. Accordingly, synthesis of these studies will facilitate the better understanding of broad patterns in responses of echinoderms to ocean warming. Herein, a meta-analysis incorporating the results of 85 studies (710 individual responses) is presented, exploring the effects of warming on various performance predictors. The mean responses of echinoderms to all magnitudes of warming were compared across multiple biological responses, ontogenetic life stages, taxonomic classes, and regions, facilitated by multivariate linear mixed effects models. Further models were conducted, which only incorporated responses to warming greater than the projected end-of-century mean annual temperatures at the collection sites. This meta-analysis provides evidence that ocean warming will generally accelerate metabolic rate (+32%) and reduce survival (−35%) in echinoderms, and echinoderms from subtropical (−9%) and tropical (−8%) regions will be the most vulnerable. The relatively high vulnerability of echinoderm larvae to warming (−20%) indicates that this life stage may be a significant developmental bottleneck in the near-future, likely reducing successful recruitment into populations. Furthermore, asteroids appear to be the class of echinoderms that are most negatively affected by elevated temperature (−30%). When considering only responses to magnitudes of warming representative of end-of-century climate change projections, the negative impacts on asteroids, tropical species and juveniles were exacerbated (−51%, −34% and −40% respectively). The results of these analyses enable better predictions of how keystone and invasive echinoderm species may perform in a warmer ocean, and the possible consequences for populations, communities and ecosystems

RawData_for_Bairos-Novak_et_al

The raw data in an Excel spreadsheet used in the R analysis. See the 'metadata' tab of the spreadsheet for more information

A novel alarm signal in aquatic prey: familiar minnows coordinate group defences against predators through chemical disturbance cues

1. Animal signalling systems outside the realm of human perception remain largely understudied. These systems consist of four main components: a signalling context, a voluntary signal, receiver responses and resulting fitness benefits to both the signaller and receiver(s). It is often most difficult to determine incidental cues from voluntary signals. One example is chemical disturbance cues released by aquatic prey during predator encounters that may serve to alert conspecifics of nearby risk and initiate tighter shoaling. We aimed to test whether disturbance cues are released incidentally (i.e. as a cue) or are produced voluntarily depending on a specific signalling context such as the audience surrounding the individual, and thus constitute a signal. 2. We hypothesized that if receivers use disturbance cues to communicate risk among themselves, they would produce more (or more potent) disturbance cues when present in a group of conspecifics rather than when they are isolated (presence/absence of an audience) and use disturbance cues more when present alongside familiar rather than unfamiliar conspecifics (audience composition effect). 3. We placed fathead minnows (Pimephales promelas) in groups with familiar fish, unfamiliar fish or as isolated individuals with no audience present, and then simulated a predator chase to evoke disturbance cues. We used bioassays with independent receivers to assess whether the disturbance cues produced differed depending on the signallers' audience. 4. We found evidence of voluntary signalling, as minnows responded to disturbance cues from groups of fish with tighter shoaling while disturbance cues from isolated minnows did not evoke a significant shoaling response (presence/absence audience effect). Receivers also increased shoaling, freezing and dashing more in response to disturbance cues from familiar groups compared to disturbance cues from unfamiliar groups or isolated minnows (audience composition effect). 5. Together, these findings support our hypothesis that disturbance cues are used as an antipredator signal to initiate coordinated group defences among familiar conspecifics involving shoaling, freezing and dashing. This study represents the strongest evidence to date that chemicals released by aquatic prey upon disturbance by predators serve as voluntary signals rather than simply cues that prey have evolved to detect when assessing their risk of predation

Chemical disturbance cues in aquatic systems: a review and prospectus

In the natural environment, animals can face potentially dangerous and often regular exposure to major environmental fluctuations such as flash flooding and drought, or the approach of a predator. For many aquatic species, exposure to these ecological disturbances triggers the release of “disturbance cues” – generally characterized as chemicals released when animals are startled but not injured. While the chemistry of such cues remains largely unexplored, they appear to provide early warning information to nearby individuals, potentially leading to behavioral decisions that increase overall fitness, particularly for social species that may coordinate group defense. In the literature, disturbance cues have received little attention relative to other chemical cues, such as damage-released alarm cues. However, recent advances in the study of disturbance cue communication have led an uptick in research on the subject. Here, we review the existing literature on responses to disturbance cues in aquatic systems. Although the majority of studies involve behavioral responses to a simulated predator approach, we describe various disturbance types across a broad range of taxa. We discuss the ecological implications of disturbance cues, including their role in risk assessment, signaling, learning, and species specificity. We also address several methodological challenges for this developing field of study, as well as the ethical and conservation implications of this research going forward. Future research on disturbance cues should address a number of key unknowns, including questions regarding disturbance cue chemistry, function, and generality

Data from: The socially mediated recovery of a fearful fish paired with periodically replaced calm models

Social learning is an important mechanism for acquiring knowledge about environmental risk. However, little work has explored the learning of safety and how such learning outcomes are shaped by the social environment. Here, we exposed minnows, Pimephales promelas, to a high-risk environment to induce behavioral responses associated with fear (e.g., neophobia). We then used the presence of calm conspecific models (low-risk individuals) to weaken these responses. When observers (individuals from the high-risk environment) and models were paired consistently in a one-on-one setting, the observers showed no recovery (i.e., no weakening of the fear responses), and instead the models indirectly acquired those responses (i.e., a socially-transmitted state of fear). However, observers paired with models that were periodically replaced with new calm models showed a significant recovery, and each new model showed diminished socially-transmitted fear. We argue that our understanding of predation-related fear and social information transfer can prove fruitful in understanding problems with fear and stress across animal taxa, including among humans who experience post-traumatic stress and secondary trauma. Our findings indicate that the periodic replacement of models can promote fear recovery in observers and reduce socially-transmitted fear in models

Data from: Better the devil you know? how familiarity and kinship affect prey responses to disturbance cues

Prey can greatly improve their odds of surviving predator encounters by eavesdropping on conspecific risk cues, but the reliability of these cues depends on both previous accuracy as well as the cue’s relevance. During a predator chase, aquatic prey release chemical disturbance cues that may vary in their reliability depending on the individuals receiving them. Thus, prey may rely differentially on disturbance cues from familiar individuals (due to previous experience) or from kin (due to their relatedness). We examined the responses of wood frog (Lithobates sylvaticus) tadpoles to disturbance cues from familiar vs. unfamiliar conspecifics and kin vs. non-kin. In accordance with our prediction, tadpoles responded differently to disturbance cues from familiar vs. unfamiliar conspecifics. Tadpoles receiving disturbance cues from unfamiliar individuals displayed a fright response, whereas tadpoles ignored disturbance cues from familiar individuals. Tadpoles may have habituated to familiar cues since they were unaccompanied by a true threat, hence rendering these cues functionally unreliable. Tadpoles responded similarly to disturbance cues from related and unrelated individuals suggesting they were similarly reliable and this mirrors the matching reliability of prey responses to damage-released alarm cues from kin and non-kin. Our findings shed light on a seldom-studied chemical communication system in aquatic prey

Data from: Olfactory cues of habitats facilitate learning about landscapes of fear

Across landscapes, prey are exposed to different levels of predation risk within different habitats. However, little is known about how prey learn about risk in different habitat types. Here, we examined if wood frog tadpoles, Lithobates sylvatica, use olfactory cues from two distinct, plant-dominated habitats (cattail and pond weed) to learn about the overall risk within a habitat and the risk posed by a specific predator species within different habitats. In our first experiment, tadpoles experienced both a high-risk and a low-risk habitat before being tested for habitat-specific neophobic responses, a cognitive trait expressed in high-risk but not low-risk environments. In the second experiment, we taught tadpoles to recognise a predator in one habitat while the other one was never associated with a predator. Tadpoles were then tested for their responses to the predator and a control in both habitats. Our results showed that high-risk cattail tadpoles developed habitat-specific neophobia. However, high-risk pond weed tadpoles developed a generalised neophobia, responding to the novel cues irrespective of the habitat where they were tested. We also found that the habitat in which prey learned the identity of a specific predator did not affect their responses to that predator when tested in different habitats. Our results provide support for the use of olfactory habitat cues by prey to learn about predation risk across landscapes, suggesting unrecognised nuances to how prey use such cues to learn about predation risk