Trick of the Eye of the Beholder
.
. Male bowerbirds build elaborate bowers, or display areas, that consist of an avenue where the female stands and an arena where the male displays. Males decorate their arenas meticulously with stones, flowers, and found objects. Previous work has shown that these bowers induce forced perspective illusions in the observing females. Now
. Kelley and Endler
. (p.
. 335
. ; see the Perspective by
.
. Anderson
.
. ) show that mating success is based on components of the illusion, rather than the physical nature of the bower. Thus, females choose their mates based on a visual illusion painstakingly constructed and maintained by the displaying male.
.

. Males often produce elaborate displays that increase their attractiveness to females, and some species extend their displays to include structures or objects that are not part of their body. Such “extended phenotypes” may communicate information that cannot be transmitted by bodily signals or may provide a more reliable signal than bodily signals. However, it is unclear whether these signals are individually distinct and whether they are consistent over long periods of time. Male bowerbirds construct and decorate bowers that function in mate choice. Bower display courts constructed by male great bowerbirds (
. Ptilonorhynchus nuchalis
. ) induce a visual illusion known as forced perspective for the female viewing the male’s display over the court, and the quality of illusion is associated with mating success. We improved the quality of the forced perspective to determine whether males maintained it at the new higher level, decreased the perspective quality back to its original value, or allowed it to decay at random over time. We found that the original perspective quality was actively recovered to individual original values within 3 d. We measured forced perspective over the course of one breeding season and compared the forced perspective of individual males between two successive breeding seasons. We found that differences in the quality of visual illusion among males were consistent within and between two breeding seasons. This suggests that forced perspective is actively and strongly maintained at a different level by each individual male.
.

Camouflage is a fundamental way for animals to avoid detection and recognition. While depth information is critical for object detection and recognition, little is known about how camouflage patterns might interfere with the mechanisms of depth perception. We reveal how many common camouflage strategies could exploit 3D visual processing mechanisms.

Many animals use shading to infer the three-dimensional (3D) shape of objects, and mimicking natural shading patterns can produce the illusion of 3D form on a flat surface. Over 150 years ago, Charles Darwin noted that the ocelli (‘eyespots’) on the feathers of the great argus Argusianus argus, when held vertically during courtship displays to females, were perfectly shaded to resemble 3D hemispheres to human viewers. We tested whether these ocelli appear 3D to birds by training chickens Gallus gallus domesticus to select images of either convex or concave shapes using shading cues, and then presenting them with images of great argus ocelli. Chickens successfully learned how to discriminate between convex and concave shapes, and treated the great argus pheasant ocelli in the same way as convex training stimuli. Our findings are consistent with previous studies that birds can perceive 3D shape from shading cues in a similar manner to humans. The perception of great argus ocelli as consistent with 3D shape by avian viewers suggests that shape illusions can play a role in male courtship.

AbstractThe 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.

Living with increasing urbanisation and human populations requires resourcefulness and flexibility in wild animals’ behaviour. Animals have to adapt to anthropogenic novelty in habitat structure and resources that may not resemble, or be as beneficial as, natural resources. Herring gulls (Larus argentatus) increasingly reside in towns and cities to breed and forage, yet how gulls are adjusting their behaviour to life in urban areas is not yet fully understood. This study investigated wild herring gulls’ responses to novel and common anthropogenic objects in urban and rural locations. We also examined whether gulls’ age influenced their object response behaviour. We found that, out of the 126 individual gulls presented with objects, 34% approached them. This suggests that the majority of targeted gulls were wary or lacked interest in the experimental set-up. of the 43 gulls that approached the objects, we found that those tested in urban locations approached more slowly than their rural counterparts. Overall, gulls showed no preference for either novel or common anthropogenic objects, and age did not influence likelihood of approach, approach speed or object choice. Individuals paid most attention to the object they approached first, potentially indicative of individual preferences. Our findings indicate that most herring gulls are not as attracted to anthropogenic objects as anecdotal reports have suggested. Covering up obvious food rewards may thus help mitigate human-gull conflict over anthropogenic food sources.

During mate choice, receivers often assess the magnitude (duration, size, etc.) of signals that vary along a continuum and reflect variation in signaler quality. It is generally assumed that receivers assess this variation linearly, meaning each difference in signaling trait between signalers results in a commensurate change in receiver response. However, increasing evidence shows receivers can respond to signals non-linearly, for example through Weber’s Law of proportional processing, where discrimination between stimuli is based on proportional, rather than absolute, differences in magnitude. We quantified mate preferences of female green swordtail fish, Xiphophorus hellerii, for pairs of males differing in body size. Preferences for larger males were better predicted by the proportional difference between males (proportional processing) than the absolute difference (linear processing). This demonstration of proportional processing of a visual signal implies that receiver perception may be an important mechanism selecting against the evolution of ever-larger signaling traits.

Among fishes in the family Poeciliidae, signals such as colour patterns, ornaments, and courtship displays play important roles in mate choice and male-male competition. Despite this, visual capabilities in Poeciliids are understudied, in particular visual acuity, the ability to resolve detail. We used three methods to quantify visual acuity in male and female green swordtails (Xiphophorus helleri), a species in which body size and the length of the male’s extended caudal fin (‘sword’) serve as assessment signals during mate choice and agonistic encounters. Topographic distribution of retinal ganglion cells (RGC) was similar in all individuals and characterized by areas of high cell densities located centro-temporally and nasally, as well as a weak horizontal streak. Based on the peak density of RGC in the centro-temporal area, anatomical acuity was estimated to be approximately 3 cycles/degree (cpd) in both sexes. However, a behavioural optomotor assay found significantly lower mean acuity in males (0.8 cpd) than females (3.0 cpd), which was not explained by differences in eye size between males and females. An additional behavioural assay, in which we trained individuals to discriminate striped gratings from grey stimuli of the same mean luminance, also showed lower acuity in males (1-2 cpd) than females (2-3 cpd). Thus, although retinal anatomy predicts identical acuity in males and females, two behavioural assays found higher acuity in females than males, a sexual dimorphism which is rare outside of invertebrates. Overall, our results have implications for understanding how Poeciliids perceive visual signals during mate choice and agonistic encounters.

AbstractShadows that are produced across the surface of an object (self-shadows) are potentially an important source of information for visual systems. Animal patterns may exploit this principle for camouflage, using pictorial cues to produce false depth information that manipulates the viewer’s detection/recognition processes. However, pictorial cues could also facilitate camouflage by matching the contrast (e.g. due to shadows) of 3D backgrounds. Aside from studies of countershading (patterning that may conceal depth information), the role of self-shadows in camouflage patterns remains unclear. Here we investigated whether pictorial cues (self-shadows) increase the survival probability of moth-like prey presented to free-living wild bird predators relative to targets without these cues. We manipulated the presence of self-shadows by adjusting the illumination conditions to produce patterned targets under directional lighting (lit from above or from below; self-shadows present) or diffuse lighting (no self-shadows). We used non-patterned targets (uniform colour) as controls. We manipulated the direction of illumination because it has been linked with depth perception in birds; objects lit from above may appear convex while those lit from below can appear concave. As shadows influence contrast, which also determines detectability, we photographed the targets in situ over the observation period, allowing us to evaluate the effect of visual metrics on survival. We found some evidence that patterned targets without self-shadows had a lower probability of survival than patterned targets with self-shadows and targets with uniform colour. Surprisingly, none of the visual metrics explained variation in survival probability. However, predators increased their foraging efficiency over time, suggesting that predator learning may have overridden the benefits afforded by camouflaging coloration.

. Many animals use shading to infer the three-dimensional (3D) shape of objects, and mimicking natural shading patterns can produce the illusion of 3D form on a flat surface. Over 150 years ago, Charles Darwin noted that the ocelli (eyespots) on the feathers of the great argus
. Argusianus argus
. when held vertically during courtship displays to females, were perfectly shaded to resemble 3D hemispheres to human viewers. We tested whether these ocelli appear 3D to birds by training chickens
. Gallus gallus domesticus
. to select images of either convex or concave shapes using shading cues, and then presenting them with images of great argus ocelli. Chickens successfully learned how to discriminate between convex and concave shapes, and treated the great argus pheasant ocelli in the same way as convex training stimuli. Our findings are consistent with previous studies that birds can perceive 3D shape from shading cues in a similar manner to humans. The perception of great argus ocelli as consistent with 3D shape by avian viewers suggests that shape illusions can play a role in male courtship.
.

Wild animals encounter humans on a regular basis, but humans vary widely in their behaviour: whereas many people ignore wild animals, some people present a threat, while others encourage animals' presence through feeding. Humans thus send mixed messages to which animals must respond appropriately to be successful. Some species appear to circumvent this problem by discriminating among and/or socially learning about humans, but it is not clear whether such learning strategies are actually beneficial in most cases. Using an individual-based model, we consider how learning rate, individual recognition (IR) of humans, and social learning (SL) affect wild animals' ability to reach an optimal avoidance strategy when foraging in areas frequented by humans. We show that ‘true’ IR of humans could be costly. We also find that a fast learning rate, while useful when human populations are homogeneous or highly dangerous, can cause unwarranted avoidance in other scenarios if animals generalize. SL reduces this problem by allowing conspecifics to observe benign interactions with humans. SL and a fast learning rate also improve the viability of IR. These results provide an insight into how wild animals may be affected by, and how they may cope with, contrasting human behaviour.

Populations of herring gulls (Larus argentatus) have declined rapidly in Britain and Ireland, but this species is increasingly breeding and foraging in urban areas and has become a source of human-wildlife conflict. Although there is a large body of literature on the behaviour of herring gulls in traditional rural colonies, urban-dwelling gulls and the behavioural drivers of their apparent success in urban areas have been less studied. Gaining a better understanding of the factors that lead to negative interactions between humans and gulls would provide an insight into how human-gull conflict can be mitigated. As gulls in urban areas often forage on anthropogenic food, they are likely to interact with humans regularly and may therefore make foraging decisions based on human cues. In this thesis, I investigate whether herring gulls use behavioural cues from humans when foraging in urban areas. I first tested whether herring gulls use the direction of human gaze when approaching an anthropogenic food source. I found that herring gulls do respond to this cue: gulls took longer to approach and peck at food when they were subjected to direct gaze. I then tested whether gulls respond specifically to human eyes rather than head direction, and whether this response is influenced by gull age or location. I found that both adult and juvenile gulls responded aversively to direct gaze, and that gulls in urban areas could be approached more closely than their counterparts in rural areas. Next, I considered whether herring gulls are attracted to objects with which humans have associated. To do this, I tested whether herring gulls peck at objects more frequently after observing a human handling the object. I found that the type of object was important: gulls pecked at handled objects comprised of packaged food, but were less likely to approach and peck at handled objects when they were not food-related. Taken together, these results strongly suggest that herring gulls foraging in urban areas use human cues. Finally, I developed an individual-based model to investigate how free-living, wild animals respond to humans in a landscape where some humans provide food or behave neutrally, while others present a threat. I showed that (a) a fast learning rate is adaptive when it would be better to avoid humans but not when it would be less energetically costly to remain close to humans, (b) an ability to recognise individual humans can help animals overcome this problem, but may only be useful if animals repeatedly encounter humans who differ inter-individually in their behaviour, and (c) socially learning about humans is likely to help animals approximate an optimal avoidance strategy. These findings provide an insight into how herring gulls, and potentially other animals, are able to forage successfully in human-dominated environments. Furthermore, by understanding the cues that gulls use, people have the opportunity to modify their behaviour to reduce the frequency of negative interactions with gulls.

Many animals exhibit contrasting shapes across their surface which are thought to help conceal them from potential predators. It has been suggested that these patterns, known as disruptive markings, function by creating false edges that break up the characteristic form of the animal. Some disruptive patterns are graded in tone so that light patches become lighter and dark patches become darker at the points where they converge. Whilst this type of edge enhancement has been shown to improve camouflage efficacy, it still remains unclear how these patterns are typically expressed within real animals and how they may function within a natural setting. In chapter 1, the strength of edge enhancement was quantified for a variety of British moth species through the use of calibrated digital photography. Across the different species, the level of edge enhancement was shown to be more pronounced near the outline of the moth compared to the centre of the wing, caused by a greater offset in the dark edge. In chapter 2, the effect of edge enhancement on camouflage was tested within a natural setting against both avian and human observers. Whilst edge enhancement had no effect on the survival of targets against avian predators, it did affect detection by humans. However, this effect was dependent upon the arrangement of pattern features, with edge enhancement reducing detection when intersecting the outline of the target but increasing detection when expressed only on internal-based markings. Regardless of pattern placement, edge enhanced targets were detected from greater distances. When combined, the results from Chapter 1 and 2 suggest the efficacy of enhanced edges is greatly influenced by their arrangement within a pattern and that they provide camouflage through some function of edge disruption.

Human-wildlife conflict is one of the greatest threats to species populations worldwide. One species facing national declines in the UK is the herring gull (Larus argentatus), despite an increase in numbers in urban areas. Gulls in urban areas are often considered a nuisance owing to behaviours such as food-snatching. Whether urban gull feeding behaviour is influenced by human behavioural cues, such as gaze direction, remains unknown. We therefore measured the approach times of herring gulls to a food source placed in close proximity to an experimenter who either looked directly at the gull or looked away. We found that only 26% of targeted gulls would touch the food, suggesting that food-snatching is likely to be conducted by a minority of individuals. When gulls did touch the food, they took significantly longer to approach when the experimenter's gaze was directed towards them compared with directed away. However, inter-individual behaviour varied greatly, with some gulls approaching similarly quickly in both treatments, while others approached much more slowly when the experimenter was looking at them. These results indicate that reducing human-herring gull conflict may be possible through small changes in human behaviour, but will require consideration of behavioural differences between individual gulls.

. It is often assumed that the primary purpose of a male's sexual display is to provide information about quality, or to strongly stimulate prospective mates, but other functions of courtship displays have been relatively neglected. Male great bowerbirds (
. Ptilonorhynchus nuchalis
. ) construct bowers that exploit the female's predictable field of view (FOV) during courtship displays by creating forced perspective illusions, and the quality of illusion is a good predictor of mating success. Here, we present and discuss two additional components of male courtship displays that use the female's predetermined viewpoint: (i) the rapid and diverse flashing of coloured objects within her FOV and (ii) chromatic adaptation of the female's eyes that alters her perception of the colour of the displayed objects. Neither is directly related to mating success, but both are likely to increase signal efficacy, and may also be associated with attracting and holding the female's attention. Signal efficacy is constrained by trade-offs between the signal components; there are both positive and negative interactions within multicomponent signals. Important signal components may have a threshold effect on fitness rather than the often assumed linear relationship.
.

Trick of the Eye of the Beholder
.
. Male bowerbirds build elaborate bowers, or display areas, that consist of an avenue where the female stands and an arena where the male displays. Males decorate their arenas meticulously with stones, flowers, and found objects. Previous work has shown that these bowers induce forced perspective illusions in the observing females. Now
. Kelley and Endler
. (p.
. 335
. ; see the Perspective by
.
. Anderson
.
. ) show that mating success is based on components of the illusion, rather than the physical nature of the bower. Thus, females choose their mates based on a visual illusion painstakingly constructed and maintained by the displaying male.
.

. Males often produce elaborate displays that increase their attractiveness to females, and some species extend their displays to include structures or objects that are not part of their body. Such “extended phenotypes” may communicate information that cannot be transmitted by bodily signals or may provide a more reliable signal than bodily signals. However, it is unclear whether these signals are individually distinct and whether they are consistent over long periods of time. Male bowerbirds construct and decorate bowers that function in mate choice. Bower display courts constructed by male great bowerbirds (
. Ptilonorhynchus nuchalis
. ) induce a visual illusion known as forced perspective for the female viewing the male’s display over the court, and the quality of illusion is associated with mating success. We improved the quality of the forced perspective to determine whether males maintained it at the new higher level, decreased the perspective quality back to its original value, or allowed it to decay at random over time. We found that the original perspective quality was actively recovered to individual original values within 3 d. We measured forced perspective over the course of one breeding season and compared the forced perspective of individual males between two successive breeding seasons. We found that differences in the quality of visual illusion among males were consistent within and between two breeding seasons. This suggests that forced perspective is actively and strongly maintained at a different level by each individual male.
.

. Borgia
. et al
. raise some questions about our recent study showing that great bowerbirds create visual illusions that are used in mate choice. We address them by providing further details about our methods and results. We also provide detailed descriptions of our geometric calculations to address their measurement and analysis questions.
.

Although the presence of vocal mimicry in songbirds is well documented, the function of such impressive copying is poorly understood. One explanation for mimicry in species that predominantly mimic alarm calls and predator vocal isations is that these birds use mimicry to confuse or deter potential threats or intruders, so these vocalisations should therefore be produced when the mimic is alarmed and be uncommon in other contexts. Male bowerbirds construct bowers to display to females and anecdotal reports from the Ptilonorhynchus genus suggest that males mimic alarm sounds when disturbed at their bowers. We quantified and compared the rate of mimicry during disturbance to the bower by a human and in naturally occurring social contexts in a population of spotted bowerbirds Ptilonorhynchus maculatus. Male bowerbirds produced mimicry more than thirty times more frequently in response to bower disturbance than they did in any other context. Neither conspecifics nor heterospecifics were attracted to the bower area by mimicry. These data are consistent with the hypothesis that the production of mimicry is associated with a response to an alarming situation. Additionally, the predominance of alarm mimicry by spotted bowerbirds raises the possibility that the birds learn these sounds when they experience alarming situations and they reproduce them in subsequent alarming situations.

. Vocal mimicry is one of the more striking aspects of avian vocalization and is widespread across songbirds. However, little is known about how mimics acquire heterospecific and environmental sounds. We investigated geographical and individual variation in the mimetic repertoires of males of a proficient mimic, the spotted bowerbird
. Ptilonorhynchus maculatus
. Male bower owners shared more of their mimetic repertoires with neighbouring bower owners than with more distant males. However, interbower distance did not explain variation in the highly repeatable renditions given by bower owners of two commonly mimicked species. From the similarity between model and mimic vocalizations and the patterns of repertoire sharing among males, we suggest that the bowerbirds are learning their mimetic repertoire from heterospecifics and not from each other.
.