Ecological, morphological and behavioural aspects of tool-use in New Caledonian crows

New Caledonian crows are amongst the most sophisticated tool-users in the animal kingdom. In this thesis I present my findings from various aspects of the crows’ behavioural ecology, morphology and cognition, contributing to our understanding of how this fascinating tool-use behaviour might have evolved. My studies in the field reveal new types of tool manufacture and foraging behaviour that help to build up a complete picture of the ecological importance of tool-use to wild crows. Additionally I demonstrate the subtlety and skill required to extract wood boring beetle larvae from their burrows, accounting for the slow development of tool-use proficiency in juvenile crows. Further work reveals how their unique visual field combines with a peculiarly straight bill to facilitate tool-use; perhaps the only evidence outside of the hominid hand for tool-use specific morphology. Recent studies suggest Corvus species are behaviourally and cognitively predisposed to become tool-users, however, through multiple lines of enquiry this thesis highlights the costs that New Caledonian crows bear in order to become successful tool-users. The unique ecological conditions in New Caledonia are likely to have made this costly form of foraging possible, helping to explain why tool-use is so rarely observed in other animals

Improvement of individual camouflage through background choice in ground-nesting birds.

Animal camouflage is a longstanding example of adaptation. Much research has tested how camouflage prevents detection and recognition, largely focusing on changes to an animal's own appearance over evolution. However, animals could also substantially alter their camouflage by behaviourally choosing appropriate substrates. Recent studies suggest that individuals from several animal taxa could select backgrounds or positions to improve concealment. Here, we test whether individual wild animals choose backgrounds in complex environments, and whether this improves camouflage against predator vision. We studied nest site selection by nine species of ground-nesting birds (nightjars, plovers and coursers) in Zambia, and used image analysis and vision modeling to quantify egg and plumage camouflage to predator vision. Individual birds chose backgrounds that enhanced their camouflage, being better matched to their chosen backgrounds than to other potential backgrounds with respect to multiple aspects of camouflage. This occurred at all three spatial scales tested (a few cm and five meters from the nest, and compared to other sites chosen by conspecifics), and was the case for the eggs of all bird groups studied, and for adult nightjar plumage. Thus, individual wild animals improve their camouflage through active background choice, with choices highly refined across multiple spatial scales

Motion dazzle and the effects of target patterning on capture success.

BACKGROUND: Stripes and other high contrast patterns found on animals have been hypothesised to cause "motion dazzle", a type of defensive coloration that operates when in motion, causing predators to misjudge the speed and direction of object movement. Several recent studies have found some support for this idea, but little is currently understood about the mechanisms underlying this effect. Using humans as model 'predators' in a touch screen experiment we investigated further the effectiveness of striped targets in preventing capture, and considered how stripes compare to other types of patterning in order to understand what aspects of target patterning are important in making a target difficult to capture. RESULTS: We find that striped targets are among the most difficult to capture, but that other patterning types are also highly effective at preventing capture in this task. Several target types, including background sampled targets and targets with a 'spot' on were significantly easier to capture than striped targets. We also show differences in capture attempt rates between different target types, but we find no differences in learning rates between target types. CONCLUSIONS: We conclude that striped targets are effective in preventing capture, but are not uniquely difficult to catch, with luminance matched grey targets also showing a similar capture rate. We show that key factors in making capture easier are a lack of average background luminance matching and having trackable 'features' on the target body. We also find that striped patterns are attempted relatively quickly, despite being difficult to catch. We discuss these findings in relation to the motion dazzle hypothesis and how capture rates may be affected more generally by pattern type.AEH received a studentship from the BBSRC and a CASE award from Dstl, Portsdown West, UK. MS and JT were supported by a Biotechnology and Biological Sciences Research Council, David Phillips Research Fellowship (BB/G022887/1).This is the final published version. It is published by BioMed Central in BMC Evolutionary Biology here: http://www.biomedcentral.com/1471-2148/14/201

The appearance of mimetic Heliconius butterflies to predators and conspecifics.

Adaptive coloration is under conflicting selection pressures: choosing potential mates and warning signaling against visually guided predators. Different elements of the color signal may therefore be tuned by evolution for different functions. We investigated how mimicry in four pairs of Heliconius comimics is potentially seen both from the perspective of butterflies and birds. Visual sensitivities of eight candidate avian predators were predicted through genetic analysis of their opsin genes. Using digital image color analysis, combined with bird and butterfly visual system models, we explored how predators and conspecifics may visualize mimetic patterns. Ultraviolet vision (UVS) birds are able to discriminate between the yellow and white colors of comimics better than violet vision (VS) birds. For Heliconius vision, males and females differ in their ability to discriminate comimics. Female vision and red filtering pigments have a significant effect on the perception of the yellow forewing band and the red ventral forewing pattern. A behavioral experiment showed that UV cues are used in mating behavior; removal of such cues was associated with an increased tendency to approach comimics as compared to conspecifics. We have therefore shown that visual signals can act to both reduce the cost of confusion in courtship and maintain the advantages of mimicry.ERC, CAPES, STR

Defeating crypsis: detection and learning of camouflage strategies.

Camouflage is perhaps the most widespread defence against predators in nature and an active area of interdisciplinary research. Recent work has aimed to understand what camouflage types exist (e.g. background matching, disruptive, and distractive patterns) and their effectiveness. However, work has almost exclusively focused on the efficacy of these strategies in preventing initial detection, despite the fact that predators often encounter the same prey phenotype repeatedly, affording them opportunities to learn to find those prey more effectively. The overall value of a camouflage strategy may, therefore, reflect both its ability to prevent detection by predators and resist predator learning. We conducted four experiments with humans searching for hidden targets of different camouflage types (disruptive, distractive, and background matching of various contrast levels) over a series of touch screen trials. As with previous work, disruptive coloration was the most successful method of concealment overall, especially with relatively high contrast patterns, whereas potentially distractive markings were either neutral or costly. However, high contrast patterns incurred faster decreases in detection times over trials compared to other stimuli. In addition, potentially distractive markings were sometimes learnt more slowly than background matching markings, despite being found more readily overall. Finally, learning effects were highly dependent upon the experimental paradigm, including the number of prey types seen and whether subjects encountered targets simultaneously or sequentially. Our results show that the survival advantage of camouflage strategies reflects both their ability to avoid initial detection (sensory mechanisms) and predator learning (perceptual mechanisms)

The evolution of patterning during movement in a large-scale citizen science game.

The motion dazzle hypothesis posits that high contrast geometric patterns can cause difficulties in tracking a moving target and has been argued to explain the patterning of animals such as zebras. Research to date has only tested a small number of patterns, offering equivocal support for the hypothesis. Here, we take a genetic programming approach to allow patterns to evolve based on their fitness (time taken to capture) and thus find the optimal strategy for providing protection when moving. Our 'Dazzle Bug' citizen science game tested over 1.5 million targets in a touch screen game at a popular visitor attraction. Surprisingly, we found that targets lost pattern elements during evolution and became closely background matching. Modelling results suggested that targets with lower motion energy were harder to catch. Our results indicate that low contrast, featureless targets offer the greatest protection against capture when in motion, challenging the motion dazzle hypothesis

Changes in women’s facial skin color over the ovulatory cycle are not detectable by the human visual system

Human ovulation is not advertised, as it is in several primate species, by conspicuous sexual swellings. However, there is increasing evidence that the attractiveness of women’s body odor, voice, and facial appearance peak during the fertile phase of their ovulatory cycle. Cycle effects on facial attractiveness may be underpinned by changes in facial skin color, but it is not clear if skin color varies cyclically in humans or if any changes are detectable. To test these questions we photographed women daily for at least one cycle. Changes in facial skin redness and luminance were then quantified by mapping the digital images to human long, medium, and shortwave visual receptors. We find cyclic variation in skin redness, but not luminance. Redness decreases rapidly after menstrual onset, increases in the days before ovulation, and remains high through the luteal phase. However, we also show that this variation is unlikely to be detectable by the human visual system. We conclude that changes in skin color are not responsible for the effects of the ovulatory cycle on women’s attractiveness

Escape Distance in Ground-Nesting Birds Differs with Individual Level of Camouflage.

Camouflage is one of the most widespread antipredator strategies in the animal kingdom, yet no animal can match its background perfectly in a complex environment. Therefore, selection should favor individuals that use information on how effective their camouflage is in their immediate habitat when responding to an approaching threat. In a field study of African ground-nesting birds (plovers, coursers, and nightjars), we tested the hypothesis that individuals adaptively modulate their escape behavior in relation to their degree of background matching. We used digital imaging and models of predator vision to quantify differences in color, luminance, and pattern between eggs and their background, as well as the plumage of incubating adult nightjars. We found that plovers and coursers showed greater escape distances when their eggs were a poorer pattern match to the background. Nightjars sit on their eggs until a potential threat is nearby, and, correspondingly, they showed greater escape distances when the pattern and color match of the incubating adult's plumage-rather than its eggs-was a poorer match to the background. Finally, escape distances were shorter in the middle of the day, suggesting that escape behavior is mediated by both camouflage and thermoregulation.In Zambia we thank the Bruce-Miller, Duckett and Nicolle families, Collins Moya and numerous other nest-finding assistants and land-owners, Lackson Chama, and the Zambia Wildlife Authority. We also thank Tony Fulford and are grateful for the helpful comments provided by Tim Caro, Innes Cuthill, Daniel Osorio, and two anonymous referees. J.T., J.W-A. and M.S. were funded by a Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/J018309/1 to M.S., and a BBSRC David Phillips Research Fellowship (BB/G022887/1) to M.S., and C.N.S was funded by a Royal Society Dorothy Hodgkin Fellowship, a BBSRC David Phillips Fellowship (BB/J014109/1) and the DST-NRF Centre of Excellence at the Percy FitzPatrick Institute.This is the author accepted manuscript. It is currently under an indefinite embargo pending publication by University of Chicago Press

A customizable, low-cost optomotor apparatus: a powerful tool for behaviourally measuring visual capability

This is the final version. Available on open access from Wiley via the DOI in this recordData Accessibility: A full parts list, 3D models, assembly instructions, and microcontroller code are provided under Creative Commons license at the GitHub repository (https://github.com/troscianko/optomotor) (DOI: 10.5281/zenodo.3840063) and as supplementary material. Construction guide, video guide, user forum, and future updates are provided here: http://www.empiricalimaging.com/optomotor/.1. Vision is the dominant sense for many animals, and there is an enormous diversity in visual capabilities. Understanding the visual abilities of a given species can therefore be key for investigating its behaviour and evolution. However, many techniques for quantifying visual capability are expensive, require specialized equipment, or are terminal for the animal. 2. Here, we discuss how to measure the optomotor (or optokinetic) response, an innate response that can be elicited without any training in a wide range of taxa, and which is quantifiable, accessible, and non-invasive, and provide guidance for carrying out optomotor experiments. 3. We provide instructions for building a customizable, programmable optomotor apparatus using 3D-printed and low-cost materials, discuss experimental design considerations for optomotor assays, include a guide that calculates the dimensions of stimuli of varying spatial frequency, and provide a table summarizing experimental parameters in prior optomotor experiments across a range of species. 4. Ultimately, making this simple technique more accessible will allow more researchers to incorporate measures of visual capability into their work. Additionally, the low cost and ease of construction of our apparatus will allow educators in a variety of settings to include optomotor assays in classroom activities or demonstrations. Although here we focus on using optomotor to measure visual acuity—the ability to perceive detail—the apparatus and stimuli described here can be adapted to measure visual capabilities including spectral, contrast, and polarization sensitivity, as well as motion detection, among others.European Union Horizon 2020Natural Environment Research Council (NERC)Royal Societ