Variation in response to environmental cues when foraging

Animals often respond differently to the same environmental cues. Where behavioural responses differ consistently between individuals over time or contexts, this is “personality”. In wild animals, personality is linked to variation in fitness and survival. Predictions on the behavioural mechanisms underlying this variation come from captive studies, on the often untested assumption that captive behaviour reveals how animals would behave in the wild. In chapter 2, using blue tits (Cyanistes caeruleus) I tested first whether behaviour in captivity predicted foraging behaviour in the wild. I measured the personality traits neophobia (latency to feed in novel scenarios) and exploratory tendency, first by relatively standard captive protocols and second, using an electronic monitoring system at feeding stations, by novel wild methods. As predicted, analogous traits correlated across contexts. Moreover, neophobia and exploratory tendency were uncorrelated within individuals in both contexts, in contrast to many other species. In captive studies, personality types also respond differently to changing environmental cues, or “environmental sensitivity”: neophobic and non-exploratory types adjust behaviour whilst neophilic and exploratory types maintain foraging routines. In chapter 3, I tested this second captive prediction in the wild, defining environmental sensitivity in the wild by changes in feeder use with varying air temperature or food supply. Neophobic and, contrary to expectation, exploratory blue tits were most environmentally sensitive. By contrast, neophilic and nonexploratory birds visited feeders at a fixed level independent of temperature and continued to visit feeders for a prolonged period even after they were emptied. Age and body size also influenced environmental sensitivity, suggesting learning and dominance interactions modify the expression of personality in the wild. From potential behavioural costs, in chapter 4 I turned to the physiological costs of personality. Variation in metabolic rate and stress metabolism may be proximate mechanisms for personality. Whilst these physiological traits are linked to oxidative stress directly, with pro-oxidants that damage body tissue a by-product of metabolism, few studies link personality to oxidative stress. I found that oxidative profile (pro-oxidants, antioxidants, oxidative stress and oxidative damage) and hence physiological costs differed notonly within traits but also related differently to neophobia and object exploration in captive-bred greenfinches (Carduelis chloris). Finally, variation in response to environmental cues may reflect differences in learning between individuals, as perhaps illustrated by age differences in environmental sensitivity (Chapter 3). In chapters 5 and 6, I investigated whether learning that a feeding site is temporally stable could cause changes in response to food appearance (“local cues”) when foraging. I predicted that birds would re-find food by spatial rather than local cues in these scenarios, as appearance can change hence local cues become unreliable over time. In chapter 5, I carried out an associative learning test to test this prediction in captive-bred greenfinches. Within a simple foraging scenario, the prediction was upheld: greenfinches favoured local cues in situations where the temporal stability of food was unknown, but switched to spatial cues when temporal stability was learnt through repeated encounters. In chapter 6 though, four of five wild bird species foraging at temporally stable bird feeders continued to respond to local cues, selecting feeders on the basis of colour. Most species were biased toward red feeders, and also responded to social cues when finding feeders: foraging strategies better suited to finding ephemeral food than re-finding temporally stable feeding sites. I suggest that wild birds use information on temporal stability from the broader environment (i.e. natural ephemeral food beyond temporally stable artificial feeders). This illustrates how animals may not necessarily forage in the wild as we would expect within specific contexts. Throughout this thesis therefore, my findings illustrate the importance of testing predictions generated from captive behaviour in the wild. Moreover, identifying variation in both the foraging strategies and physiological costs to individual variation in behaviour, this thesis provides new insight into the adaptive significance of animal personality

Stress exposure in early post-natal life reduces telomere length: an experimental demonstration in a long-lived seabird

Exposure to stressors early in life is associated with faster ageing and reduced longevity. One important mechanism that could underlie these late life effects is increased telomere loss. Telomere length in early post-natal life is an important predictor of subsequent lifespan, but the factors underpinning its variability are poorly understood. Recent human studies have linked stress exposure to increased telomere loss. These studies have of necessity been non-experimental and are consequently subjected to several confounding factors; also, being based on leucocyte populations, where cell composition is variable and some telomere restoration can occur, the extent to which these effects extend beyond the immune system has been questioned. In this study, we experimentally manipulated stress exposure early in post-natal life in nestling European shags (Phalacrocorax aristotelis) in the wild and examined the effect on telomere length in erythrocytes. Our results show that greater stress exposure during early post-natal life increases telomere loss at this life-history stage, and that such an effect is not confined to immune cells. The delayed effects of increased telomere attrition in early life could therefore give rise to a ‘time bomb’ that reduces longevity in the absence of any obvious phenotypic consequences early in life

Do glucocorticoids predict fitness? Linking environmental conditions, corticosterone and reproductive success in the blue tit, Cyanistes caeruleus

Glucocorticoids, including corticosterone (CORT), have been suggested to provide a physiological link between ecological conditions and fitness. Specifically, CORT, which is elevated in response to harsh conditions, is predicted to be correlated with reduced fitness. Yet, empirical studies show that CORT can be non-significantly, positively and negatively linked with fitness. Divergent environmental conditions between years or study systems may influence whether CORT is linked to fitness. To test this, we monitored free-living blue tits ( Cyanistes caeruleus ) during breeding over 3 years. We quantified foraging conditions during brood rearing, and examined whether they were correlated with parental baseline CORT and reproductive success. We then tested whether CORT predicted fitness. Elevated parental CORT was associated with lower temperatures, greater rainfall and lower territory-scale oak density. Whereas asynchrony with the caterpillar food peak was correlated with reduced nestling mass and fledging success, but not parental CORT. Only low temperatures were associated with both reduced nestling mass and elevated parental CORT. Despite this, parents with elevated CORT had lighter offspring in all years. Contrarily, in 2009 parental CORT was positively correlated with the number fledged. The absence of a direct link between the foraging conditions that reduce nestling quality and elevate parental CORT suggests that parental CORT may provide a holistic measure of conditions where parents are working harder to meet the demands of developing young. As the positive correlation between parental CORT and fledging success differed between years, this suggests that contrasting conditions between years can influence correlations between parental CORT and fitness. Ultimately, as CORT concentrations are intrinsically variable and linked to the prevalent conditions, studies that incorporate environmental harshness will improve our understanding of evolutionary endocrinology. </jats:p

Skin temperature reveals the intensity of acute stress

Acute stress triggers peripheral vasoconstriction, causing a rapid, short-term drop in skin temperature in homeotherms. We tested, for the first time, whether this response has the potential to quantify stress, by exhibiting proportionality with stressor intensity. We used established behavioural and hormonal markers: activity level and corticosterone level, to validate a mild and more severe form of an acute restraint stressor in hens (Gallus gallus domesticus). We then used infrared thermography (IRT) to non-invasively collect continuous temperature measurements following exposure to these two intensities of acute handling stress. In the comb and wattle, two skin regions with a known thermoregulatory role, stressor intensity predicted the extent of initial skin cooling, and also the occurrence of a more delayed skin warming, providing two opportunities to quantify stress. With the present, cost-effective availability of IRT technology, this non-invasive and continuous method of stress assessment in unrestrained animals has the potential to become common practice in pure and applied research

Eye region surface temperature reflects both energy reserves and circulating glucocorticoids in a wild bird

Body temperature of endotherms shows substantial within- and between-individual variation, but the sources of this variation are not fully understood in wild animals. Variation in body temperature can indicate how individuals cope with their environment via metabolic or stress-induced effects, both of which may relate to depletion of energy reserves. Body condition can reflect heat production through changes to metabolic rate made to protect energy reserves. Additionally, changes in metabolic processes may be mediated by stress-related glucocorticoid secretion, which is associated with altered blood-flow patterns that affect regional body temperatures. Accordingly, both body condition and glucocorticoid secretion should relate to body temperature. We used thermal imaging, a novel non-invasive method of temperature measurement, to investigate relationships between body condition, glucocorticoid secretion and body surface temperature in wild blue tits (Cyanistes caeruleus). Individuals with lower body condition had lower eye-region surface temperature in both non-breeding and breeding seasons. Eye-region surface temperature was also negatively correlated with baseline circulating glucocorticoid levels in non-breeding birds. Our results demonstrate that body surface temperature can integrate multiple aspects of physiological state. Consequently, remotely-measured body surface temperature could be used to assess such aspects of physiological state non-invasively in free-living animals at multiple life history stages

Dietary antioxidants in life-history trade-offs: differential effects of a-tocopherol supplementation on blue tit Cyanistes caeruleus mothers and offspring during reproduction

α-Tocopherol is assumed to be the most biologically active dietary antioxidant in vivo, but despite its potential importance little is known about its impacts on wild birds. Reproduction is presumed to be costly for parents through several routes, including increased oxidative stress, particularly for bird species producing large clutches. If dietary antioxidants can ameliorate oxidative stress associated with reproduction, mothers supplemented with dietary antioxidants are predicted to be in improved condition and/or invest more resources in reproduction than controls. We provided adult blue tit pairs with an α-tocopherol-enriched or control food supplement during nest building and egg laying, then cross-fostered half broods between treatment groups to test the theory that α-tocopherol-supplemented mothers would invest more in self-maintenance or reproduction than controls. We found that α-tocopherol supplementation had no effect on the maternal condition or reproductive investment. However, effects on nestlings were evident: nestlings from α-tocopherol-supplemented mothers were smaller at hatching. There was no effect on chick fledging mass, fledging success or lipid peroxidation, but the catch-up growth exhibited by chicks from α-tocopherol-supplemented parents may be considered costly. Thus, our results do not provide evidence for a benefit of maternal α-tocopherol supplementation at a biologically relevant dose on either themselves or their offspring. We discuss our findings in terms of ongoing research on the multifaceted roles that dietary ‘antioxidants’ can have in vivo, and the issues of disentangling their impacts on physiology and behaviour in the wild

Parental age influences offspring telomere loss

1. The age of the parents at the time of offspring production can influence offspring longevity, but the underlying mechanisms remain poorly understood. The effect of parental age on offspring telomere dynamics (length and loss rate) is one mechanism that could be important in this context. 2. Parental age might influence the telomere length that offspring inherit or age-related differences in the quality of parental care could influence the rate of offspring telomere loss. However, these routes have generally not been disentangled. 3. Here, we investigated whether parental age was related to offspring telomere dynamics using parents ranging in age from 2 to 22 years old in a free-living population of a long-lived seabird, the European shag (Phalacrocorax aristotelis). By measuring the telomere length of offspring at hatching and towards the end of the post-natal growth period, we could assess whether any potential parental age effect was confined to the post-natal rearing period. 4. There was no effect of maternal or paternal age on the initial telomere length of their chicks. However, chicks produced by older mothers and fathers experienced significantly greater telomere loss during the post-natal nestling growth period. We had relatively few nests in which the ages of both parents were known, and individuals in this population mate assortatively with respect to age. Thus, we could not conclusively determine whether the parental age effect was due to maternal age, paternal age, or both; however, it appears that the effect is stronger in mothers. 5. These results demonstrate that in this species, there was no evidence that parental age was related to offspring hatching telomere length. However, telomere loss during nestling growth was reduced in the offspring of older parents. This could be due to an age-related deterioration in the quality of the environment that parents provide, or because parents that invest less in offspring rearing live to an older age

Individual variation in corticosterone and personality traits in the blue tit Cyanistes caeruleus

Source: Variation in personality traits is predicted to reflect physiology, but the extent to which variations in stress hormones derive from differences in personality and/or state-dependent factors remains unclear. To investigate this, wild blue tits (Cyanistes caeruleus) were briefly brought into captivity and scored for personality and corticosterone (Cort) concentrations. More active females had lower baseline Cort than less active individuals. Exploratory tendency and neophobia did not co-vary with baseline Cort. Stress-induced Cort concentrations were correlated negatively with exploratory tendency and haematocrit, but positively with mass gain in captivity. Therefore, baseline and stress-induced Cort concentrations in wintering blue tits were associated with state-dependent variables, sex, age and personality traits. Key to interpreting the physiology of personality traits seems to be their interactions with other traits that mediate ability to utilise resources, and thus influence an individual’s perception of its current and future energy balance

Data from: Individual variation in the oxidative costs of personality traits

1.‘Personality traits’ are behavioural differences between individuals that are stable within individuals. Different combinations of personality traits can correlate with fitness variation but the mechanisms remain unclear. There is the suggestion that personality reflects variation in physiology. For example, ‘fast’ (bold, active, fast exploring) individuals are predicted to maintain a higher metabolic rate than ‘slow’ animals. A raised metabolic rate can result in a proliferation of reactive oxygen species (ROS) which, if unchecked, cause oxidative stress. Thus, the ‘extended pace of life theory’ predicts that ‘fast’ individuals will pay higher oxidative costs than ‘slow’ ones. Alternatively, stress hormones, which are often relatively high in ‘slow’ individuals, can also cause proliferation of ROS and subsequent oxidative damage. Here, we assessed co-variation between personality and oxidative profile in wild blue tits. 2.The personality traits neophobia (latency to approach food near novel objects), activity level in a novel environment and exploratory tendency (controlling for differences in activity) assayed in captivity were repeatable within individuals but were uncorrelated with each other. Reactive oxygen metabolites (ROMs an index of pro-oxidant status) and OXY (antioxidant capacity) were also uncorrelated with each other and did not vary with age or sex. Blood sampling birds within three minutes of capture from their familiar cage versus after 15 minutes of exposure to a standardised stressor did not affect ROMs or OXY. 3.Wintering blue tits that were both highly neophobic and exploratory had low OXY defences and individuals that showed low neophobia and low exploration had high OXY defences. Variation in ROMs was not explained by any personality trait. High exploratory tendency also correlated with a reduction in body condition in captivity, but body condition did not predict ROMs or OXY. Activity level in the exploration trial did not vary with oxidative profile or change in body condition. 4.Personality types differed in antioxidant defences, and it was the combination of an individual's personality traits that proved important. ROS production and antioxidant defences will vary due to many processes e.g. resource allocation, not just metabolic rate and stress responsiveness. Consequently, the costs of personality traits and thus the predictions regarding fitness are complex. This article is protected by copyright. All rights reserved