Living in mixed species groups promotes predator learning in degraded habitats

Living in mix-species aggregations provides animals with substantive anti-predator, foraging and locomotory advantages while simultaneously exposing them to costs, including increased competition and pathogen exposure. Given each species possess unique morphology, competitive ability, parasite vulnerability and predator defences, we can surmise that each species in mixed groups will experience a unique set of trade-offs. In addition to this unique balance, each species must also contend with anthropogenic changes, a relatively new, and rapidly increasing phenomenon, that adds further complexity to any system. This complex balance of biotic and abiotic factors is on full display in the exceptionally diverse, yet anthropogenically degraded, Great Barrier Reef of Australia. One such example within this intricate ecosystem is the inability of some damselfish to utilize their own chemical alarm cues within degraded habitats, leaving them exposed to increased predation risk. These cues, which are released when the skin is damaged, warn nearby individuals of increased predation risk and act as a crucial associative learning tool. Normally, a single exposure of alarm cues paired with an unknown predator odour facilitates learning of that new odour as dangerous. Here, we show that Ambon damselfish, Pomacentrus amboinensis, a species with impaired alarm responses in degraded habitats, failed to learn a novel predator odour as risky when associated with chemical alarm cues. However, in the same degraded habitats, the same species learned to recognize a novel predator as risky when the predator odour was paired with alarm cues of the closely related, and co-occurring, whitetail damselfish, Pomacentrus chrysurus. The importance of this learning opportunity was underscored in a survival experiment which demonstrated that fish in degraded habitats trained with heterospecific alarm cues, had higher survival than those we tried to train with conspecific alarm cues. From these data, we conclude that redundancy in learning mechanisms among prey guild members may lead to increased stability in rapidly changing environments.

Revisiting the influence of learning in predator functional response, how it can lead to shapes different from type III.

Predator/Parasitoid functional response is one of the main tools used to study predation behaviour, and in assessing the potential of biological control candidates. It is generally accepted that predator learning in prey searching and manipulation can produce the appearance of type III functional response. Holling proposed that in the presence of alternative prey, at some point the predator would shift the preferred prey, leading to the appearance of a sigmoid function that characterized that functional response. This is supported by the analogy between enzyme kinetics and functional response that Holling used as the basis for developing this theory. However, after several decades, sigmoidal functional responses appear in the absence of alternative prey in most of the biological taxa studied. Here, we propose modelling the effect of learning on the functional response by using the explicit incorporation of learning curves in the parameters of the Holling functional response, the attack rate (a), and the manipulation time (h). We then study how the variation in the parameters of the learning curves causes variations in the shape of the functional response curve. We found that the functional response product of learning can be either type I, II or III, depending on what parameters act on the organism, and how much it can learn throughout the length of the study. Therefore the presence of other types of curves should not be automatically associated with the absence of learning. These results are important from an ecological point of view because when type III functional response is associated with learning, it is generally accepted that it can operate as a stabilizing factor in population dynamics. Our results, to the contrary, suggest that depending on how it acts, it may even be destabilizing by generating the appearance of functional responses close to type I.

Variable crab camouflage patterns defeat search image formation

Understanding what maintains the broad spectrum of variation in animal phenotypes and how this influences survival is a key question in biology. Frequency dependent selection – where predators temporarily focus on one morph at the expense of others by forming a “search image” – can help explain this phenomenon. However, past work has never tested real prey colour patterns, and rarely considered the role of different types of camouflage. Using a novel citizen science computer experiment that presented crab “prey” to humans against natural backgrounds in specific sequences, we were able to test a range of key hypotheses concerning the interactions between predator learning, camouflage and morph. As predicted, switching between morphs did hinder detection, and this effect was most pronounced when crabs had “disruptive” markings that were more effective at destroying the body outline. To our knowledge, this is the first evidence for variability in natural colour patterns hindering search image formation in predators, and as such presents a mechanism that facilitates phenotypic diversity in nature.

The signal detection problem of aposematic prey revisited: integrating prior social and personal experience

Ever since Alfred R. Wallace suggested brightly coloured, toxic insects warn predators about their unprofitability, evolutionary biologists have searched for an explanation of how these aposematic prey evolve and are maintained in natural populations. Understanding how predators learn about this widespread prey defence is fundamental to addressing the problem, yet individuals differ in their foraging decisions and the predominant application of associative learning theory largely ignores predators' foraging context. Here we revisit the suggestion made 15 years ago that signal detection theory provides a useful framework to model predator learning by emphasizing the integration of prior information into predation decisions. Using multiple experiments where we modified the availability of social information using video playback, we show that personal information (sampling aposematic prey) improves how predators (great tits, Parus major ) discriminate between novel aposematic and cryptic prey. However, this relationship was not linear and beyond a certain point personal encounters with aposematic prey were no longer informative for prey discrimination. Social information about prey unpalatability reduced attacks on aposematic prey across learning trials, but it did not influence the relationship between personal sampling and discrimination. Our results suggest therefore that acquiring social information does not influence the value of personal information, but more experiments are needed to manipulate pay-offs and disentangle whether information sources affect response thresholds or change discrimination. This article is part of the theme issue ‘Signal detection theory in recognition systems: from evolving models to experimental tests’.

Evolution of switchable aposematism: insights from individual-based simulations

Some defended prey animals can switch on their normally hidden aposematic signals. This switching may occur in reaction to predators’ approach (pre-attack signals) or attack (post-attack signals). Switchable aposematism has been relatively poorly studied, but we can expect that it might bring a variety of benefits to an aposmetic organism. First, the switching could startle the predators (deimatism). Second, it could facilitate aversive learning. Third, it could minimize exposure or energetic expense, as the signal can be switched off. These potential benefits might offset costs of developing, maintaining and utilizing the switchable traits. Here we focused on the third benefit of switchability, the cost-saving aspect, and developed an individual-based computer simulation of predators and prey. In 88,128 model runs, we observed evolution of permanent, pre-attack, or post-attack aposematic signals of varying strength. We found that, in general, the pre-attack switchable aposematism may require moderate predator learning speed, high basal detectability, and moderate to high signal cost. On the other hand, the post-attack signals may arise under slow predator learning, low basal detectability and high signal cost. When predator population turnover is fast, it may lead to evolution of post-attack aposematic signals that are not conforming to the above tendency. We also suggest that a high switching cost may exert different selection pressure on the pre-attack than the post-attack switchable strategies. To our knowledge, these are the first theoretical attempts to systematically explore the evolution of switchable aposematism relative to permanent aposematism in defended prey. Our simulation model is capable of addressing additional questions beyond the scope of this article, and we open the simulation software, program manual and source code for free public use.

School is out on noisy reefs: the effect of boat noise on predator learning and survival of juvenile coral reef fishes

Noise produced by anthropogenic activities is increasing in many marine ecosystems. We investigated the effect of playback of boat noise on fish cognition. We focused on noise from small motorboats, since its occurrence can dominate soundscapes in coastal communities, the number of noise-producing vessels is increasing rapidly and their proximity to marine life has the potential to cause deleterious effects. Cognition—or the ability of individuals to learn and remember information—is crucial, given that most species rely on learning to achieve fitness-promoting tasks, such as finding food, choosing mates and recognizing predators. The caveat with cognition is its latent effect: the individual that fails to learn an important piece of information will live normally until the moment where it needs the information to make a fitness-related decision. Such latent effects can easily be overlooked by traditional risk assessment methods. Here, we conducted three experiments to assess the effect of boat noise playbacks on the ability of fish to learn to recognize predation threats, using a common, conserved learning paradigm. We found that fish that were trained to recognize a novel predator while being exposed to ‘reef + boat noise’ playbacks failed to subsequently respond to the predator, while their ‘reef noise’ counterparts responded appropriately. We repeated the training, giving the fish three opportunities to learn three common reef predators, and released the fish in the wild. Those trained in the presence of ‘reef + boat noise’ playbacks survived 40% less than the ‘reef noise’ controls over our 72 h monitoring period, a performance equal to that of predator-naive fish. Our last experiment indicated that these results were likely due to failed learning, as opposed to stress effects from the sound exposure. Neither playbacks nor real boat noise affected survival in the absence of predator training. Our results indicate that boat noise has the potential to cause latent effects on learning long after the stressor has gone.

Testing social learning of anti-predator responses in juvenile jackdaws: the importance of accounting for levels of agitation

Social learning is often assumed to help young animals respond appropriately to potential threats in the environment. We brought wild, juvenile jackdaws briefly into captivity to test whether short exposures to conspecific vocalizations are sufficient to promote anti-predator learning. Individuals were presented with one of two models—a stuffed fox representing a genuine threat, or a toy elephant simulating a novel predator. Following an initial baseline presentation, juveniles were trained by pairing models with either adult mobbing calls, indicating danger, or contact calls suggesting no danger. In a final test phase with no playbacks, birds appeared to have habituated to the elephant, regardless of training, but responses to the fox remained high throughout, suggesting juveniles already recognized it as a predator before the experiment began. Training with mobbing calls did seem to generate elevated escape responses, but this was likely to be a carry-over effect of the playback in the previous trial. Overall, we found little evidence for social learning. Instead, individuals' responses were mainly driven by their level of agitation immediately preceding each presentation. These results highlight the importance of accounting for agitation in studies of anti-predator learning, and whenever animals are held in captivity for short periods.

Optimal background matching camouflage

Background matching is the most familiar and widespread camouflage strategy: avoiding detection by having a similar colour and pattern to the background. Optimizing background matching is straightforward in a homogeneous environment, or when the habitat has very distinct sub-types and there is divergent selection leading to polymorphism. However, most backgrounds have continuous variation in colour and texture, so what is the best solution? Not all samples of the background are likely to be equally inconspicuous, and laboratory experiments on birds and humans support this view. Theory suggests that the most probable background sample (in the statistical sense), at the size of the prey, would, on average, be the most cryptic. We present an analysis, based on realistic assumptions about low-level vision, that estimates the distribution of background colours and visual textures, and predicts the best camouflage. We present data from a field experiment that tests and supports our predictions, using artificial moth-like targets under bird predation. Additionally, we present analogous data for humans, under tightly controlled viewing conditions, searching for targets on a computer screen. These data show that, in the absence of predator learning, the best single camouflage pattern for heterogeneous backgrounds is the most probable sample.