Ecological and morphological correlates of visual acuity in birds.

Birds use their visual systems for important tasks, such as foraging and predator detection, that require them to resolve an image. However, visual acuity (the ability to perceive spatial detail) varies by two orders of magnitude across birds. Prior studies indicate that eye size and aspects of a species' ecology may drive variation in acuity, but these studies have been restricted to small numbers of species. We used a literature review to gather data on acuity measured either behaviorally or anatomically for 94 species from 38 families. We then examined how acuity varies in relation to (1) eye size, (2) habitat spatial complexity, (3) habitat light level, (4) diet composition, (5) prey mobility and (6) foraging mode. A phylogenetically controlled model including all of the above factors as predictors indicated that eye size and foraging mode are significant predictors of acuity. Examining each ecological variable in turn revealed that acuity is higher in species whose diet comprises vertebrates or scavenged food and whose foraging modes require resolving prey from farther away. Additionally, species that live in spatially complex, vegetative habitats have lower acuity than expected for their eye sizes. Together, our results suggest that the need to detect important objects from far away - such as predators for species that live in open habitats, and food items for species that forage on vertebrate and scavenged prey - has likely been a key driver of higher acuity in some species, helping us to elucidate how visual capabilities may be adapted to an animal's visual needs.

Weber's Law.

Bullough et al. introduce Weber's Law and proportional processing during perception.

Proportional processing of a visual mate choice signal in the green swordtail, Xiphophorus hellerii.

During mate choice, receivers often assess the magnitude (duration, size, etc.) of signals that vary along a continuum and reflect variation in signaller quality. It is generally assumed that receivers assess this variation linearly, meaning each difference in signalling trait between signallers 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 signalling traits.

Does shading on great argus Argusianus argus feathers create a three-dimensional illusion?

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.

3D animal camouflage.

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.

Predator or provider? How wild animals respond to mixed messages from humans.

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.

Sex differences in behavioural and anatomical estimates of visual acuity in the green swordtail, Xiphophorus helleri.

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 (RGCs) was similar in all individuals and was 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 RGCs in the centro-temporal area, anatomical acuity was estimated to be approximately 3 cycles per 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 that is rare outside of invertebrates. Overall, our results have implications for understanding how poeciliids perceive visual signals during mate choice and agonistic encounters.

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.

The Role of Animal Cognition in Human-Wildlife Interactions.

Humans have a profound effect on the planet's ecosystems, and unprecedented rates of human population growth and urbanization have brought wild animals into increasing contact with people. For many species, appropriate responses toward humans are likely to be critical to survival and reproductive success. Although numerous studies have investigated the impacts of human activity on biodiversity and species distributions, relatively few have examined the effects of humans on the behavioral responses of animals during human-wildlife encounters, and the cognitive processes underpinning those responses. Furthermore, while humans often present a significant threat to animals, the presence or behavior of people may be also associated with benefits, such as food rewards. In scenarios where humans vary in their behavior, wild animals would be expected to benefit from the ability to discriminate between dangerous, neutral and rewarding people. Additionally, individual differences in cognitive and behavioral phenotypes and past experiences with humans may affect animals' ability to exploit human-dominated environments and respond appropriately to human cues. In this review, we examine the cues that wild animals use to modulate their behavioral responses toward humans, such as human facial features and gaze direction. We discuss when wild animals are expected to attend to certain cues, how information is used, and the cognitive mechanisms involved. We consider how the cognitive abilities of wild animals are likely to be under selection by humans and therefore influence population and community composition. We conclude by highlighting the need for long-term studies on free-living, wild animals to fully understand the causes and ecological consequences of variation in responses to human cues. The effects of humans on wildlife behavior are likely to be substantial, and a detailed understanding of these effects is key to implementing effective conservation strategies and managing human-wildlife conflict.

Finding a signal hidden among noise: how can predators overcome camouflage strategies?

Substantial progress has been made in the past 15 years regarding how prey use a variety of visual camouflage types to exploit both predator visual processing and cognition, including background matching, disruptive coloration, countershading and masquerade. By contrast, much less attention has been paid to how predators might overcome these defences. Such strategies include the evolution of more acute senses, the co-opting of other senses not targeted by camouflage, changes in cognition such as forming search images, and using behaviours that change the relationship between the cryptic individual and the environment or disturb prey and cause movement. Here, we evaluate the methods through which visual camouflage prevents detection and recognition, and discuss if and how predators might evolve, develop or learn counter-adaptations to overcome these. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

Urban herring gulls use human behavioural cues to locate food.

While many animals are negatively affected by urbanization, some species appear to thrive in urban environments. Herring gulls (Larus argentatus) are commonly found in urban areas and often scavenge food discarded by humans. Despite increasing interactions between humans and gulls, little is known about the cognitive underpinnings of urban gull behaviour and to what extent they use human behavioural cues when making foraging decisions. We investigated whether gulls are more attracted to anthropogenic items when they have been handled by a human. We first presented free-living gulls with two identical food objects, one of which was handled, and found that gulls preferentially pecked at the handled food object. We then tested whether gulls' attraction to human-handled objects generalizes to non-food items by presenting a new sample of gulls with two non-food objects, where, again, only one was handled. While similar numbers of gulls approached food and non-food objects in both experiments, they did not peck at handled non-food objects above chance levels. These results suggest that urban gulls generally show low levels of neophobia, but that they use human handling as a cue specifically in the context of food. These behaviours may contribute to gulls' successful exploitation of urban environments.

Herring gulls respond to human gaze direction.

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.

California scrub-jays reduce visual cues available to potential pilferers by matching food colour to caching substrate.

Some animals hide food to consume later; however, these caches are susceptible to theft by conspecifics and heterospecifics. Caching animals can use protective strategies to minimize sensory cues available to potential pilferers, such as caching in shaded areas and in quiet substrate. Background matching (where object patterning matches the visual background) is commonly seen in prey animals to reduce conspicuousness, and caching animals may also use this tactic to hide caches, for example, by hiding coloured food in a similar coloured substrate. We tested whether California scrub-jays (Aphelocoma californica) camouflage their food in this way by offering them caching substrates that either matched or did not match the colour of food available for caching. We also determined whether this caching behaviour was sensitive to social context by allowing the birds to cache when a conspecific potential pilferer could be both heard and seen (acoustic and visual cues present), or unseen (acoustic cues only). When caching events could be both heard and seen by a potential pilferer, birds cached randomly in matching and non-matching substrates. However, they preferentially hid food in the substrate that matched the food colour when only acoustic cues were present. This is a novel cache protection strategy that also appears to be sensitive to social context. We conclude that studies of cache protection strategies should consider the perceptual capabilities of the cacher and potential pilferers.

How do great bowerbirds construct perspective illusions?

Many animals build structures to provide shelter, avoid predation, attract mates or house offspring, but the behaviour and potential cognitive processes involved during building are poorly understood. Great bowerbird (Ptilinorhynchus nuchalis) males build and maintain display courts by placing tens to hundreds of objects in a positive size-distance gradient. The visual angles created by the gradient create a forced perspective illusion that females can use to choose a mate. Although the quality of illusion is consistent within males, it varies among males, which may reflect differences in how individuals reconstruct their courts. We moved all objects off display courts to determine how males reconstructed the visual illusion. We found that all individuals rapidly created the positive size-distance gradient required for forced perspective within the first 10 objects placed. Males began court reconstruction by placing objects in the centre of the court and then placing objects further out, a technique commonly used when humans lay mosaics. The number of objects present after 72 h was not related to mating success or the quality of the illusion, indicating that male skill at arranging objects rather than absolute number of objects appears to be important. We conclude that differences arise in the quality of forced perspective illusions despite males using the same technique to reconstruct their courts.

Visual effects in great bowerbird sexual displays and their implications for signal design.

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.

Male great bowerbirds create forced perspective illusions with consistently different individual quality.

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.

Illusions promote mating success in great bowerbirds.

Sexual selection studies normally compare signal strengths, but signal components and sensory processing may interact to create misleading or attention-capturing illusions. Visual illusions can be produced by altering object and scene geometry in ways that trick the viewer when seen from a particular direction. Male great bowerbirds actively maintain size-distance gradients of objects on their bower courts that create forced-perspective illusions for females viewing their displays from within the bower avenue. We show a significant relationship between mating success and the female's view of the gradient; this view explains substantially more variance in mating success than the strength of the gradients. Illusions may be widespread in other animals because males of most species display to females with characteristic orientation and distance, providing excellent conditions for illusions.

The mimetic repertoire of the spotted bowerbird Ptilonorhynchus maculatus.

Although vocal mimicry in songbirds is well documented, little is known about the function of such mimicry. One possibility is that the mimic produces the vocalisations of predatory or aggressive species to deter potential predators or competitors. Alternatively, these sounds may be learned in error as a result of their acoustic properties such as structural simplicity. We determined the mimetic repertoires of a population of male spotted bowerbirds Ptilonorhynchus maculatus, a species that mimics predatory and aggressive species. Although male mimetic repertoires contained an overabundance of vocalisations produced by species that were generally aggressive, there was also a marked prevalence of mimicry of sounds that are associated with alarm such as predator calls, alarm calls and mobbing calls, irrespective of whether the species being mimicked was aggressive or not. We propose that it may be the alarming context in which these sounds are first heard that may lead both to their acquisition and to their later reproduction. We suggest that enhanced learning capability during acute stress may explain vocal mimicry in many species that mimic sounds associated with alarm.

Transforming growth factor-ß: activation by neuraminidase and role in highly pathogenic H5N1 influenza pathogenesis.

Transforming growth factor-beta (TGF-ß), a multifunctional cytokine regulating several immunologic processes, is expressed by virtually all cells as a biologically inactive molecule termed latent TGF-ß (LTGF-ß). We have previously shown that TGF-ß activity increases during influenza virus infection in mice and suggested that the neuraminidase (NA) protein mediates this activation. In the current study, we determined the mechanism of activation of LTGF-ß by NA from the influenza virus A/Gray Teal/Australia/2/1979 by mobility shift and enzyme inhibition assays. We also investigated whether exogenous TGF-ß administered via a replication-deficient adenovirus vector provides protection from H5N1 influenza pathogenesis and whether depletion of TGF-ß during virus infection increases morbidity in mice. We found that both the influenza and bacterial NA activate LTGF-ß by removing sialic acid motifs from LTGF-ß, each NA being specific for the sialic acid linkages cleaved. Further, NA likely activates LTGF-ß primarily via its enzymatic activity, but proteases might also play a role in this process. Several influenza A virus subtypes (H1N1, H1N2, H3N2, H5N9, H6N1, and H7N3) except the highly pathogenic H5N1 strains activated LTGF-ß in vitro and in vivo. Addition of exogenous TGF-ß to H5N1 influenza virus-infected mice delayed mortality and reduced viral titers whereas neutralization of TGF-ß during H5N1 and pandemic 2009 H1N1 infection increased morbidity. Together, these data show that microbe-associated NAs can directly activate LTGF-ß and that TGF-ß plays a pivotal role protecting the host from influenza pathogenesis.