A Sensory-Driven Trade-Off between Coordinated Motion in Social Prey and a Predator's Visual Confusion.

Social animals are capable of enhancing their awareness by paying attention to their neighbors, and prey found in groups can also confuse their predators. Both sides of these sensory benefits have long been appreciated, yet less is known of how the perception of events from the perspectives of both prey and predator can interact to influence their encounters. Here we examined how a visual sensory mechanism impacts the collective motion of prey and, subsequently, how their resulting movements influenced predator confusion and capture ability. We presented virtual prey to human players in a targeting game and measured the speed and accuracy with which participants caught designated prey. As prey paid more attention to neighbor movements their collective coordination increased, yet increases in prey coordination were positively associated with increases in the speed and accuracy of attacks. However, while attack speed was unaffected by the initial state of the prey, accuracy dropped significantly if the prey were already organized at the start of the attack, rather than in the process of self-organizing. By repeating attack scenarios and masking the targeted prey's neighbors we were able to visually isolate them and conclusively demonstrate how visual confusion impacted capture ability. Delays in capture caused by decreased coordination amongst the prey depended upon the collection motion of neighboring prey, while it was primarily the motion of the targets themselves that determined capture accuracy. Interestingly, while a complete loss of coordination in the prey (e.g., a flash expansion) caused the greatest delay in capture, such behavior had little effect on capture accuracy. Lastly, while increases in collective coordination in prey enhanced personal risk, traveling in coordinated groups was still better than appearing alone. These findings demonstrate a trade-off between the sensory mechanisms that can enhance the collective properties that emerge in social animals and the individual group member's predation risk during an attack

Computerized stimuli for studying oddity effects

Visually hunting predators must overcome the challenges that prey groups present. One such challenge is the confusion effect where an overburdened visual system means predators are unable to successfully target prey. A strategy to overcome confusion is the targeting of distinct, or odd, individuals (the oddity effect). In live prey experiments, manipulation of group member phenotypes can be challenging and prey may differ on more than the single feature one intends to define as odd. The use of highly controllable computerized stimuli to study predator-prey interactions is increasingly popular in the field of behavioral ecology. However, to our knowledge, the validity of computerized stimuli to study the oddity effect has not been established.Predator choice experiments were conducted using naive stickleback predators to ascertain whether the oddity effect could be demonstrated in the absence of live prey. We found evidence for both the oddity effect and preferential targeting of group edges and low density regions, as would be predicted if predators targeted prey individuals to minimize confusion. The oddity effect was evident at a low threshold, above which dots were no longer perceived as odd, and no longer attacked more often than expected by chance.We conclude that computerized stimuli are an improved, practical method for studying oddity effects while further validating the use of similar methods for studying other aspects of visual predation. In addition to higher control of ‘prey’ appearance, the replacement of live prey animals with digital stimuli is ethically beneficial and reusing code improves experimental efficiency

Cognitive Control of Escape Behaviour

When faced with potential predators, animals instinctively decide whether there is a threat they should escape from, and also when, how, and where to take evasive action. While escape is often viewed in classical ethology as an action that is released upon presentation of specific stimuli, successful and adaptive escape behaviour relies on integrating information from sensory systems, stored knowledge, and internal states. From a neuroscience perspective, escape is an incredibly rich model that provides opportunities for investigating processes such as perceptual and value-based decision-making, or action selection, in an ethological setting. We review recent research from laboratory and field studies that explore, at the behavioural and mechanistic levels, how elements from multiple information streams are integrated to generate flexible escape behaviour

Cognitive Control of Escape Behaviour

When faced with potential predators, animals instinctively decide whether there is a threat they should escape from, and also when, how, and where to take evasive action. While escape is often viewed in classical ethology as an action that is released upon presentation of specific stimuli, successful and adaptive escape behaviour relies on integrating information from sensory systems, stored knowledge, and internal states. From a neuroscience perspective, escape is an incredibly rich model that provides opportunities for investigating processes such as perceptual and value-based decision-making, or action selection, in an ethological setting. We review recent research from laboratory and field studies that explore, at the behavioural and mechanistic levels, how elements from multiple information streams are integrated to generate flexible escape behaviour

Behavioural flexibility in response to environmental change

A fundamental challenge in biology is to understand how animals can respond to the unprecedented environmental changes caused by human activities. In aquatic systems, pollution and disturbance from anthropogenic activities often impacts upon the sensory environment, and affects a number of important fitness-related behaviours. This PhD focuses on how a degraded environment impacts the behavioural responses of fish. The first section (chapters 2, 3 and 4) examines whether a degraded visual environment immediately affects the aggregation behaviour of fish as prey, and explores the implications for fish as predators. The second section (chapters 5 and 6) considers the way that previous experiences of a degraded or variable environment shape behavioural responses. Together, the results highlight the importance of considering the relationship between environmental conditions and behaviour over different time spans and during different developmental stages in order to understand how fish may respond to anthropogenic environmental change.The first section offers new evidence on the ways that groups of fish respond to predators in turbid water, and how predators target individuals within those groups. In chapter 2, I investigate how shoals of guppies respond to a simulated aerial predator attack in increasing levels of turbidity. I find that, in turbid water, guppies form looser shoals, and alter their behaviour in response to a simulated attack by showing weaker escape manoeuvres and increasing freezing behaviour as opposed to darting escape manoeuvres. In chapter 3, I explore the ‘selfish herd movement’ rules that guppies use to form shoals in response to a predator attack in clear and turbid water. I find that guppies use more complex rules (moving towards a location determined by the position of multiple individuals) in clear water, resulting in large compact shoals. By comparison, guppies are unable to use these rules when forming groups in turbid water, resulting in smaller, more fragmented shoals. In chapter 4, I consider the effect of turbidity from the perspective of both predator and prey, in the context of the oddity effect. Firstly, I assess the effect of turbidity on how stickleback predators target Daphnia prey individuals of different sizes from within mixed groups. Secondly, I explore how turbidity influences the social choices made by sticklebacks. From the perspective of the predator, sticklebacks selected large bodied Daphnia from mixed groups more than expected by chance in clear water, but not in turbid water. From the perspective of the prey, large individuals lost their preference for size-matched shoalmates in turbid water, whereas small individuals showed no social preference in either clear or turbid water. The oddity effect appears weakened in turbid water, relaxing predation pressure on large odd individuals at the expense of small individuals. Together, these three chapters consider the immediate, flexible responses of both predator and prey to short-term changes in turbidity.The second section of the thesis explores the longer-term impacts of a degraded or variable environment on the behavioural responses of fish. In chapter 5, I investigate how adult guppies respond to different food cues (visual, olfactory, or a combination of both) with increasing levels of experience of a visually poor environment. Previous work rearing guppies under similar conditions found that individuals make a sensory switch from vision to olfaction. I find that, although guppies with more experience of a dark environment increase their foraging success in visually poor environments, they do not make a sensory switch from vision to olfaction as seen in juvenile fish. Finally, in chapter 6, I step away from the visual environment and look at how recent experience of a variable habitat combined with low or high food levels affects boldness and exploratory behaviour in guppies. While some behaviours are modified with experience of low food, for example, the time to attack a food item, I find that exploratory behaviour was not influenced by either energy state or experience of a variable environment, remaining remarkably stable over time. These final two chapters highlight the importance of investigating behavioural responses to the environment over different time spans and during different developmental stages

Physical and Biological Drivers of Juvenile Fish Distributions in Unstructured Shallow Tropical Nearshore Habitats

The structural complexity of aquatic habitats can influence the ecological processes that occur within them, as fine-scale topographic features act as refugia for small fishes, buffering the effects of environmental stressors. Accordingly, the habitat requirements of juvenile demersal fishes in shallow littoral zones are often defined by their associations with distinct benthic microhabitats, such as densely vegetated substrates. However, an array of ecologically-important juvenile fishes also associate with topographically-homogeneous, sparsely-vegetated substrata. Absent the benefits offered by structural refugia, such fishes may be more affected by environmental variability and may have evolved distinct strategies for coping with stressors. I examined this hypothesis by assessing the factors shaping juvenile fish assemblages across the littoral zones of a subtropical island, where I predicted that flow-related stress and positive social interactions would be influential in governing the distributions of species occupying open, unstructured habitats. Spatio-temporal variability in the strength of wave-and tide-driven water movement were among the principal drivers of habitat use for a variety of juvenile fishes, exerting the most pronounced effects on species with an aversion to dense benthic vegetation (i.e., Bothus spp., and Albula vulpes), with little impact on species inhabiting seagrass (Haemulon spp. and Halichoeres bivittatus). Spatial segregation between A. vulpes and its cryptic congener Albula goreensis was unrelated to benthic habitat characteristics but well-explained by differential relationships with wave exposure, suggesting that niche partitioning between these functionally-indistinct species was mediated by flow. After accounting for phenotypic clustering caused by an extensive suite of environmental filters, residual correlations in species abundance were dominated by strongly- asymmetric positive associations, primarily between soft-bottom benthivores and Eucinostomus spp. Interspecific relationships were weak among seagrass-associated taxa. Disparities in the foraging behaviors and putative vigilance-keeping abilities of Eucinostomus spp. and its associate A. vulpes implied that the large organizational influence of eucinostomids could be explained by their capacity for producing risk-related information, which more vulnerable species exploited. Collectively, these findings support the hypothesis that fishes using unstructured habitats are more exposed to flow-related stress than those occupying complex habitats, and likewise that they employ alternative antipredator strategies, relying on social mechanisms to reduce predation risk

Evolution of fish schools: a theoretical study by agent-based simulation and game-theoretic analysis

This thesis aimed to identify the underlying mechanism which drives fish to evolve into the schooling behaviour under predation. Previous works used to explain this formation by group benefits, individual differences or evolutionary trade-offs. However, conflicts from these explanations to the natural fish are considerable. Based on agent-based simulations and game-theoretic analyses, this thesis demonstrated that the intraspecies competition in a relatively homogeneous population is sufficient to cause the evolution of fish schools. It has been shown that when predators exhibit the ‘marginal predation’, that is, only catching prey on the margin of a group, prey fish must evolve to form a selfish herd, which will be increasingly crowded until no outer fish can enter it. In this case, fish should evolve to leave the group margin together, as the originally reported ‘collective departure strategy’, to expose the inner fish and share the risk. This adaptation then leads to the emergence of fish schools. The thesis further showed that the ‘marginal predation’ of predators and the ‘collective departure’ of prey is able to form an evolutionarily stable state in a coevolutionary system, which completed the explanation of the evolution of fish schools in nature

USING VIRTUAL REALITY TO INVESTIGATE ‘PROTEAN’ ANTI-PREDATOR BEHAVIOUR

Prey animals have evolved a wide variety of behaviours to combat the threat of predation, many of which have received considerable empirical and theoretical attention and are generally well understood in terms of their function and mechanistic underpinning. However, one of the most commonly observed and taxonomically widespread antipredator behaviours of all has, remarkably, received almost no experimental investigation: so-called ‘protean’ behaviour. This is defined as ‘behaviour that is sufficiently unpredictable to prevent a predator anticipating in detail the future position or actions of its prey’. In this thesis, I have elucidated the mechanisms that allow protean behaviour to be an effective anti-predatory response. This was explored with two approaches. Firstly, through the novel and extremely timely use of virtual reality to allow human ‘predators’ to attack and chase virtual prey in three-dimensions from a first-person perspective, thereby bringing the realism that has been missing from previous studies on predator-prey dynamics. Secondly through the three-dimensional tracking of protean behaviour in a highly tractable model species, the painted lady butterfly (Vanessa cardui). I explored this phenomenon in multiple contexts. Firstly, I simulated individual protean prey and explored the effects of unpredictability in their movement rules with respect to targeting accuracy of human ‘predators’ in virtual reality. Next, I examined the concept of ‘protean insurance’ via digitised movements of the painted lady butterfly, exploring the qualities of this animals’ movement paths related to human targeting ability. I then explored how the dynamics of animal groupings affected protean movement. Specifically, I investigated how increasing movement path complexity interacted with the well-documented ‘confusion effect’. I explored this question using both an experimental study and a VR citizen science game disseminated to the general public via the video game digital distribution service ‘Steam’. Subsequently, I explored another phenomenon associated with groupings of prey items; the ‘oddity effect’, which describes the preferential targeting of phenotypically odd individuals by predators. Typically, this phenomenon is associated with oddity of colouration or size. In this case, I investigated whether oddity of protean movement patterns relative to other group members could induce a ‘behavioural oddity effect’. Finally, I used a specialised genetic algorithm (GA) that was driven by human performance with respect to targeting prey items. I investigated the emergent protean movement paths that resulted from sustained predation pressure from humans. Specifically, I examined the qualities of the most fit movement paths with respect to control evolutions that were not under the selection pressure of human performance (randomised evolution). In the course of this thesis, I have gained a deeper understanding of a near ubiquitous component of predator prey interactions that has until recently been the subject of little empirical study. These findings provide important insights into the understudied phenomenon of protean movement, which are directly applicable to predator –prey dynamics within a broad range of taxa

The emergence of active perception - seeking conceptual foundations

The aim of this thesis is to explain the emergence of active perception. It takes an interdisciplinary approach, by providing the necessary conceptual foundations for active perception research - the key notions that bridge the conceptual gaps remaining in understanding emergent behaviours of active perception in the context of robotic implementations. On the one hand, the autonomous agent approach to mobile robotics claims that perception is active. On the other hand, while explanations of emergence have been extensively pursued in Artificial Life, these explanations have not yet successfully accounted for active perception.The main question dealt with in this thesis is how active perception systems, as behaviour -based autonomous systems, are capable of providing relatively optimal perceptual guidance in response to environmental challenges, which are somewhat unpredictable. The answer is: task -level emergence on grounds of complicatedly combined computational strategies, but this notion needs further explanation.To study the computational strategies undertaken in active perception re- search, the thesis surveys twelve implementations. On the basis of the surveyed implementations, discussions in this thesis show that the perceptual task executed in support of bodily actions does not arise from the intentionality of a homuncu- lus, but is identified automatically on the basis of the dynamic small mod- ules of particular robotic architectures. The identified tasks are accomplished by quasi -functional modules and quasi- action modules, which maintain transformations of perceptual inputs, compute critical variables, and provide guidance of sensory -motor movements to the most relevant positions for fetching further needed information. Given the nature of these modules, active perception emerges in a different fashion from the global behaviour seen in other autonomous agent research.The quasi- functional modules and quasi- action modules cooperate by estimating the internal cohesion of various sources of information in support of the envisaged task. Specifically, such modules basically reflect various computational facilities for a species to single out the most important characteristics of its ecological niche. These facilities help to achieve internal cohesion, by maintaining a stepwise evaluation over the previously computed information, the required task, and the most relevant features presented in the environment.Apart from the above exposition of active perception, the process of task - level emergence is understood with certain principles extracted from four models of life origin. First, the fundamental structure of active perception is identified as the stepwise computation. Second, stepwise computation is promoted from baseline to elaborate patterns, i.e. from a simple system to a combinatory system. Third, a core requirement for all stepwise computational processes is the comparison between collected and needed information in order to insure the contribution to the required task. Interestingly, this point indicates that active perception has an inherent pragmatist dimension.The understanding of emergence in the present thesis goes beyond the distinc- tion between external processes and internal representations, which some current philosophers argue is required to explain emergence. The additional factors are links of various knowledge sources, in which the role of conceptual foundations is two -fold. On the one hand, those conceptual foundations elucidate how various knowledge sources can be linked. On the other, they make possible an interdisci- plinary view of emergence. Given this two -fold role, this thesis shows the unity of task -level emergence. Thus, the thesis demonstrates a cooperation between sci- ence and philosophy for the purpose of understanding the integrity of emergent cognitive phenomena