Andrea S. Griffin

Social learning about predators: A review and prospectus

In comparison with social learning about food, social learning about predators has received little attention. Yet such research is of potential interest to students of animal cognition and conservation biologists. I summarize evidence for social learning about predators by fish, birds, eutherian mammals, and marsupials. I consider the proposal that this phenomenon is a case of S-S classical conditioning and suggest that evolution may have modified some of the properties of learning to accommodate for the requirements of learning socially about danger. I discuss some between-species differences in the properties of socially acquired predator avoidance and suggest that learning may be faster and more robust in species in which alarm behavior reliably predicts high predatory threat. Finally, I highlight how studies of socially acquired predator avoidance can inform the design of prerelease antipredator training programs for endangered species.

Learning specificity in acquired predator recognition

Predator recognition is often dependent upon experience. This behavioural plasticity can potentially be exploited to enhance the antipredator behaviour of captive-bred animals, but it is first necessary to understand the specificity of learning. We enhanced the responses of tammar wallabies, Macropus eugenii, to a model fox, Vulpes vulpes, by presenting this novel predator in conjunction with a human simulating a capture procedure. A control group had identical total exposure to fox and human, but with no such predictive relationship between these two events. Animals that experienced paired presentations of fox and human behaved more cautiously towards the fox after training than controls. To assess whether this learnt response was specific to the fox, we presented the animals with an array of visual stimuli both before and after training. The tammars generalized their acquired response from the predator with which they were trained to a predator with which they were not trained (cat, Felis catus), but not to a nonpredator (goat, Capra hircus). Tammars also exhibited a transient increase in response to a model wallaby after training. We suggest that this effect is more likely to reflect social behaviour than generalization of the learnt response from predator to conspecific. Two additional controls revealed that changes in behaviour after training were not attributable to the presentation device and were not caused by a general decrease in response threshold associated with training. Our results suggest that tammar wallabies perceive predators as a natural category.

Innovation and problem solving: A review of common mechanisms

Behavioural innovations have become central to our thinking about how animals adjust to changing environments. It is now well established that animals vary in their ability to innovate, but understanding why remains a challenge. This is because innovations are rare, so studying innovation requires alternative experimental assays that create opportunities for animals to express their ability to invent new behaviours, or use pre-existing ones in new contexts. Problem solving of extractive foraging tasks has been put forward as a suitable experimental assay. We review the rapidly expanding literature on problem solving of extractive foraging tasks in order to better understand to what extent the processes underpinning problem solving, and the factors influencing problem solving, are in line with those predicted, and found, to underpin and influence innovation in the wild. Our aim is to determine whether problem solving can be used as an experimental proxy of innovation. We find that in most respects, problem solving is determined by the same underpinning mechanisms, and is influenced by the same factors, as those predicted to underpin, and to influence, innovation. We conclude that problem solving is a valid experimental assay for studying innovation, propose a conceptual model of problem solving in which motor diversity plays a more central role than has been considered to date, and provide recommendations for future research using problem solving to investigate innovation. This article is part of a Special Issue entitled: Cognition in the wild.

Cognition and personality: an analysis of an emerging field

It is now well established that individuals can differ consistently in their average levels of behaviour across different contexts. There have recently been calls to apply the same adaptive framework to interindividual differences in cognition. These calls have culminated in the suggestion that variation in personality and cognition should correlate. We suggest that both these appealing notions are conceptually and logistically problematic. We identify the first crucial step for establishing any cognition-personality relationship. This is to determine the degree to which cognitive abilities yield consistent task performance. We then suggest how to establish whether such consistency exists. Finally, we discuss why formulating predictions about how cognition might be related to personality is much more difficult than is currently realised.

Olfactory predator recognition: wallabies may have to learn to be wary

Many species modify their behaviour in response to the scents of their predators, but species or populations living without predators may lose such abilities. This loss has been suggested to be irreversible, and to constitute a significant hurdle in restoring historical ecosystems. Olfactory predator recognition was studied in two macropodid marsupials - the tammar wallaby ( Macropus eugenii ) and the red-necked pademelon ( Thylogale thetis ). Both species are in the ‘critical weight range’ of Australian native mammals that have been negatively affected by the introduction of novel predators since European settlement. Predator-naive animals were tested by exposing subjects simultaneously to two feeders with either a predator or a herbivore faecal or urine sample beneath the food tray. The presence of predator olfactory cues beneath the feeder did not affect foraging behaviour or feeder use when compared to control stimuli (herbivore faeces or urine). Previous studies have found that predator-experienced herbivorous marsupials modify their behaviour in the presence of predator scents. In contrast, our studies of predator-naive individuals found no evidence of such selectivity, suggesting that marsupial herbivores may have to learn to modify their behaviour in response to olfactory cues from predators. This implies that the loss of olfactory predator recognition may not be irreversible. Animals translocated from predator-free areas could potentially be trained to recognise the smells of their predators.

Social learning of antipredator behaviour in a marsupial

Abstract Socially acquired predator recognition has been demonstrated in a range of taxa, but there is no experimental evidence for this phenomenon in marsupials. We have previously shown that tammar wallabies, Macropus eugenii, can be individually trained to avoid a model fox, Vulpes vulpes. Here, we examined whether such acquired responses can be socially transmitted to predator-naive companions. Tammars were given training trials in which they observed the response of a demonstrator wallaby that was either fearful of the fox (experimental group), or indifferent to it (control group). Tammars in the experimental group subsequently responded to the fox model with significantly higher vigilance levels than controls. To examine the specificity of this acquired antipredator behaviour, we measured responses to an array of other visual stimuli after training and compared these with the results of identical pretraining tests. There was a small difference between the two groups in responses to a model cat, Felis catus, but not to a model nonpredator (goat, Capra hircus). There were also no differences between experimental and control groups during blank trials, in which no stimulus was presented, showing that the elevated vigilance response to the fox did not simply reflect a general increase in arousal. The effect of training was hence to inculcate a relatively specific response to the fox, with only limited generalization to another predator stimulus. These findings provide the first evidence for social learning in a marsupial and suggest that this group has cognitive characteristics convergent with those of eutherian mammals. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.

The paradox of invasion in birds: competitive superiority or ecological opportunism?

Why can alien species succeed in environments to which they have had no opportunity to adapt and even become more abundant than many native species? Ecological theory suggests two main possible answers for this paradox: competitive superiority of exotic species over native species and opportunistic use of ecological opportunities derived from human activities. We tested these hypotheses in birds combining field observations and experiments along gradients of urbanization in New South Wales (Australia). Five exotic species attained densities in the study area comparable to those of the most abundant native species, and hence provided a case for the invasion paradox. The success of these alien birds was not primarily associated with a competitive superiority over native species: the most successful invaders were smaller and less aggressive than their main native competitors, and were generally excluded from artificially created food patches where competition was high. More importantly, exotic birds were primarily restricted to urban environments, where the diversity and abundance of native species were low. This finding agrees with previous studies and indicates that exotic and native species rarely interact in nature. Observations and experiments in the field revealed that the few native species that exploit the most urbanized environments tended to be opportunistic foragers, adaptations that should facilitate survival in places where disturbances by humans are frequent and natural vegetation has been replaced by man-made structures. Successful invaders also shared these features, suggesting that their success is not a paradox but can be explained by their capacity to exploit ecological opportunities that most native species rarely use.

Tracking changing environments: innovators are fast, but not flexible learners.

Behavioural innovations are increasingly thought to provide a rich source of phenotypic plasticity and evolutionary change. Innovation propensity shows substantial variation across avian taxa and provides an adaptive mechanism by which behaviour is flexibly adjusted to changing environmental conditions. Here, we tested for the first time the prediction that inter-individual variation in innovation propensity is equally a measure of behavioural flexibility. We used Indian mynas, Sturnus tristis, a highly successful worldwide invader. Results revealed that mynas that solved an extractive foraging task more quickly learnt to discriminate between a cue that predicted food, and one that did not more quickly. However, fast innovators were slower to change their behaviour when the significance of the food cues changed. This unexpected finding appears at odds with the well-established view that avian taxa with larger brains relative to their body size, and therefore greater neural processing power, are both faster, and more flexible learners. We speculate that the existence of this relationship across taxa can be reconciled with its absence within species by assuming that fast, innovative learners and non innovative, slow, flexible learners constitute two separate individual strategies, which are both underpinned by enhanced neural processing power. This idea is consistent with the recent proposal that individuals may differ consistently in ‘cognitive style’, differentially trading off speed against accuracy in cognitive tasks.

Consumer and motor innovation in the common myna: the role of motivation and emotional responses

Behavioural innovation is believed to be an important way in which animals devise solutions to new problems, yet the factors underpinning individual differences in innovation remain unclear. Here, we asked how motivational states and emotional responses to novelty shape the innovation process with a series of experiments in common mynas, Sturnus tristis. To this aim, we measured experimentally the willingness of adult individuals to eat a new food (consumer innovation) and to develop a new foraging technique (motor innovation), as well as their degree of neophobia, exploration, shyness, motivation and activity levels. Common mynas showed some propensity for consumer and motor innovations, with 55% and 22% of individuals solving the respective tasks. Moreover, individuals that solved the task significantly decreased their latency to solve it subsequently, indicating that learning had occurred. Differences in problem-solving performance were not related to sex, and individuals that solved the consumer task did not solve the motor innovation task faster. The likelihood of solving the motor task increased with propensity of the individual to explore the test apparatus, suggesting that the task was solved by trial and error. Exploration increased with the motivation to feed and decreased with the degree of neophobia. Thus, while differences in innovation propensity between individuals may result from cognitive differences, our results highlight that they may also reflect particular motivational states or emotional responses of individuals to novel situations.

To innovate or not: contrasting effects of social groupings on safe and risky foraging in Indian mynahs

Foraging innovations are increasingly recognized as an important source of phenotypic plasticity, evolutionary change and adaptation to environmental challenges. One line of research has successfully demonstrated that innovation can represent a stable individual trait, but by the same token has shown strong contextual effects on innovation. We examined the effects of social context on innovative foraging behaviour. Across two separate experiments, we measured the individual propensity of Indian mynahs, Acridotheres tristis, to innovate when alone, in pairs, or in groups of five birds. Although innovators remained consistent in their relative innovation performance ranking (high, medium, low), the presence of one or more conspecifics reduced the likelihood of innovating, and increased innovation latencies, significantly relative to when individuals were tested alone. A neophobia test in which latency to forage was compared in both the absence and the presence of a novel object, in each of two social contexts (solitary versus social), showed that the presence of conspecifics caused mynahs to forage significantly faster in a safe situation (object absent) relative to when alone, but to delay foraging in a risky situation (object present). Together, these findings suggest that sociality can have contrasting effects on foraging in safe and risky situations, and, in some species at least, effects of sociality on innovative foraging may hence be more akin to those observed in the presence of risk. Negotiation over engaging with risks inherent to innovative foraging offered the most likely explanation for socially inhibited innovation behaviour, and may act to constrain the diffusion of innovations under some conditions.