Exposure to food insecurity increases energy storage and reduces somatic maintenance in European starlings (Sturnus vulgaris).

Birds exposed to food insecurity-defined as temporally variable access to food-respond adaptively by storing more energy. To do this, they may reduce energy allocation to other functions such as somatic maintenance and repair. To investigate this trade-off, we exposed juvenile European starlings (Sturnus vulgaris, n = 69) to 19 weeks of either uninterrupted food availability or a regime where food was unpredictably unavailable for a 5-h period on 5 days each week. Our measures of energy storage were mass and fat scores. Our measures of somatic maintenance were the growth rate of a plucked feather, and erythrocyte telomere length (TL), measured by analysis of the terminal restriction fragment. The insecure birds were heavier than the controls, by an amount that varied over time. They also had higher fat scores. We found no evidence that they consumed more food overall, though our food consumption data were incomplete. Plucked feathers regrew more slowly in the insecure birds. TL was reduced in the insecure birds, specifically, in the longer percentiles of the within-individual TL distribution. We conclude that increased energy storage in response to food insecurity is achieved at the expense of investment in somatic maintenance and repair.

Food insecurity increases energetic efficiency, not food consumption: an exploratory study in European starlings.

Food insecurity-defined as limited or unpredictable access to nutritionally adequate food-is associated with higher body mass in humans and birds. It is widely assumed that food insecurity-induced fattening is caused by increased food consumption, but there is little evidence supporting this in any species. We developed a novel technology for measuring foraging, food intake and body mass in small groups of aviary-housed European starlings (Sturnus vulgaris). Across four exploratory experiments, we demonstrate that birds responded to 1-2 weeks of food insecurity by increasing their body mass despite eating less. Food-insecure birds therefore increased their energetic efficiency, calculated as the body mass maintained per unit of food consumed. Mass gain was greater in birds that were lighter at baseline and in birds that faced greater competition for access to food. Whilst there was variation between experiments in mass gain and food consumption under food insecurity, energetic efficiency always increased. Bomb calorimetry of guano showed reduced energy density under food insecurity, suggesting that the energy assimilated from food increased. Behavioural observations of roosting showed inconsistent evidence for reduced physical activity under food insecurity. Increased energetic efficiency continued for 1-2 weeks after food security was reinstated, indicating an asymmetry in the speed of the response to food insecurity and the recovery from it. Future work to understand the mechanisms underlying food insecurity-induced mass gain should focus on the biological changes mediating increased energetic efficiency rather than increased energy consumption.

Time perception and patience: individual differences in interval timing precision predict choice impulsivity in European starlings, Sturnus vulgaris.

Impulsivity, in the sense of the extent rewards are devalued as the time until their realization increases, is linked to various negative outcomes in humans, yet understanding of the cognitive mechanisms underlying it is limited. Variation in the imprecision of interval timing is a possible contributor to variation in impulsivity. We use a numerical model to generate predictions concerning the effect of timing imprecision on impulsivity. We distinguish between fixed imprecision (the imprecision that applies even when timing the very shortest time intervals) and proportional imprecision (the rate at which imprecision increases as the interval becomes longer). The model predicts that impulsivity should increase with increasing fixed imprecision, but decrease with increasing proportional imprecision. We present data from a cohort of European starlings (Sturnus vulgaris, n = 28) in which impulsivity had previously been measured through an intertemporal choice paradigm. We tested interval timing imprecision in the same individuals using a tri-peak temporal reproduction procedure. We found repeatable individual differences in both fixed and proportional imprecision. As predicted, birds with greater proportional imprecision in interval timing made fewer impulsive choices, whilst those with greater fixed imprecision tended to make more. Contradictory observations in the literature regarding the direction of association between timing imprecision and impulsivity might be clarified by distinguishing between fixed and proportional components of imprecision.

The experiences of migrants to Australia who stutter.

PURPOSE: Migration is a contemporary, global matter. With the number of international migrants doubling over the past four decades, speech-language pathologists will likely work with migrants who have childhood-onset stuttering. However, combined migration and stuttering experiences have never been investigated specifically. This study is the first to investigate the experiences of migrants to Australia who stutter. METHODS: Three women and six men, aged 23 to 66 years old, participated. Data from individual interviews were analysed using Interpretative Phenomenological Analysis to examine the 'lived experience' of participants, as well as with NVivo 12 software for the management of coding. Participants also completed The Overall Assessment of the Speaker's Experience of Stuttering (OASES™). RESULTS: The stress experienced from migration interacted and compounded the existing stress of stuttering. Central themes emerged pertaining to the impact of increased stress on self-identity, the interactions of the stresses, as well as the coping strategies/facilitators. Stuttering and other personal factors, such as language(s) spoken and accent, had a negative impact on communication skills. CONCLUSION: Migration cannot be experienced independently of a stutter, as both are intrinsically linked to self-identity. The combined stress of migration with stuttering amplified the perception of feeling abnormal and resulted in difficulties with establishing a stable self-identity and a sense of belonging in the new context. Participants found strength in the company of others and considered Australia to be accepting of stuttering.

Developmental history, energetic state and choice impulsivity in European starlings, Sturnus vulgaris.

Impulsivity-the extent to which a reward is devalued by the amount of time until it is realized-can be affected by an individual's current energetic state and long-term developmental history. In European starlings (Sturnus vulgaris), a previous study found that birds that were lighter for their skeletal size, and birds that had undergone greater shortening of erythrocyte telomeres over the course of development, were more impulsive as adults. Here, we studied the impulsivity of a separate cohort of 29 starlings hand-reared under different combinations of food amount and begging effort. The task involved repeated choice between a key yielding one pellet after 3 s and another key yielding two pellets after 8 s. Impulsivity was operationalised as the proportion of choices for the short-delay option. We found striking variation in impulsivity. We did not replicate the results of the previous study concerning developmental telomere attrition, though combining all the evidence to date in a meta-analysis did support that robustness of that association. We also found that early-life conditions and mass for skeletal size interacted in predicting impulsivity. Specifically, birds that had experienced the combination of high begging effort and low food amount were less impulsive than other groups, and the usual negative relationship between impulsivity and body mass was abolished in birds that had experienced high begging effort. We discuss methodological differences between our study and studies that measure impulsivity using an adjusting-delay procedure.

Developmental history and stress responsiveness are related to response inhibition, but not judgement bias, in a cohort of European starlings (Sturnus vulgaris).

Judgement bias tasks are designed to provide markers of affective states. A recent study of European starlings (Sturnus vulgaris) demonstrated modest familial effects on judgement bias performance, and found that adverse early experience and developmental telomere attrition (an integrative marker of biological age) both affected judgement bias. Other research has shown that corticosterone levels affect judgement bias. Here, we investigated judgement bias using a modified Go/No Go task in a new cohort of starlings (n = 31) hand-reared under different early-life conditions. We also measured baseline corticosterone and the corticosterone response to acute stress in the same individuals. We found evidence for familial effects on judgement bias, of a similar magnitude to the previous study. We found no evidence that developmental treatments or developmental telomere attrition were related to judgement bias per se. We did, however, find that birds that experienced the most benign developmental conditions, and birds with the greatest developmental telomere attrition, were significantly faster to probe the learned unrewarded stimulus. We also found that the birds whose corticosterone levels were faster to return towards baseline after an acute stressor were slower to probe the learned unrewarded stimulus. Our results illustrate the potential complexities of relationships between early-life experience, stress and affectively mediated decision making. For judgement bias tasks, they demonstrate the importance of clearly distinguishing factors that affect patterns of responding to the learned stimuli (i.e. response inhibition in the case of the Go/No Go design) from factors that influence judgements under ambiguity.

Chronological age, biological age, and individual variation in the stress response in the European starling: a follow-up study.

The strength of the avian stress response declines with age. A recently published study of European starlings (Sturnus vulgaris) found that a marker of biological age predicted the strength of the stress response even in individuals of the same chronological age. Specifically, birds that had experienced greater developmental telomere attrition (DTA) showed a lower peak corticosterone (CORT) response to an acute stressor, and more rapid recovery of CORT levels towards baseline. Here, we performed a follow-up study using the same capture-handling-restraint stressor in a separate cohort of starlings that had been subjected to a developmental manipulation of food availability and begging effort. We measured the CORT response at two different age points (4 and 18 months). Our data suggest a decline in the strength of the CORT response with chronological age: peak CORT was lower at the second age point, and there was relatively more reduction in CORT between 15 and 30 min. Individual consistency between the two age points was low, but there were modest familial effects on baseline and peak CORT. The manipulation of begging effort affected the stress response (specifically, the reduction in CORT between 15 and 30 min) in an age-dependent manner. However, we did not replicate the associations with DTA observed in the earlier study. We meta-analysed the data from the present and the earlier study combined, and found some support for the conclusions of the earlier paper.

Evaluating the cyclic ratio schedule as an assay of feeding behaviour in the European starling (Sturnus vulgaris).

The cyclic ratio (CR) schedule is a behavioural assay developed to study feeding in rats, in which the number of operant responses required to obtain food reward (the ratio requirement) increases and then decreases in a repeating cycle. In a recent study, we used the CR schedule with European starlings (Sturnus vulgaris) to investigate the effects of an early-life manipulation on adult feeding behaviour. As this was the first time the CR schedule had been used with any bird species, a more in-depth evaluation is warranted. Here, we performed a fuller CR experiment with the same birds as the prior study, a year later. First, we examine the individual consistency of feeding behaviour between experimental sessions and also between CR schedules comprising different ratio requirement progressions. We found that between-session consistency was poor to moderate, and that a geometric ratio progression provided greater between-session consistency than an arithmetic ratio progression. Second, we tried to replicate some of the canonical findings from rats working on CR schedules. In contrast to findings from rats, we found that defence of feeding rates did not increase when starlings were acutely food deprived. However, as in rats, we found that the post-reinforcement pause increased linearly with the upcoming ratio requirement, suggesting that starlings were able to learn the cyclic nature of the schedule. Third, we compared the results from the present study concerning the impacts of our early-life treatment with those from our earlier study. We found that the majority of our previous findings were replicated in the same individuals one year on, reinforcing our previous conclusion that the early-life manipulation had canalised our birds into two groups with different patterns of feeding rate defence.

Early-life begging effort reduces adult body mass but strengthens behavioural defence of the rate of energy intake in European starlings.

Animals require strategies for coping with periods when food is scarce. Such strategies include storing fat as a buffer, and defending the rate of energy intake by changing foraging behaviour when food becomes difficult to obtain. Storage and behavioural defence may constitute alternative strategies for solving the same problem. We would thus expect any developmental influences that limit fat storage in adulthood to also induce a compensatory alteration in adult foraging behaviour, specifically when food is hard to obtain. In a cohort of hand-reared European starlings, we found that higher manipulated early-life begging effort caused individuals to maintain consistently lower adult body mass over a period of two years. Using an operant foraging task in which we systematically varied the costs of obtaining food, we show that higher early-life begging effort also caused stronger behavioural defence of the rate of energy intake when food was more costly to obtain. Among individuals with the same developmental history, however, those individuals who defended their rate of energy intake most strongly were also the heaviest. Our results are relevant to understanding why there are marked differences in body weight and foraging behaviour even among individuals inhabiting the same environment.

A marker of biological ageing predicts adult risk preference in European starlings, Sturnus vulgaris.

Why are some individuals more prone to gamble than others? Animals often show preferences between 2 foraging options with the same mean reward but different degrees of variability in the reward, and such risk preferences vary between individuals. Previous attempts to explain variation in risk preference have focused on energy budgets, but with limited empirical support. Here, we consider whether biological ageing, which affects mortality and residual reproductive value, predicts risk preference. We studied a cohort of European starlings (Sturnus vulgaris) in which we had previously measured developmental erythrocyte telomere attrition, an established integrative biomarker of biological ageing. We measured the adult birds' preferences when choosing between a fixed amount of food and a variable amount with an equal mean. After controlling for change in body weight during the experiment (a proxy for energy budget), we found that birds that had undergone greater developmental telomere attrition were more risk averse as adults than were those whose telomeres had shortened less as nestlings. Developmental telomere attrition was a better predictor of adult risk preference than either juvenile telomere length or early-life food supply and begging effort. Our longitudinal study thus demonstrates that biological ageing, as measured via developmental telomere attrition, is an important source of lasting differences in adult risk preferences.

Dissociating the effects of alternative early-life feeding schedules on the development of adult depression-like phenotypes.

Early-life adversity is associated with increased vulnerability to depression in humans, and depression-like phenotypes in animals. However, different types of adverse experience may leave different signatures in adulthood. We experimentally manipulated the Amount of food delivered to European starling nestlings and the begging Effort required to obtain food during early development. Here, we report behavioural data in adulthood from a task that assessed sensitivity to shifts in reward magnitude characteristic of depression-like low mood. Birds that had experienced Hard Effort were more food motivated than birds that had experienced Easy Effort. Both Effort and Amount affected sensitivity to shifts in reward magnitude: Hard Effort birds showed an enhanced negative contrast effect following loss of reward ('disappointment'), and Lean Amount birds failed to show a normal positive contrast effect following gain in reward (a lack of 'elation'). Therefore, the feeding schedule experienced for just 10 days in early life caused enduring effects on feeding motivation and sensitivity to reward loss/gain consistent with human depression. Furthermore, the contrast effects were specific to different types of adversity. These results highlight the importance of early-life feeding schedules in the development of depression-like phenotypes.

A marker of biological age explains individual variation in the strength of the adult stress response.

The acute stress response functions to prioritize behavioural and physiological processes that maximize survival in the face of immediate threat. There is variation between individuals in the strength of the adult stress response that is of interest in both evolutionary biology and medicine. Age is an established source of this variation-stress responsiveness diminishes with increasing age in a range of species-but unexplained variation remains. Since individuals of the same chronological age may differ markedly in their pace of biological ageing, we asked whether biological age-measured here via erythrocyte telomere length-predicts variation in stress responsiveness in adult animals of the same chronological age. We studied two cohorts of European starlings in which we had previously manipulated the rate of biological ageing by experimentally altering the competition experienced by chicks in the fortnight following hatching. We predicted that individuals with greater developmental telomere attrition, and hence greater biological age, would show an attenuated corticosterone (CORT) response to an acute stressor when tested as adults. In both cohorts, we found that birds with greater developmental telomere attrition had lower peak CORT levels and a more negative change in CORT levels between 15 and 30 min following stress exposure. Our results, therefore, provide strong evidence that a measure of biological age explains individual variation in stress responsiveness: birds that were biologically older were less stress responsive. Our results provide a novel explanation for the phenomenon of developmental programming of the stress response: observed changes in stress physiology as a result of exposure to early-life adversity may reflect changes in ageing.

Effects of early life adversity and sex on dominance in European starlings.

Dominance in socially foraging animals may be related to sex and to variation in individual quality. Individual quality may in turn reflect conditions during early development. We studied dominance in a cohort of adult European starlings, Sturnus vulgaris, that had been subject to experimental manipulations of food supply and begging effort when they were nestlings. We measured dominance in two different contexts, contests over a food resource and relative position on a sloping perch, over the course of 3 weeks. Dominance in food contests was extremely stable over the 3 weeks and relative perch position somewhat stable. Males were dominant over females in contests over food and perched in higher positions. These sex differences were not explained by males' greater size or body weight. Food dominance and perch position were uncorrelated. Neither early life food supply nor early life begging effort affected food dominance; nor did an alternative measure of developmental stress, developmental telomere attrition. Birds that had been made to beg more as nestlings perched in higher positions than those that had begged less. Our results did not support the hypothesis that early life adversity leads to lower adult dominance rank in the context of feeding, and we suggest that relative perch position may have measured individual preference rather than competitive ability.

Early-life adversity accelerates cellular ageing and affects adult inflammation: Experimental evidence from the European starling.

Early-life adversity is associated with accelerated cellular ageing during development and increased inflammation during adulthood. However, human studies can only establish correlation, not causation, and existing experimental animal approaches alter multiple components of early-life adversity simultaneously. We developed a novel hand-rearing paradigm in European starling nestlings (Sturnus vulgaris), in which we separately manipulated nutritional shortfall and begging effort for a period of 10 days. The experimental treatments accelerated erythrocyte telomere attrition and increased DNA damage measured in the juvenile period. For telomere attrition, amount of food and begging effort exerted additive effects. Only the combination of low food amount and high begging effort increased DNA damage. We then measured two markers of inflammation, high-sensitivity C-reactive protein and interleukin-6, when the birds were adults. The experimental treatments affected both inflammatory markers, though the patterns were complex and different for each marker. The effect of the experimental treatments on adult interleukin-6 was partially mediated by increased juvenile DNA damage. Our results show that both nutritional input and begging effort in the nestling period affect cellular ageing and adult inflammation in the starling. However, the pattern of effects is different for different biomarkers measured at different time points.

Evolution of elaborate parental care: phenotypic and genetic correlations between parent and offspring traits.

The evolution of elaborate forms of parental care is an important topic in behavioral ecology, yet the factors shaping the evolution of complex suites of parental and offspring traits are poorly understood. Here, we use a multivariate quantitative genetic approach to study phenotypic and genetic correlations between parental and offspring traits in the burying beetle Nicrophorus vespilloides. To this end, we recorded 2 prenatal traits (clutch size and egg size), 2 postnatal parental behaviors (direct care directed toward larvae and indirect care directed toward resource maintenance), 1 offspring behavior (begging), and 2 measures of breeding success (larval dispersal mass and number of dispersing larvae). Females breeding on larger carcasses provided less direct care but produced larger larvae than females breeding on smaller carcasses. Furthermore, there were positive phenotypic correlations between clutch size, direct, and indirect care. Both egg size and direct care were positively correlated with dispersal mass, whereas clutch size was negatively correlated with dispersal mass. Clutch size and number of dispersed larvae showed genetic variance both in terms of differences between populations of origin and significant heritabilities. However, we found no evidence of genetic variance underlying other parental or offspring traits. Our results suggest that correlations between suites of parental traits are driven by variation in individual quality rather than trade-offs, that some parental traits promote offspring growth while others increase the number of offspring produced, and that parental and offspring traits might respond slowly to selection due to low levels of additive genetic variance.

Adaptive principles of weight regulation: Insufficient, but perhaps necessary, for understanding obesity.

We reflect on the major issues raised by a thoughtful and diverse set of commentaries on our target article. We draw attention to the need to differentiate between ultimate and proximate explanation; the insurance hypothesis (IH) needs to be understood as an ultimate-level argument, although we welcome the various suggestions made about proximate mechanisms. Much of this response is concerned with clarifying the interrelationships between adaptationist explanations like the IH, constraint explanations, and dysfunction explanations, in understanding obesity. We also re-examine the empirical evidence base, concurring that it is equivocal and only partially supportive. Several commentators offer additional supporting evidence, whereas others propose alternative explanations for the evidence we reviewed and suggest ways that our current knowledge could be strengthened. Finally, we take the opportunity to clarify some of the assumptions and predictions of our formal model.

Food insecurity as a driver of obesity in humans: The insurance hypothesis.

Integrative explanations of why obesity is more prevalent in some sectors of the human population than others are lacking. Here, we outline and evaluate one candidate explanation, the insurance hypothesis (IH). The IH is rooted in adaptive evolutionary thinking: The function of storing fat is to provide a buffer against shortfall in the food supply. Thus, individuals should store more fat when they receive cues that access to food is uncertain. Applied to humans, this implies that an important proximate driver of obesity should be food insecurity rather than food abundance per se. We integrate several distinct lines of theory and evidence that bear on this hypothesis. We present a theoretical model that shows it is optimal to store more fat when food access is uncertain, and we review the experimental literature from non-human animals showing that fat reserves increase when access to food is restricted. We provide a meta-analysis of 125 epidemiological studies of the association between perceived food insecurity and high body weight in humans. There is a robust positive association, but it is restricted to adult women in high-income countries. We explore why this could be in light of the IH and our theoretical model. We conclude that although the IH alone cannot explain the distribution of obesity in the human population, it may represent a very important component of a pluralistic explanation. We also discuss insights it may offer into the developmental origins of obesity, dieting-induced weight gain, and anorexia nervosa.

Brood size moderates associations between relative size, telomere length, and immune development in European starling nestlings.

For young birds in a nest, body size may have implications for other aspects of development such as telomere length and immune function. However, it is possible to predict associations in either direction. On the one hand, there may be trade-offs between growth and telomere maintenance, and growth and investment in immune function, suggesting there will be negative correlations. On the other hand, relatively larger individuals might be advantaged in competition with their nest-mates, allowing them to garner more resources overall, leading to positive correlations. We studied development over the nestling period in 34 nests of wild European starlings, Sturnus vulgaris. Intrabrood competition is typically more intense in larger broods. Hence, we predicted that body size should become an increasingly positive predictor of telomere length and immune functioning as brood size increases. In partial support of our prediction, there were significant interactions between brood size and body size in predicting both erythrocyte telomere length change and plasma levels of the cytokine interleukin-6. The associations between body size and these outcomes went from negative in the smallest broods to positive in the largest. A further immune marker, high-sensitivity C-reactive protein, showed no systematic patterning with body size or brood size. Our results confirm that the size to which a nestling grows is important for telomere dynamics and the development of the immune system, but the phenotypic associations are moderated by the competitive context.

Early life adversity increases foraging and information gathering in European starlings, Sturnus vulgaris.

Animals can insure themselves against the risk of starvation associated with unpredictable food availability by storing energy reserves or gathering information about alternative food sources. The former strategy carries costs in terms of mass-dependent predation risk, while the latter trades off against foraging for food; both trade-offs may be influenced by an individual's developmental history. Here, we consider a possible role of early developmental experience in inducing different mass regulation and foraging strategies in European starlings. We measured the body mass, body condition, foraging effort, food consumption and contrafreeloading (foraging for food hidden in sand when equivalent food is freely available) of adult birds (≥10 months old) that had previously undergone a subtle early life manipulation of food competition (cross-fostering into the highest or lowest ranks in the brood size hierarchy when 2-12 days of age). We found that developmentally disadvantaged birds were fatter in adulthood and differed in foraging behaviour compared with their advantaged siblings. Disadvantaged birds were hyperphagic compared with advantaged birds, but only following a period of food deprivation, and also spent more time contrafreeloading. Advantaged birds experienced a trade-off between foraging success and time spent contrafreeloading, whereas disadvantaged birds faced no such trade-off, owing to their greater foraging efficiency. Thus, developmentally disadvantaged birds appeared to retain a phenotypic memory of increased nestling food competition, employing both energy storage and information-gathering insurance strategies to a greater extent than their advantaged siblings. Our results suggest that subtle early life disadvantage in the form of psychosocial stress and/or food insecurity can leave a lasting legacy on foraging behaviour and mass regulation even in the absence of food insufficiency during development or adulthood.