Maud C. O. Ferrari

Chemical ecology of predator–prey interactions in aquatic ecosystems: a review and prospectusThe present review is one in the special series of reviews on animal–plant interactions.

The interaction between predator and prey is an evolutionary arms race, for which early detection by either party is often the key to success. In aquatic ecosystems, olfaction is an essential source of information for many prey and predators and a number of cues have been shown to play a key role in trait-mediated indirect interactions in aquatic communities. Here, we review the nature and role of predator kairomones, chemical alarm cues, disturbance cues, and diet cues on the behaviour, morphology, life history, and survival of aquatic prey, focusing primarily on the discoveries from the last decade. Many advances in the field have been accomplished: testing the survival value of those chemicals, providing field validation of laboratory results, understanding the extent to which chemically mediated learning may benefit the prey, understanding the role of these chemicals in mediating morphological and life-history adaptations, and most importantly, the selection pressures leading to the evolution of chemi...

Evolution and behavioural responses to human‐induced rapid environmental change

Almost all organisms live in environments that have been altered, to some degree, by human activities. Because behaviour mediates interactions between an individual and its environment, the ability of organisms to behave appropriately under these new conditions is crucial for determining their immediate success or failure in these modified environments. While hundreds of species are suffering dramatically from these environmental changes, others, such as urbanized and pest species, are doing better than ever. Our goal is to provide insights into explaining such variation. We first summarize the responses of some species to novel situations, including novel risks and resources, habitat loss/fragmentation, pollutants and climate change. Using a sensory ecology approach, we present a mechanistic framework for predicting variation in behavioural responses to environmental change, drawing from models of decision‐making processes and an understanding of the selective background against which they evolved. Where immediate behavioural responses are inadequate, learning or evolutionary adaptation may prove useful, although these mechanisms are also constrained by evolutionary history. Although predicting the responses of species to environmental change is difficult, we highlight the need for a better understanding of the role of evolutionary history in shaping individuals’ responses to their environment and provide suggestion for future work.

Replenishment of fish populations is threatened by ocean acidification

There is increasing concern that ocean acidification, caused by the uptake of additional CO2 at the ocean surface, could affect the functioning of marine ecosystems; however, the mechanisms by which population declines will occur have not been identified, especially for noncalcifying species such as fishes. Here, we use a combination of laboratory and field-based experiments to show that levels of dissolved CO2 predicted to occur in the ocean this century alter the behavior of larval fish and dramatically decrease their survival during recruitment to adult populations. Altered behavior of larvae was detected at 700 ppm CO2, with many individuals becoming attracted to the smell of predators. At 850 ppm CO2, the ability to sense predators was completely impaired. Larvae exposed to elevated CO2 were more active and exhibited riskier behavior in natural coral-reef habitat. As a result, they had 5–9 times higher mortality from predation than current-day controls, with mortality increasing with CO2 concentration. Our results show that additional CO2 absorbed into the ocean will reduce recruitment success and have far-reaching consequences for the sustainability of fish populations.

The paradox of risk allocation: a review and prospectus

Predation is one of the most important selection pressures acting on prey behaviour. While numerous studies have shown that when predation risk is high, prey tend to increase vigilance and reduce foraging effort, until recently, few studies have looked at how the temporal pattern of risk influences antipredator behaviour. The risk allocation hypothesis predicts that as predation risk fluctuates over time (e.g. as predators come and go), the intensity of prey vigilance and foraging should depend on both the level of risk and the proportion of time that predators are present. If predators are usually absent, prey can meet their energy demands during safe periods, and thus respond strongly during the rare times when predators are present. In contrast, if predators are almost always present, prey might need to forage actively even though predators are present, a counterintuitive prediction for many behavioural ecologists. In this review, we present and highlight the paradoxical nature of the risk allocation model. We then review studies that empirically tested the model. These studies provide only mixed support for the model. Importantly, we identify factors that help to explain why some studies supported the model and others did not. In particular, we find that studies that gave prey more time to assess and learn the risk regime had a higher probability of yielding results that supported the model. Finally, we suggest extensions of the model framework to incorporate broader and more complex ecological contexts.

The role of learning in the development of threat-sensitive predator avoidance by fathead minnows

The ability to recognize a potential predator and display adaptive antipredator behaviour is crucial to the survival of prey animals. Prey should gain a fitness advantage by displaying antipredator responses with an intensity that matches their risk of predation. Understanding how such responses develop is the focus of our current study. Many prey fish do not show innate recognition of predators. Thus, learning is necessary and a strong selection pressure should exist to make learning as efficient as possible. In this study we investigated the ability of predator-naive fathead minnows, Pimephales promelas, to learn to recognize an unknown predator, brook charr, Salvelinus fontinalis. First, we conditioned minnows to recognize charr odour by exposing them to various concentrations of chemical alarm cues simultaneously with the odour of the charr and we subsequently tested them for recognition of this odour as a predation threat. Our objective was to test whether there was a match between the intensity of their antipredator responses during conditioning and recognition trials. Second, we tested whether minnows could learn to recognize charr through cultural transmission (i.e. by observing a conspecific responding to the odour of the predator) and we tested for a correlation between the intensity of response of the tutors during conditioning and the intensity of the learned responses by the observers during recognition trials. For both learning modes, the intensity of the response during the conditioning phase was retained during subsequent recognition trials. Our results suggest that minnows learn to respond more intensely to predation cues associated with high risk.

Generalization of learned predator recognition: an experimental test and framework for future studies

While some prey species possess an innate recognition of their predators, others require learning to recognize their predators. The specific characteristics of the predators that prey learn and whether prey can generalize this learning to similar predatory threats have been virtually ignored. Here, we investigated whether fathead minnows that learned to chemically recognize a specific predator species as a threat has the ability to generalize their recognition to closely related predators. We found that minnows trained to recognize the odour of a lake trout as a threat (the reference predator) generalized their responses to brook trout (same genus as lake trout) and rainbow trout (same family), but did not generalize to a distantly related predatory pike or non-predatory suckers. We also found that the intensity of antipredator responses to the other species was correlated with the phylogenetic distance to the reference predator; minnows responded with a higher intensity response to brook trout than rainbow trout. This is the first study showing that prey have the ability to exhibit generalization of predator odour recognition. We discuss these results and provide a theoretical framework for future studies of generalization of predator recognition.

Epidermal ‘alarm substance’ cells of fishes maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation

Many fishes possess specialized epidermal cells that are ruptured by the teeth of predators, thus reliably indicating the presence of an actively foraging predator. Understanding the evolution of these cells has intrigued evolutionary ecologists because the release of these alarm chemicals is not voluntary. Here, we show that predation pressure does not influence alarm cell production in fishes. Alarm cell production is stimulated by exposure to skin-penetrating pathogens (water moulds: Saprolegnia ferax and Saprolegnia parasitica), skin-penetrating parasites (larval trematodes: Teleorchis sp. and Uvulifer sp.) and correlated with exposure to UV radiation. Suppression of the immune system with environmentally relevant levels of Cd inhibits alarm cell production of fishes challenged with Saprolegnia. These data are the first evidence that alarm substance cells have an immune function against ubiquitous environmental challenges to epidermal integrity. Our results indicate that these specialized cells arose and are maintained by natural selection owing to selfish benefits unrelated to predator–prey interactions. Cell contents released when these cells are damaged in predator attacks have secondarily acquired an ecological role as alarm cues because selection favours receivers to detect and respond adaptively to public information about predation.

Phenotypically plastic neophobia: a response to variable predation risk

Prey species possess a variety of morphological, life history and behavioural adaptations to evade predators. While specific evolutionary conditions have led to the expression of permanent, non-plastic anti-predator traits, the vast majority of prey species rely on experience to express adaptive anti-predator defences. While ecologists have identified highly sophisticated means through which naive prey can deal with predation threats, the potential for death upon the first encounter with a predator is still a remarkably important unresolved issue. Here, we used both laboratory and field studies to provide the first evidence for risk-induced neophobia in two taxa (fish and amphibians), and argue that phenotypically plastic neophobia acts as an adaptive anti-predator strategy for vulnerable prey dealing with spatial and temporal variation in predation risk. Our study also illustrates how risk-free maintenance conditions used in laboratory studies may blind researchers to adaptive anti-predator strategies that are only expressed in high-risk conditions.

Effects of Ocean Acidification on Learning in Coral Reef Fishes

Ocean acidification has the potential to cause dramatic changes in marine ecosystems. Larval damselfish exposed to concentrations of CO2 predicted to occur in the mid- to late-century show maladaptive responses to predator cues. However, there is considerable variation both within and between species in CO2 effects, whereby some individuals are unaffected at particular CO2 concentrations while others show maladaptive responses to predator odour. Our goal was to test whether learning via chemical or visual information would be impaired by ocean acidification and ultimately, whether learning can mitigate the effects of ocean acidification by restoring the appropriate responses of prey to predators. Using two highly efficient and widespread mechanisms for predator learning, we compared the behaviour of pre-settlement damselfish Pomacentrus amboinensis that were exposed to 440 µatm CO2 (current day levels) or 850 µatm CO2, a concentration predicted to occur in the ocean before the end of this century. We found that, regardless of the method of learning, damselfish exposed to elevated CO2 failed to learn to respond appropriately to a common predator, the dottyback, Pseudochromis fuscus. To determine whether the lack of response was due to a failure in learning or rather a short-term shift in trade-offs preventing the fish from displaying overt antipredator responses, we conditioned 440 or 700 µatm-CO2 fish to learn to recognize a dottyback as a predator using injured conspecific cues, as in Experiment 1. When tested one day post-conditioning, CO2 exposed fish failed to respond to predator odour. When tested 5 days post-conditioning, CO2 exposed fish still failed to show an antipredator response to the dottyback odour, despite the fact that both control and CO2-treated fish responded to a general risk cue (injured conspecific cues). These results indicate that exposure to CO2 may alter the cognitive ability of juvenile fish and render learning ineffective.

Impaired learning of predators and lower prey survival under elevated CO2: A consequence of neurotransmitter interference

Ocean acidification is one of the most pressing environmental concerns of our time, and not surprisingly, we have seen a recent explosion of research into the physiological impacts and ecological consequences of changes in ocean chemistry. We are gaining considerable insights from this work, but further advances require greater integration across disciplines. Here, we showed that projected near-future CO2 levels impaired the ability of damselfish to learn the identity of predators. These effects stem from impaired neurotransmitter function; impaired learning under elevated CO2 was reversed when fish were treated with gabazine, an antagonist of the GABA-A receptor - a major inhibitory neurotransmitter receptor in the brain of vertebrates. The effects of CO2 on learning and the link to neurotransmitter interference were manifested as major differences in survival for fish released into the wild. Lower survival under elevated CO2 , as a result of impaired learning, could have a major influence on population recruitment.