Reward history modulates visual attention in an avian model.

Attention can be biased towards previously reward-associated stimuli even when they are task-irrelevant and physically non-salient, although studies of reward-modulated attention have been largely limited to primate (including human and nonhuman) models. Birds have been shown to have the capacity to discriminate reward and spatial cues in a manner similar to primates, but whether reward history involuntarily affects their attention in the same way remains unclear. We adapted a spatial cueing paradigm with differential rewards to investigate how reward modulates the allocation of attention in peafowl (Pavo cristatus). The birds were required to locate and peck a target on a computer screen that was preceded by a high-value or low-value color cue that was uninformative with respect to the location of the upcoming target. All birds exhibited a validity effect (performance enhanced on valid compared to invalid cue), and an interaction effect between value and validity was evident at the group level, being particularly pronounced in the birds with the greatest amount of reward training. The time course of reward learning was conspicuously incremental, phenomenologically slower compared to primates. Our findings suggest a similar influence of reward history on attention across phylogeny despite a significant difference in neuroanatomy.

The gaze of a social monkey is perceptible to conspecifics and predators but not prey.

Eye gaze is an important source of information for animals, implicated in communication, cooperation, hunting and antipredator behaviour. Gaze perception and its cognitive underpinnings are much studied in primates, but the specific features that are used to estimate gaze can be difficult to isolate behaviourally. We photographed 13 laboratory-housed tufted capuchin monkeys (Sapajus [Cebus] apella) to quantify chromatic and achromatic contrasts between their iris, pupil, sclera and skin. We used colour vision models to quantify the degree to which capuchin eye gaze is discriminable to capuchins, their predators and their prey. We found that capuchins, regardless of their colour vision phenotype, as well as their predators, were capable of effectively discriminating capuchin gaze across ecologically relevant distances. Their prey, in contrast, were not capable of discriminating capuchin gaze, even under relatively ideal conditions. These results suggest that specific features of primate eyes can influence gaze perception, both within and across species.

A songbird strategically modifies its blinking behavior when viewing human faces.

Even though blinking is necessary to maintain clear vision in many species, blinking is likely costly because it temporarily impairs vision. Given this cost, individuals can strategically modify their blinking behavior to minimize information loss. We tested whether a songbird species modifies its blinking behavior when viewing potential threats (human faces). We recorded the blinking behavior of captive great-tailed grackles (Quiscalus mexicanus) before, during, and after they viewed human face stimuli or control stimuli (tree bark as well as scrambled versions of human faces and tree bark). We found that the birds inhibited their blinking behavior the most when viewing human faces versus controls. In addition, they inhibited their blinking behavior more when viewing human faces that were directed rather than averted. Furthermore, when viewing the human faces, their blinking behavior was modified based on reactivity. These results suggest that a songbird can strategically modify its blinking behavior based on its perceived level of risk.

Great-tailed grackles can independently direct their eyes toward different targets.

Many species use eye movements to direct their overt attention toward specific targets within their environments. Some species can move each eye independently but we have a limited understanding of whether they can simultaneously monitor different targets with each eye. This study, therefore, tested whether a songbird can independently move its eyes towards two different targets. Captive great-tailed grackles (Quiscalus mexicanus) were simultaneously presented with one target in their left visual field and another target in their right visual field; the targets were both in the upper visual fields, both in the lower visual fields, or one target was in the upper visual field of one eye, while the other target was in the lower visual field of the other eye. The grackles correctly directed their left and right eyes toward the targets regardless of where the targets appeared at levels greater than chance. These results demonstrate that an avian species can perform simultaneous eye movements towards two different targets.

A songbird inhibits blinking behaviour in flight.

Visual attention plays a fundamental role in avian flight but attention is likely limited whenever birds blink. Because blinks are necessary to maintaining proper vision, this study tested the hypothesis that birds strategically inhibit their blinks in flight. The blinks of captive great-tailed grackles (Quiscalus mexicanus) were recorded before, during and after they flew a short distance in an open environment. The grackles spent the least amount of time blinking in flight (take-off, during flight and landing) and the most amount of time blinking at impact. Their blinking behaviour was similar before and after flight. These results suggest that grackles strategically inhibit their blinking behaviour in flight, potentially because blinks impose costs to avian flight.

Conjugate eye movements guide jumping locomotion in an avian species.

Many animals rely on vision to successfully locomote through their environments. However, our understanding of the interaction between vision and locomotion is surprisingly limited. This study therefore examined the visual mechanisms guiding jumping locomotion in an avian species. It recorded the eye movements of captive Indian peafowl (Pavo cristatus) as they jumped up onto and down from a perch. Peafowl shifted their eyes forward as they were jumping, increasing the degree of binocular overlap. Their eye movements were highly conjugate as they were jumping but were otherwise loosely conjugate. Finally, the peafowl rarely directed their gaze toward landing spots. These results suggest that eye movements play a central role in avian locomotion and they can vary depending on the specific locomotor task.

Selective attention in peacocks during assessment of rival males.

Males in many species compete intensely for access to females. In order to minimize costly interactions, they can assess their rivals' competitive abilities by evaluating traits and behaviors. We know little about how males selectively direct their attention to make these assessments. Using Indian peafowl (Pavo cristatus) as a model system, we examined how males visually assess their competitors by continuously tracking the gaze of freely moving peacocks during the mating season. When assessing rivals, peacocks selectively gazed toward the lower display regions of their rivals, including the lower eyespot and fishtail feathers, dense feathers, body and wings. Their attention was modified based on the rivals' behavior such that they spent more time looking at rivals when rivals were shaking their wings and moving. The results indicate that peacocks selectively allocate their attention during rival assessment. The gaze patterns of males assessing rivals were largely similar to those of females evaluating mates, suggesting that some male traits serve a dual function in both intra- and intersexual selection. However, males spent more time than females looking at the upper eyespots and this could indicate that the upper eyespots function more in close-up rival assessment than mate choice.

Eye and head movements shape gaze shifts in Indian peafowl.

Animals selectively direct their visual attention toward relevant aspects of their environments. They can shift their attention using a combination of eye, head and body movements. While we have a growing understanding of eye and head movements in mammals, we know little about these processes in birds. We therefore measured the eye and head movements of freely behaving Indian peafowl (Pavo cristatus) using a telemetric eye-tracker. Both eye and head movements contributed to gaze changes in peafowl. When gaze shifts were smaller, eye movements played a larger role than when gaze shifts were larger. The duration and velocity of eye and head movements were positively related to the size of the eye and head movements, respectively. In addition, the coordination of eye and head movements in peafowl differed from that in mammals; peafowl exhibited a near-absence of the vestibulo-ocular reflex, which may partly result from the peafowl's ability to move their heads as quickly as their eyes.

Selective attention in peacocks during predator detection.

Predation can exert strong selective pressure on the evolution of behavioral and morphological traits in birds. Because predator avoidance is key to survival and birds rely heavily on visual perception, predation may have shaped avian visual systems as well. To address this question, we examined the role of visual attention in antipredator behavior in peacocks (Pavo cristatus). Peacocks were exposed to a model predator while their gaze was continuously recorded with a telemetric eye-tracker. We found that peacocks spent more time looking at and made more fixations on the predator compared to the same spatial location before the predator was revealed. The duration of fixations they directed toward conspecifics and environmental features decreased after the predator was revealed, indicating that the peacocks were rapidly scanning their environment with their eyes. Maximum eye movement amplitudes and amplitudes of consecutive saccades were similar before and after the predator was revealed. In cases where conspecifics detected the predator first, peacocks appeared to learn that danger was present by observing conspecifics' antipredator behavior. Peacocks were faster to detect the predator when they were fixating closer to the area where the predator would eventually appear. In addition, pupil size increased after predator exposure, consistent with increased physiological arousal. These findings demonstrate that peacocks selectively direct their attention toward predatory threats and suggest that predation has influenced the evolution of visual orienting systems.

Peafowl antipredator calls encode information about signalers.

Animals emit vocalizations that convey information about external events. Many of these vocalizations, including those emitted in response to predators, also encode information about the individual that produced the call. The relationship between acoustic features of antipredator calls and information relating to signalers (including sex, identity, body size, and social rank) were examined in peafowl (Pavo cristatus). The "bu-girk" antipredator calls of male and female peafowl were recorded and 20 acoustic parameters were automatically extracted from each call. Both the bu and girk elements of the antipredator call were individually distinctive and calls were classified to the correct signaler with over 90% and 70% accuracy in females and males, respectively. Females produced calls with a higher fundamental frequency (F0) than males. In both females and males, body size was negatively correlated with F0. In addition, peahen rank was related to the duration, end mean frequency, and start harmonicity of the bu element. Peafowl antipredator calls contain detailed information about the signaler and can potentially be used by receivers to respond to dangerous situations.

Through their eyes: selective attention in peahens during courtship.

Conspicuous, multicomponent ornamentation in male animals can be favored by female mate choice but we know little about the cognitive processes females use to evaluate these traits. Sexual selection may favor attention mechanisms allowing the choosing females to selectively and efficiently acquire relevant information from complex male display traits and, in turn, may favor male display traits that effectively capture and hold female attention. Using a miniaturized telemetric gaze-tracker, we show that peahens (Pavo cristatus) selectively attend to specific components of peacock courtship displays and virtually ignore other, highly conspicuous components. Females gazed at the lower train but largely ignored the head, crest and upper train. When the lower train was obscured, however, females spent more time gazing at the upper train and approached the upper train from a distance. Our results suggest that peahens mainly evaluate the lower train during close-up courtship but use the upper train as a long-distance attraction signal. Furthermore, we found that behavioral display components (train rattling and wing shaking) captured and maintained female attention, indicating that interactions between display components may promote the evolution of multicomponent displays. Taken together, these findings suggest that selective attention plays a crucial role in sexual selection and likely influences the evolution of male display traits.

Gut microbiome diversity and composition is associated with exploratory behavior in a wild-caught songbird.

BACKGROUND: The gut microbiome influences its host in a myriad of ways, from immune system development to nutrient utilization. However, our understanding of the relationship between the gut microbiome and behavior, especially in wild species, is still poor. One behavior that potentially interacts with the gut microbiome is exploratory behavior, which animals use to acquire new information from the environment. We hypothesized that diversity of the gut microbiome will be correlated with exploratory behavior in a wild-caught bird species. To test this hypothesis, we captured wild house sparrows (Passer domesticus) and collected fecal samples to measure the diversity of their gut microbiomes. We then introduced individuals to a novel environment and measured their exploratory behavior. RESULTS: We found that birds with higher alpha diversity of the gut microbiome exhibited higher exploratory behavior. These results suggest that high exploratory birds encounter more types of environmental microbes that contribute to their diverse gut microbiome compared with less exploratory birds. Alternatively, increased gut microbiome diversity may contribute to increased exploratory behavior. We also found differences in beta diversity when comparing high and low exploring birds, indicating differences in microbiome community structure. When comparing predicted functional pathways of the birds' microbiomes, we found that the microbiomes of high explorers contained more pathways involved in biofilm formation and xenobiotic degradation than those of low explorers. CONCLUSIONS: Overall, we found that the alpha and beta diversity of the gut microbiome is correlated with exploratory behavior of house sparrows. The predicted functions of the gut microbiome from high explorers differs from that of low explorers. Our study highlights the importance of considering the gut microbiome when investigating animal behavior.

Brief exposure to captivity in a songbird is associated with reduced diversity and altered composition of the gut microbiome.

The gut microbiome is important for host fitness and is influenced by many factors including the host's environment. Captive environments could potentially influence the richness and composition of the microbiome and understanding these effects could be useful information for the care and study of millions of animals in captivity. While previous studies have found that the microbiome often changes due to captivity, they have not examined how quickly these changes can occur. We predicted that the richness of the gut microbiome of wild-caught birds would decrease with brief exposure to captivity and that their microbiome communities would become more homogeneous. To test these predictions, we captured wild house sparrows (Passer domesticus) and collected fecal samples to measure their gut microbiomes immediately after capture ("wild sample") and again 5-10 days after capture ("captive sample"). There were significant differences in beta diversity between the wild and captive samples, and captive microbiome communities were more homogenous but only when using nonphylogenetic measures. Alpha diversity of the birds' microbiomes also decreased in captivity. The functional profiles of the microbiome changed, possibly reflecting differences in stress or the birds' diets before and during captivity. Overall, we found significant changes in the richness and composition of the microbiome after only a short exposure to captivity. These findings highlight the necessity of considering microbiome changes in captive animals for research and conservation purposes.

Dopamine receptor activation elicits a possible stress-related coping behavior in a wild-caught songbird.

Animals experience stress throughout their lives and exhibit both physiological and behavioral responses to cope with it. The stress response can become harmful when prolonged and increasing evidence suggests that dopamine plays a critical role in extinguishing the stress response. In particular, activation of the D2 dopamine receptor reduces glucocorticoids and increases coping behavior, i.e., behavioral responses to adverse stimuli that reduce the harmful effects of stress. However, few studies have examined the effects of dopamine on the stress responses of wild species. We therefore tested the hypothesis that activation of the D2 dopamine receptor influences coping-like behavior in a wild-caught species. We recorded behavior of house sparrows (Passer domesticus) before and after they received injections of D2 dopamine agonists, D2 dopamine antagonists, or saline. House sparrows are common in urban environments and understanding how they cope with stress may help us better understand how animals cope with urban stressors. We found that the birds significantly increased biting of inanimate objects after the agonist but there was no change following the antagonist or saline. The biting of inanimate objects may be a mechanism of behavioral coping. This change in biting behavior was not correlated with general movement. This study supports the hypothesis that D2 dopamine receptor activation is involved in the regulation of the stress response in a wild bird.

Circulating Hormones and Dominance Status Predict Female Behavior during Courtship in a Lekking Species.

Female competitive behaviors during courtship can have substantial fitness consequences, yet we know little about the physiological and social mechanisms underlying these behaviors-particularly for females of polygynous lek mating species. We explored the hormonal and social drivers of female intersexual and intrasexual behavior during courtship by males in a captive population of Indian peafowl. We investigated whether (1) female non-stress induced circulating estradiol (E2) and corticosterone (CORT) levels or (2) female dominance status in a dyad predicts female solicitation behavior. We also tested whether female circulating E2 and CORT predict dominant females' aggressive behaviors toward subordinate females in the courtship context. Our findings demonstrate that females with higher levels of circulating E2 as well as higher levels of circulating CORT solicit more courtships from males. Dominant females also solicit more courtships from males than subordinate females. Female intrasexual aggressive behaviors during courtship, however, were not associated with circulating levels of E2 or CORT. Overall, we conclude that circulating steroid hormones in conjunction with social dominance might play a role in mediating female behaviors associated with competition for mates. Experimental manipulation and measures of hormonal flexibility throughout the breeding season in relation to competitive and sexual behaviors will be necessary to further examine the link between hormonal mechanisms and female behavior in polygynous lekking systems.

Chimpanzee (Pan troglodytes) gaze is conspicuous at ecologically-relevant distances.

Chimpanzee (Pan troglodytes) sclera appear much darker than the white sclera of human eyes, to such a degree that the direction of chimpanzee gaze may be concealed from conspecifics. Recent debate surrounding this topic has produced mixed results, with some evidence suggesting that (1) primate gaze is indeed concealed from their conspecifics, and (2) gaze colouration is among the suite of traits that distinguish uniquely social and cooperative humans from other primates (the cooperative eye hypothesis). Using a visual modelling approach that properly accounts for specific-specific vision, we reexamined this topic to estimate the extent to which chimpanzee eye coloration is discriminable. We photographed the faces of captive chimpanzees and quantified the discriminability of their pupil, iris, sclera, and surrounding skin. We considered biases of cameras, lighting conditions, and commercial photography software along with primate visual acuity, colour sensitivity, and discrimination ability. Our visual modeling of chimpanzee eye coloration suggests that chimpanzee gaze is visible to conspecifics at a range of distances (within approximately 10 m) appropriate for many species-typical behaviours. We also found that chimpanzee gaze is discriminable to the visual system of primates that chimpanzees prey upon, Colobus monkeys. Chimpanzee sclera colour does not effectively conceal gaze, and we discuss this result with regard to the cooperative eye hypothesis, the evolution of primate eye colouration, and methodological best practices for future primate visual ecology research.

A songbird can detect the eyes of conspecifics under daylight and artificial nighttime lighting.

Eyes convey important information about the external and internal worlds of animals. Individuals can follow the gaze of others to learn about the location of salient objects as well as assess eye qualities to evaluate the health, age or other internal states of conspecifics. Because of the increasing prevalence of artificial lighting at night (ALAN), urbanized individuals can potentially garner information from conspecific eyes under both daylight and ALAN. We tested this possibility using a visual modeling approach in which we estimated the maximum distance at which individuals could detect conspecific eyes under daylight and high levels of ALAN. We also estimated the minimum light level at which individuals could detect conspecific eyes. Great-tailed grackles (Quiscalus mexicanus) were used as our study species because they are highly social and are unusual among birds in that they regularly gather at nocturnal roosts in areas with high levels of ALAN. This visual modelling approach revealed that grackles can detect conspecific eyes under both daylight and ALAN, regardless of iris coloration. The grackles could detect conspecific eyes at farther distances in daylight compared to ALAN. Our results highlight the potential importance of lighting conditions in shaping social interactions.

Sclera color in humans facilitates gaze perception during daytime and nighttime.

Species vary widely in the conspicuousness of their eye morphology and this could influence gaze perception. Eyes with conspicuous morphology can enhance gaze perception while eyes with camouflaged morphology may hinder gaze perception. While evidence suggests that conspicuous eye morphology enhances gaze perception, little is known about how environmental conditions affect this interaction. Thus, we investigated whether environmental light conditions affect gaze perception. Human subjects (Homo sapiens) were instructed to find direct-gaze faces within arrays of averted-gaze faces or to find averted-gaze faces within arrays of directed-gaze faces. The faces were displayed under conditions simulating nighttime or daytime conditions. Furthermore, the faces had naturally-colored sclera (white) or modified sclera (same color as the iris). Participants were fastest and most accurate in detecting faces during the daytime and nighttime conditions when the sclera were naturally-colored. Participants were worst at detecting faces with modified sclera during the nighttime conditions. These results suggest that eyes with conspicuous morphology enhance gaze perception during both daytime and nighttime conditions.

Sclera and Iris Color Interact to Influence Gaze Perception.

The white sclera is important in facilitating gaze perception in humans. Iris color may likewise influence gaze perception but no previous studies have directly assessed its effect. We therefore examined how the interaction between sclera and iris color influences human gaze perception. We recorded the eye movements of human participants as they performed a visual search task with human faces exhibiting directed or averted gaze. The faces either exhibited light or dark irises. In addition, the faces had sclera that were depigmented (white) or pigmented (matched the color of the iris). We found that participants were quick and accurate in evaluating gaze regardless of iris color in faces with depigmented sclera. When the sclera were pigmented, participants were slower to evaluate the gaze of faces with both light and dark irises but these effects were most pronounced in the faces with dark irises. Furthermore, participants were generally less accurate in assessing faces with pigmented sclera when the irises were dark rather than light. Our results suggest that depigmented sclera are especially important for gaze perception in faces with dark irises. Because depigmented sclera likely evolved at a time when ancestral humans exhibited dark irises, the depigmented sclera may have been crucial for efficient and accurate gaze perception in ancestral humans.

Birds adjust acoustic directionality to beam their antipredator calls to predators and conspecifics.

Animals in many vertebrate species vocalize in response to predators, but it is often unclear whether these antipredator calls function to communicate with predators, conspecifics or both. We evaluated the function of antipredator calls in 10 species of passerines by measuring the acoustic directionality of these calls in response to experimental presentations of a model predator. Acoustic directionality quantifies the radiation pattern of vocalizations and may provide evidence about the receiver of these calls. We predicted that antipredator calls would have a lower directionality if they function to communicate with surrounding conspecifics, and a higher directionality and aimed at the receiver if they function to communicate with the predator. Our results support both of these functions. Overall, the birds produce antipredator calls that have a relatively low directionality, suggesting that the calls radiate in many directions to alert conspecifics. However, birds in some species increase the directionality of their calls when facing the predator. They can even direct their calls towards the predator when facing lateral to it--effectively vocalizing sideways towards the predator. These results suggest that antipredator calls in some species are used to communicate both to conspecifics and to predators, and that birds adjust the directionality of their calls with remarkable sophistication according to the context in which they are used.