Multiple behavioural, morphological and cognitive developmental changes arise from a single alteration to early life spatial environment, resulting in fitness consequences for released pheasants

This is the final version of the article. Available from the Royal Society via the DOI in this record.Subtle variations in early rearing environment influence morphological, cognitive and behavioural processes that together impact on adult fitness. We manipulated habitat complexity experienced by young pheasants (Phasianus colchicus) in their first seven weeks, adding a third accessible dimension by placing elevated perches in their rearing pens mimicking natural variation in habitat complexity. This simple manipulation provoked an interrelated suite of morphological, cognitive and behavioural changes, culminating in decreased wild mortality of birds from complex habitats compared with controls. Three mechanisms contribute to this: Pheasants reared with perches had a morphology which could enable them to fly to the higher branches and cope with prolonged roosting. They had a higher propensity to roost off the ground at night in the wild. More generally, these birds had more accurate spatial memory. Consequently, birds were at a reduced risk of terrestrial predation. The fitness consequences of variation in early rearing on behavioural development are rarely studied in the wild but we show that this is necessary because the effects can be broad ranging and not simple, depending on a complex interplay of behavioural, cognitive and morphological elements, even when effects that the treatments provoke are relatively short term and plastic.M.A.W. was jointly funded by the University of Exeter and the Game and Wildlife Conservation Trust. J.R.M. was funded by an ERC Consolidator Award (616474)

Why do many pheasants released in the UK die, and how can we best reduce their natural mortality?

This is the final version of the article. Available from Springer Verlag via the DOI in this record.Around 60% of pheasants released for shooting in the UK, an estimated 21 million birds, do not end up at their intended fate: being shot. This constitutes wastage, raising economic, environmental and ethical questions. We review what is known of the fates of released pheasants and consider why they do not directly contribute to the numbers harvested. We focus on four main explanations: predation, disease, starvation and dispersal, and highlight other important causes of mortality. For each explanation, we attempt to attribute levels of loss and identify timings or conditions when such losses may be heaviest. We review factors that exacerbate losses and methods available to mitigate them. Opportunities for amelioration may arise at all stages of the rearing and release of pheasants and involve changes to the conditions under which eggs are produced, the way young pheasants are reared or the management of the environment into which they are released. We found few studies investigating impacts of post-release management techniques on pheasant survival outside of the breeding season within a UK context. We found that a number of less commonly deployed practices focusing on early-life, pre-release management may improve survival. Given the scale of pheasant releasing in the UK, even improvements in survival of 1% would mean that ~ 350,000 fewer birds die of natural causes. Complementing current post-release management with proven novel pre-release management interventions could reduce the number of pheasants required for release, whilst maintaining current shooting levels. Lowering release numbers would lower financial costs, benefit the environment and reduce some ethical concerns over the release and shooting of reared pheasants

Group social rank is associated with performance on a spatial learning task (article)

This is the final published version. Available from the Royal Society via the DOI in this record.The dataset associated with this article is located in ORE at: http://hdl.handle.net/10871/30840Dominant individuals differ from subordinates in their performances on cognitive tasks across a suite of taxa. Previous studies often only consider dyadic relationships, rather than the more ecologically relevant social hierarchies or networks, hence failing to account for how dyadic relationships may be adjusted within larger social groups. We used a novel statistical method: randomized Elo-ratings, to infer the social hierarchy of 18 male pheasants, Phasianus colchicus, while in a captive, mixed-sex group with a linear hierarchy. We assayed individual learning performance of these males on a binary spatial discrimination task to investigate whether inter-individual variation in performance is associated with group social rank. Task performance improved with increasing trial number and was positively related to social rank, with higher ranking males showing greater levels of success. Motivation to participate in the task was not related to social rank or task performance, thus indicating that these rank-related differences are not a consequence of differences in motivation to complete the task. Our results provide important information about how variation in cognitive performance relates to an individual's social rank within a group. Whether the social environment causes differences in learning performance or instead, inherent differences in learning ability predetermine rank remains to be tested.ERC Consolidator Award (616474) to J.R.M

Individuals in larger groups are more successful on spatial discrimination tasks

This is the final version of the article. Available from the publisher via the DOI in this record.To understand how natural selection may act on cognitive processes, it is necessary to reliably determine interindividual variation in cognitive abilities. However, an individual's performance in a cognitive test may be influenced by the social environment. The social environment explains variation between species in cognitive performances, with species that live in larger groups purportedly demonstrating more advanced cognitive abilities. It also explains variation in cognitive performances within species, with larger groups more likely to solve novel problems than smaller groups. Surprisingly, an effect of group size on individual variation in cognitive performance has rarely been investigated and much of our knowledge stems from impaired performance of individuals reared in isolation. Using a within-subjects design we assayed individual learning performance of adult female pheasants, Phasianus colchicus, while housed in groups of three and five. Individuals experienced the group sizes in a different order, but were presented with two spatial discrimination tasks, each with a distinct cue set, in a fixed order. We found that across both tasks individuals housed in the large groups had higher levels of success than individuals housed in the small groups. Individuals had higher levels of success on their second than their first task, irrespective of group size. We suggest that the expression of individual learning performance is responsive to the current social environment but the mechanisms underpinning this relationship require further investigation. Our study demonstrates that it is important to account for an individual's social environment when attempting to characterize cognitive capacities. It also demonstrates the flexibility of an individual's cognitive performance depending on the social context.The work was funded by an ERC Consolidator Award to J.R.M (616474)

Size dimorphism and sexual segregation in pheasants: tests of three competing hypotheses (article)

This is the final version. Available from PeerJ via the DOI in this record.The dataset associated with this article is in ORE at: https://doi.org/10.24378/exe.683Fine scale sexual segregation outside of the mating season is common in sexually dimorphic and polygamous species, particularly in ungulates. A number of hypotheses predict sexual segregation but these are often contradictory with no agreement as to a common cause, perhaps because they are species specific. We explicitly tested three of these hypotheses which are commonly linked by a dependence on sexual dimorphism for animals which exhibit fine-scale sexual segregation; the Predation Risk Hypothesis, the Forage Selection Hypothesis, and the Activity Budget Hypothesis, in a single system the pheasant, Phasianus colchicus; a large, sedentary bird that is predominantly terrestrial and therefore analogous to ungulates rather than many avian species which sexually segregate. Over four years we reared 2,400 individually tagged pheasants from one day old and after a period of 8–10 weeks we released them into the wild. We then followed the birds for 7 months, during the period that they sexually segregate, determined their fate and collected behavioural and morphological measures pertinent to the hypotheses. Pheasants are sexually dimorphic during the entire period that they sexually segregate in the wild; males are larger than females in both body size and gut measurements. However, this did not influence predation risk and predation rates (as predicted by the Predation Risk Hypothesis), diet choice (as predicted by the Forage Selection Hypothesis), or the amount of time spent foraging, resting or walking (as predicted by the Activity Budget Hypothesis). We conclude that adult sexual size dimorphism is not responsible for sexual segregation in the pheasant in the wild. Instead, we consider that segregation may be mediated by other, perhaps social, factors. We highlight the importance of studies on a wide range of taxa to help further the knowledge of sexual segregation.The work was jointly funded by the University of Exeter, the Game and Wildlife Conservation Trust and an ERC Consolidator Award (616474) awarded to Joah R. Madden

The relationship between social rank and spatial learning in pheasants, Phasianus colchicus: Cause or consequence? (article)

This is the final version. Available from PeerJ via the DOI in this record.The dataset associated with this article is in ORE: https://doi.org/10.24378/exe.143Individual differences in performances on cognitive tasks have been found to differ according to social rank across multiple species. However, it is not clear whether an individual's cognitive performance is flexible and the result of their current social rank, modulated by social interactions (social state dependent hypothesis), or if it is determined prior to the formation of the social hierarchy and indeed influences an individual's rank (prior attributes hypothesis). We separated these two hypotheses by measuring learning performance of male pheasants, Phasianus colchicus, on a spatial discrimination task as chicks and again as adults. We inferred adult male social rank from observing agonistic interactions while housed in captive multi-male multi-female groups. Learning performance of adult males was assayed after social rank had been standardised; by housing single males with two or four females. We predicted that if cognitive abilities determine social rank formation we would observe: consistency between chick and adult performances on the cognitive task and chick performance would predict adult social rank. We found that learning performances were consistent from chicks to adults for task accuracy, but not for speed of learning and chick learning performances were not related to adult social rank. Therefore, we could not support the prior attributes hypothesis of cognitive abilities aiding social rank formation. Instead, we found that individual differences in learning performances of adults were predicted by the number of females a male was housed with; males housed with four females had higher levels of learning performance than males housed with two females; and their most recent recording of captive social rank, even though learning performance was assayed while males were in a standardized, non-competitive environment. This does not support the hypothesis that direct social pressures are causing the inter-individual variation in learning performances that we observe. Instead, our results suggest that there may be carry-over effects of aggressive social interactions on learning performance. Consequently, whether early life spatial learning performances influence social rank is unclear but these performances are modulated by the current social environment and a male's most recent social rank.European Research Counci

Differences in social preference between the sexes during ontogeny drive segregation in a precocial species (article)

This is the final version of the article. Available from the publisher via the DOI in this record.The datasets analysed during the current study are available at the Open Research Exeter repository. http://hdl.handle.net/ 10871/27114.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.The work was jointly funded by the University of Exeter, the Game and Wildlife Conservation Trust, a Royal Society Small Project Grant awarded to JRM and an ERC Consolidator Grant (616474) awarded to JRM

The welfare of game birds destined for release into the wild: A balance between early life care and preparation for future natural hazards

This is the author accepted manuscript. The final version is available from the Universities Federation for Animal Welfare (UFAW) via the DOI in this recordGlobally, over 110 million game birds are reared annually and released for recreational hunting. Game birds differ from other reared livestock because they experience two very distinct environments during their lives. Chicks are first reared in captivity for 6-12 weeks under managed, stable conditions and then released into the wild. A limited set of 13 studies have explored how the rearing conditions experienced by chicks influences their pre-release welfare, typically in terms of physical injury (feather-pecking) or behavioural assays of stress responses. However, no studies have considered the specific indicators of welfare of game birds after release. We therefore need to draw from studies that do not specifically investigate welfare but instead ones that examine how rearing environments influence post-release morphology, behaviour and survival. Consequently, we reviewed how reared and wild-born game birds differ and suggest methods by which more naturalistic rearing conditions may be achieved. We noted five areas where artificial rearing deviates substantially from natural conditions: absence of adults; unnatural chick densities; unnatural diet; unnatural physical environment; and exclusion of predation risk. Mimicking or introducing some of these elements in game bird rearing practice could bring two benefits: i) facilitating more natural behaviour by the chicks during rearing; and ii) ensuring that birds after release are better able to cope with natural hazards. Together, these could result in an improved overall welfare for game birds. For example, enrichment of the spatial environment may serve to both improve welfare pre-release and after release into the wild. However, some adaptations may induce poor welfare for a short period in the young birds. For example, exposure to predators may be temporarily stressful, but ultimately such experiences in early life may permit them to better cope with such threats when released into the wild. Therefore, to achieve an optimal welfare for the entirety of a game bird's life, a careful balance between the conditions experienced in early life and adequate preparation for later life in the wild is required.European Research Council (ERC

Low survival of strongly footed pheasants may explain constraints on lateralization

This is the final version. Available from Springer Nature via the DOI in this record.Brain lateralization is considered adaptive because it leads to behavioral biases and specializations that bring fitness benefits. Across species, strongly lateralized individuals perform better in specific behaviors likely to improve survival. What constrains continued exaggerated lateralization? We measured survival of pheasants, finding that individuals with stronger bias in their footedness had shorter life expectancies compared to individuals with weak biases. Consequently, weak, or no footedness provided the highest fitness benefits. If, as suggested, footedness is indicative of more general brain lateralization, this could explain why continued brain lateralization is constrained even though it may improve performance in specific behaviors.This work was supported by a European Research Council Consolidator Award (616474) awarded to JRM

Cytokine mRNA profiles in Epstein-Barr virus-associated post-transplant lymphoproliferative disorders.

Cytokine mRNA patterns were analyzed in 11 post-transplant lymphoproliferative disorder (PTLD) specimens using qualitative reverse-transcriptase polymerase chain reaction (RT-PCR). In each case, a pattern of IL2-, IFN gamma-, IL4+, IL10+ was seen. A similar pattern was observed in a spleen sample from 1 patient with contemporaneous PTLD elsewhere. Semiquantitative RT-PCR for cytokine message was performed using RNA from bronchoalveolar lavage (BAL) specimens obtained from 2 patients with pulmonary PTLD. In both cases, IL4 message predominated. Reduction of message coincided with resolution of the tumors. The pattern differed from that seen in 1 patient with acute pulmonary rejection, in which RT-PCR of BAL cells showed predominance of IL6 and IFN gamma. We conclude that at least some PTLDs exist within a T-helper cell type 2 (Th2)-like cytokine microenvironment. The presence of a similar mRNA pattern in an extratumoral specimen at the time of PTLD suggests that it may reflect a systemic phenomenon. Disappearance of this pattern following PTLD resolution indicates its dynamic nature and is consistent with the hypothesis that specific cytokines contribute to the development of PTLDs