Spatial memory predicts home range size and predation risk in pheasants.

Most animals confine their activities to a discrete home range, long assumed to reflect the fitness benefits of obtaining spatial knowledge about the landscape. However, few empirical studies have linked spatial memory to home range development or determined how selection operates on spatial memory via the latter's role in mediating space use. We assayed the cognitive ability of juvenile pheasants (Phasianus colchicus) reared under identical conditions before releasing them into the wild. Then, we used high-throughput tracking to record their movements as they developed their home ranges, and determined the location, timing and cause of mortality events. Individuals with greater spatial reference memory developed larger home ranges. Mortality risk from predators was highest at the periphery of an individual's home range in areas where they had less experience and opportunity to obtain spatial information. Predation risk was lower in individuals with greater spatial memory and larger core home ranges, suggesting selection may operate on spatial memory by increasing the ability to learn about predation risk across the landscape. Our results reveal that spatial memory, determined from abstract cognitive assays, shapes home range development and variation, and suggests predation risk selects for spatial memory via experience-dependent spatial variation in mortality.

Spatial cognitive ability is associated with transitory movement speed but not straightness during the early stages of exploration.

Memories about the spatial environment, such as the locations of foraging patches, are expected to affect how individuals move around the landscape. However, individuals differ in the ability to remember spatial locations (spatial cognitive ability) and evidence is growing that these inter-individual differences influence a range of fitness proxies. Yet empirical evaluations directly linking inter-individual variation in spatial cognitive ability and the development and structure of movement paths are lacking. We assessed the performance of young pheasants (Phasianus colchicus) on a spatial cognition task before releasing them into a novel, rural landscape and tracking their movements. We quantified changes in the straightness and speed of their transitory paths over one month. Birds with better performances on the task initially made slower transitory paths than poor performers but by the end of the month, there was no difference in speed. In general, birds increased the straightness of their path over time, indicating improved efficiency independent of speed, but this was not related to performance on the cognitive task. We suggest that initial slow movements may facilitate more detailed information gathering by better performers and indicates a potential link between an individual's spatial cognitive ability and their movement behaviour.

The modularity of a social group does not affect the transmission speed of a novel, socially learned behaviour, or the formation of local variants.

The structure of a group is critical in determining how a socially learnt behaviour will spread. Predictions from theoretical models indicate that specific parameters of social structure differentially influence social transmission. Modularity describes how the structure of a group or network is divided into distinct subgroups or clusters. Theoretical modelling indicates that the modularity of a network will predict the rate of behavioural spread within a group, with higher modularity slowing the rate of spread and facilitating the establishment of local behavioural variants which can prelude local cultures. Despite prolific modelling approaches, empirical tests via manipulations of group structure remain scarce. We experimentally manipulated the modularity of populations of domestic fowl chicks, Gallus gallus domesticus, to affect the transmission of a novel foraging behaviour. We compared the spread of behaviour in populations with networks of high or low modularity against control populations where social transmission was prevented. We found the foraging behaviour to spread socially between individuals when the social transmission was permitted; however, modularity did not increase the speed of behavioural spread nor lead to the initial establishments of shared behavioural variants. This result suggests that factors in the social transmission process additional to the network structure may influence behavioural spread.

Is habitat selection in the wild shaped by individual-level cognitive biases in orientation strategy?

Cognitive biases for encoding spatial information (orientation strategies) in relation to self (egocentric) or landmarks (allocentric) differ between species or populations according to the habitats they occupy. Whether biases in orientation strategy determine early habitat selection or if individuals adapt their biases following experience is unknown. We determined orientation strategies of pheasants, Phasianus colchicus, using a dual-strategy maze with an allocentric probe trial, before releasing them (n = 20) into a novel landscape, where we monitored their movement and habitat selection. In general, pheasants selected for woodland over non-woodland habitat, but allocentric-biased individuals exhibited weaker avoidance of non-woodland habitat, where we expected allocentric navigation to be more effective. Sex did not influence selection but was associated with speed and directional persistence in non-woodland habitat. Our results suggest that an individual's habitat selection is associated with inherent cognitive bias in early life, but it is not yet clear what advantages this may offer.

Heritability and correlations among learning and inhibitory control traits.

To understand the evolution of cognitive abilities, we need to understand both how selection acts upon them and their genetic (co)variance structure. Recent work suggests that there are fitness consequences for free-living individuals with particular cognitive abilities. However, our current understanding of the heritability of these abilities is restricted to domesticated species subjected to artificial selection. We investigated genetic variance for, and genetic correlations among four cognitive abilities: inhibitory control, visual and spatial discrimination, and spatial ability, measured on >450 pheasants, Phasianus colchicus, over four generations. Pheasants were reared in captivity but bred from adults that lived in the wild and hence, were subject to selection on survival. Pheasant chicks are precocial and were reared without parents, enabling us to standardize environmental and parental care effects. We constructed a pedigree based on 15 microsatellite loci and implemented animal models to estimate heritability. We found moderate heritabilities for discrimination learning and inhibitory control (h2 = 0.17-0.23) but heritability for spatial ability was low (h2 = 0.09). Genetic correlations among-traits were largely positive but characterized by high uncertainty and were not statistically significant. Principle component analysis of the genetic correlation matrix estimate revealed a leading component that explained 69% of the variation, broadly in line with expectations under a general intelligence model of cognition. However, this pattern was not apparent in the phenotypic correlation structure which was more consistent with a modular view of animal cognition. Our findings highlight that the expression of cognitive traits is influenced by environmental factors which masks the underlying genetic structure.

A Matador-like Predator Diversion Strategy Driven by Conspicuous Coloration in Guppies.

Understanding the adaptive function of conspicuous coloration has been a major focus of evolutionary biology for much of the last century. Although considerable progress has been made in explaining how conspicuous coloration can be used in functions as diverse as sexual and social signaling, startling predators, and advertising toxicity [1], there remain a multitude of species that display conspicuous coloration that cannot be explained by existing theory. Here we detail a new "matador-like" divertive antipredator strategy based on conspicuous coloration in Trinidadian guppies (Poecilia reticulata). Guppies encountering predatory fish rapidly enhance the conspicuousness of their eyes by blackening their irises. By pitting biomimetic robotic guppies against real predatory fish, we show this conspicuous eye coloration diverts attacks away from the guppies' center of mass to their head. To determine the function of this seemingly counterintuitive behavior, we developed a method for simulating escape probabilities when live prey interact with ballistic attacking predators, and find this diversion effect significantly benefits black-eyed guppies because they evade capture by rapidly pivoting away from the predator once it has committed to its attack. Remarkably, this antipredator strategy reverses the commonly observed negative scaling relationship between prey size and evasive ability, with larger fish benefiting most from diverting predators. Taken together, our results introduce a new antipredator divertive strategy that may be widely used by conspicuously colored prey that rely on agility to escape their predators.

The inhibitory control of pheasants (Phasianus colchicus) weakens when previously learned environmental information becomes unpredictable.

Inhibitory control (IC) is the ability to intentionally restrain initial, ineffective responses to a stimulus and instead exhibit an alternative behaviour that is not pre-potent but which effectively attains a reward. Individuals (both humans and non-human animals) differ in their IC, perhaps as a result of the different environmental conditions they have experienced. We experimentally manipulated environmental predictability, specifically how reliable information linking a cue to a reward was, over a very short time period and tested how this affected an individual's IC. We gave 119 pheasants (Phasianus colchicus) the opportunity to learn to associate a visual cue with a food reward in a binary choice task. We then perturbed this association for half the birds, whereas control birds continued to be rewarded when making the correct choice. We immediately measured all birds' on a detour IC task and again 3 days later. Perturbed birds immediately performed worse than control birds, making more unrewarded pecks at the apparatus than control birds, although this effect was less for individuals that had more accurately learned the initial association. The effect of the perturbation was not seen 3 days later, suggesting that individual IC performance is highly plastic and susceptible to recent changes in environmental predictability. Specifically, individuals may perform poorly in activities requiring IC immediately after information in their environment is perturbed, with the perturbation inducing emotional arousal. Our finding that recent environmental changes can affect IC performance, depending on how well an animal has learned about that environment, means that interpreting individual differences in IC must account for both prior experience and relevant individual learning abilities.

Response learning confounds assays of inhibitory control on detour tasks.

The ability to inhibit prepotent actions towards rewards that are made inaccessible by transparent barriers has been considered to reflect capacities for inhibitory control (IC). Typically, subjects initially reach directly, and incorrectly, for the reward. With experience, subjects may inhibit this action and instead detour around barriers to access the reward. However, assays of IC are often measured across multiple trials, with the location of the reward remaining constant. Consequently, other cognitive processes, such as response learning (acquisition of a motor routine), may confound accurate assays of IC. We measured baseline IC capacities in pheasant chicks, Phasianus colchicus, using a transparent cylinder task. Birds were then divided into two training treatments, where they learned to access a reward placed behind a transparent barrier, but experienced differential reinforcement of a particular motor response. In the stationary-barrier treatment, the location of the barrier remained constant across trials. We, therefore, reinforced a fixed motor response, such as always go left, which birds could learn to aid their performance. Conversely, we alternated the location of the barrier across trials for birds in the moving-barrier treatment and hence provided less reinforcement of their response learning. All birds then experienced a second presentation of the transparent cylinder task to assess whether differences in the training treatments influenced their subsequent capacities for IC. Birds in the stationary-barrier treatment showed a greater improvement in their subsequent IC performance after training compared to birds in the moving-barrier treatment. We, therefore, suggest that response learning aids IC performance on detour tasks. Consequently, non-target cognitive processes associated with different neural substrates appear to underlie performances on detour tasks, which may confound accurate assays of IC. Our findings question the construct validity of a commonly used paradigm that is widely considered to assess capacities for IC in humans and other animals.

Unpredictable environments enhance inhibitory control in pheasants.

The ability to control impulsive actions is an important executive function that is central to the self-regulation of behaviours and, in humans, can have important implications for mental and physical health. One key factor that promotes individual differences in inhibitory control (IC) is the predictability of environmental information experienced during development (i.e. reliability of resources and social trust). However, environmental predictability can also influence motivational and other cognitive abilities, which may therefore confound interpretations of the mechanisms underlying IC. We investigated the role of environmental predictability, food motivation and cognition on IC. We reared pheasant chicks, Phasianus colchicus, under standardised conditions, in which birds experienced environments that differed in their spatial predictability. We systematically manipulated spatial predictability during their first 8 weeks of life, by either moving partitions daily to random locations (unpredictable environment) or leaving them in fixed locations (predictable environment). We assessed motivation by presenting pheasants with two different foraging tasks that measured their dietary breadth and persistence to acquire inaccessible food rewards, as well as recording their latencies to acquire a freely available baseline worm positioned adjacent to each test apparatus, their body condition (mass/tarsus3) and sex. We assessed cognitive performance by presenting each bird with an 80-trial binary colour discrimination task. IC was assessed using a transparent detour apparatus, which required subjects to inhibit prepotent attempts to directly acquire a visible reward through the barrier and instead detour around a barrier. We found greater capacities for IC in pheasants that were reared in spatially unpredictable environments compared to those reared in predictable environments. While IC was unrelated to individual differences in cognitive performance on the colour discrimination task or motivational measures, we found that environmental predictability had differential effects on sex. Males reared in an unpredictable environment, and all females regardless of their rearing environment, were less persistent than males reared in a predictable environment. Our findings, therefore, suggest that an individual's developmental experience can influence their performance on IC tasks.

Intra-individual variation in performance on novel variants of similar tasks influences single factor explanations of general cognitive processes.

Intra-individual variation in performance within and across cognitive domains may confound interpretations of both domain-general and domain-specific abilities. Such variation is rarely considered in animal test batteries. We investigate individual consistency in performance by presenting pheasant chicks (n = 31), raised under standardized conditions, with nine different cognitive tasks. Among these tasks were two replicated novel variants of colour learning and colour reversal problems, tests of positional learning and memory, as well as two different tasks that captured multiple putative measures of inhibitory control and motor-related performance. These task variants were also used to compare subjects' performance on alternative test batteries comprised of different task combinations. Subjects' performance improved with experience, yet we found relatively little consistency in their performance, both within similar tasks using different paradigms and across different tasks. Parallel analysis revealed non-significant factors when all nine tasks were included in a principal axis factor analysis. However, when different combinations of six of the nine tasks were included in principal axis factoring, 14 of 84 combinations revealed significant main factors, explaining between 28 and 35% of the variance in task performance. While comparable findings have been suggested to reflect domain-general intelligence in other species, we found no evidence to suggest that a single factor encompassed a diverse range of cognitive abilities in pheasants. Instead, we reveal how single factor explanations of cognitive processes can be influenced by test battery composition and intra-individual variation in performance across tasks. Our findings highlight the importance of conducting multiple tests within specific domains to ensure robust cognitive measures are obtained.

Dynamic eye colour as an honest signal of aggression.

Animal eyes are some of the most widely recognisable structures in nature. Due to their salience to predators and prey, most research has focused on how animals hide or camouflage their eyes [1]. However, across all vertebrate Classes, many species actually express brightly coloured or conspicuous eyes, suggesting they may have also evolved a signalling function. Nevertheless, perhaps due to the difficulty with experimentally manipulating eye appearance, very few species beyond humans [2] have been experimentally shown to use eyes as signals [3]. Using staged behavioural trials we show that Trinidadian guppies (Poecilia reticulata), which can rapidly change their iris colour, predominantly express conspicuous eye colouration when performing aggressive behaviours towards smaller conspecifics. Furthermore, using a novel, visually realistic robotic system to create a mismatch between signal and relative competitive ability, we show that eye colour is used to honestly signal aggressive motivation. Specifically, robotic 'cheats' (that is, smaller, less-competitive robotic fish that display aggressive eye colouration when defending a food patch) attracted greater food competition from larger real fish. Our study suggests that eye colour may be an under-appreciated aspect of signalling in animals, shows the utility of our biomimetic robotic system for investigating animal behaviour, and provides experimental evidence that socially mediated costs towards low-quality individuals may maintain the honesty of dynamic colour signals.

Do detour tasks provide accurate assays of inhibitory control?

Transparent Cylinder and Barrier tasks are used to purportedly assess inhibitory control in a variety of animals. However, we suspect that performances on these detour tasks are influenced by non-cognitive traits, which may result in inaccurate assays of inhibitory control. We therefore reared pheasants under standardized conditions and presented each bird with two sets of similar tasks commonly used to measure inhibitory control. We recorded the number of times subjects incorrectly attempted to access a reward through transparent barriers, and their latencies to solve each task. Such measures are commonly used to infer the differential expression of inhibitory control. We found little evidence that their performances were consistent across the two different Putative Inhibitory Control Tasks (PICTs). Improvements in performance across trials showed that pheasants learned the affordances of each specific task. Critically, prior experience of transparent tasks, either Barrier or Cylinder, also improved subsequent inhibitory control performance on a novel task, suggesting that they also learned the general properties of transparent obstacles. Individual measures of persistence, assayed in a third task, were positively related to their frequency of incorrect attempts to solve the transparent inhibitory control tasks. Neophobia, Sex and Body Condition had no influence on individual performance. Contrary to previous studies of primates, pheasants with poor performance on PICTs had a wider dietary breadth assayed using a free-choice task. Our results demonstrate that in systems or taxa where prior experience and differences in development cannot be accounted for, individual differences in performance on commonly used detour-dependent PICTS may reveal more about an individual's prior experience of transparent objects, or their motivation to acquire food, than providing a reliable measure of their inhibitory control.

A novel continuous inhibitory-control task: variation in individual performance by young pheasants (Phasianus colchicus).

Inhibitory control enables subjects to quickly react to unexpectedly changing external demands. We assessed the ability of young (8 weeks old) pheasants Phasianus colchicus to exert inhibitory control in a novel response-inhibition task that required subjects to adjust their movement in space in pursuit of a reward across changing target locations. The difference in latencies between trials in which the target location did and did not change, the distance travelled towards the initially indicated location after a change occurred, and the change-signal reaction time provided a consistent measure that could be indicative of a pheasant's inhibitory control. Between individuals, there was a great variability in these measures; these differences were not correlated with motivation either to access the reward or participate in the test. However, individuals that were slower to reach rewards in trials when the target did not change exhibited evidence of stronger inhibitory control, as did males and small individuals. This novel test paradigm offers a potential assay of inhibitory control that utilises a natural feature of an animal's behavioural repertoire, likely common to a wide range of species, specifically their ability to rapidly alter their trajectory when reward locations switch.

Differences in social preference between the sexes during ontogeny drive segregation in a precocial species.

ABSTRACT: Hypotheses for why animals sexually segregate typically rely on adult traits, such as differences in sexual roles causing differential habitat preferences, or size dimorphism inducing differences in diet or behaviour. However, segregation can occur in juveniles before such roles or size dimorphism is well established. In young humans, leading hypotheses suggest that (1) sexes differ in their activity and the synchronisation of behaviour causes segregation and (2) sexes separate in order to learn and maximise future reproductive roles. We reared pheasants, Phasianus colchicus, from hatching in the absence of adults in a controlled environment. Females aggregated with their own sex from hatching, whereas males initially exhibited random association, but segregation became pronounced with age. The increase in segregation corresponded to an increase in sexual size dimorphism. By standardising habitat availability and diet and by removing predation risk, we could disregard the Predation Risk and the Forage Selection Hypotheses operating at this age. Activity budgets did not differ between the sexes, providing no support for the Behavioural Synchrony or the Activity Budget Hypotheses. Both sexes preferentially approached groups of unfamiliar, same-sex birds in binary choice tests, providing support for the Social Preference Hypothesis. Females may segregate to avoid male aggression. Sexual segregation may become established early in development, especially in precocial species, such as pheasants. A clear understanding of ontogenetic factors is essential to further our understanding of adult assortment patterns. Assortment by sex may not be inherent, but rather emerge as a consequence of social interactions early in life. SIGNIFICANCE STATEMENT: Hypotheses pertaining to the force driving sexual segregation typically rely on adult traits, such as size dimorphism or differences in sexual roles. However, in some species, animals segregate as juveniles, so that most hypotheses previously invoked to explain sexual segregation in adults are irrelevant. We reared pheasants, Phasianus colchicus, from hatching and monitored multiple aspects of the chicks' life history in an effort to determine what causes sexual segregation. Females aggregate with their own sex from hatching, whereas males initially have a more random association, but segregation becomes pronounced as both sexes got older, coinciding with greater sexual dimorphism. We controlled for influences of predation risk and dietary/habitat choice and found that activity budgets did not differ between the sexes. Instead, we found that both sexes preferred their own sex when presented with a binary choice, providing evidence that social preference could drive sexual segregation in pheasants.