Corticosterone facilitates begging and affects resource allocation in the black-legged kittiwake

Parent black-legged kittiwakes (Rissa tridactyla) and their dependent chicks respond to food shortages by increasing circulatinglevels of corticosterone. To examine the behavioral significanceof corticosterone release, we experimentally increased levelsof circulating corticosterone in parents and chicks up to thelevels observed during food shortages. We found that corticosterone-implantedchicks begged more frequently than sham-implanted controls.Corticosterone-implanted chicks in broods of two begged morefrequently than singletons. Parent kittiwakes then respondedto the increase in corticosterone levels in their chicks byincreasing chick-feeding rates. However, feeding rates werenot different among corticosterone-implanted chicks in broodsof two and singletons. We also found that corticosterone-implantedparents spent more time away from the nest—perhaps foraging—andless time brooding/guarding chicks than sham-implanted controls.Untreated mates of the corticosterone-implanted bird did notcompensate for the change in their partner's behavior; consequently, chicks were left unattended about 20% of the time compared to1% at the control nests. However, corticosterone-implantedparents did not decrease their chick-feeding rates. Our findingssuggest two functional implications of the increased corticosteronesecretion during food shortages in the black-legged kittiwake:it facilitates begging in chicks, and it affects time allocatedby parents to guarding young at the nest. Thus, release of corticosterone might provide a mechanistic link between physiological condition and behavioral interactions among adults and theiryoung.     

The adrenocortical response of tufted puffin chicks to nutritional deficits

In several seabirds, nutritional state of a nest-bound chick is negatively correlated with the activity of its hypothalamus–pituitary–adrenal (HPA) axis. Increased corticosterone (cort) secretion has been shown to facilitate changes in behavior that allow hungry chicks to obtain more food from parents. However, if parents are not willing/able to buffer their young from temporary food shortages, increased cort secretion could be detrimental to undernourished chicks. In a system where parents are insensitive to chick demands, low benefits and high costs of activation of the HPA-axis in hungry chicks should lead to a disassociation of the nutritional state of the young and the activity of its HPA-axis. We tested this novel hypothesis for the tufted puffin (Fratercula cirrhata), a seabird with intermittent provisioning of a nest-bound semi-precocial chick. We examined the HPA-axis activity of captive chicks exposed to the following: (1) a short-term (24 h) food deprivation; and (2) an array of prolonged (3 weeks) restrictions in feeding regimens. We found that in response to a short-term food deprivation chicks decreased baseline levels of cort and thyroid hormones. In response to prolonged restrictions, food-limited chicks exhibited signs of nutritional deficit: they had lower body mass, endogenous lipid reserves, and thyroid hormone titers compared to chicks fed ad libitum. However, baseline and maximum acute stress-induced levels of cort were also lower in food-restricted chicks compared to those of chicks fed ad libitum. These results support a major prediction of the study hypothesis that puffin chicks suppress HPA-axis activity in response to short- and long-term nutritional deficits. This physiological adaptation may allow a chick to extend its development in the nest, while eluding detrimental effects of chronic cort elevation.     

A mechanistic link between chick diet and decline in seabirds?

A climatic regime shift during the mid-1970s in the North Pacific resulted in decreased availability of lipid-rich fish to seabirds and was followed by a dramatic decline in number of kittiwakes breeding on the Pribilof Islands. Although production of chicks in the mid-1970s was adequate to sustain kittiwake populations in the early 1980s, the disappearance of birds from breeding colonies apparently exceeded recruitment. No mechanism has been proposed to explain why recruitment would differ among fledglings fed lipid-rich or lipid-poor fish during development. Here we show that diets low in lipids induce nutritional stress and impair cognitive abilities in young red-legged kittiwakes, Rissa brevirostris. Specifically, growth retardation, increased secretion of stress hormones and inferior ability to associate food distribution with visual cues were observed in individuals fed lipid-poor diets. We conclude that lipid-poor diets during development affect the quality of young seabirds, which is likely to result in their increased mortality and low recruitment.     

Sociality, glucocorticoids and direct fitness in the communally rearing rodent, Octodon degus

While ecological causes of sociality (or group living) have been identified, proximate mechanisms remain less clear. Recently, close connections between sociality, glucocorticoid hormones (cort) and fitness have been hypothesized. In particular, cort levels would reflect a balance between fitness benefits and costs of group living, and therefore baseline cort levels would vary with sociality in a way opposite to the covariation between sociality and fitness. However, since reproductive effort may become a major determinant of stress responses (i.e., the cort–adaptation hypothesis), cort levels might also be expected to vary with sociality in a way similar to the covariation between sociality and fitness. We tested these expectations during three years in a natural population of the communally rearing degu, Octodon degus. During each year we quantified group membership, measured fecal cortisol metabolites (a proxy of baseline cort levels under natural conditions), and estimated direct fitness. We recorded that direct fitness decreases with group size in these animals. Secondly, neither group size nor the number of females (two proxies of sociality) influenced mean (or coefficient of variation, CV) baseline cortisol levels of adult females. In contrast, cortisol increased with per capita number of offspring produced and offspring surviving to breeding age during two out of three years examined. Together, our results imply that variation in glucocorticoid hormones is more linked to reproductive challenge than to the costs of group living. Most generally, our study provided independent support to the cort–adaptation hypothesis, according to which reproductive effort is a major determinant, yet temporally variable, influence on cort–fitness covariation.     

Components of productivity in black-legged kittiwakes Rissa tridactyla: response to supplemental feeding

In contrast to the high productivity of black-legged kittiwakes in Britain, kittiwakes at many colonies in Alaska have failed chronically to reproduce since the mid 1970s. To determine if food is limiting productivity and, if so, at what stages of nesting food shortages are most severe, in 1996 and 1997 we supplementally fed kittiwakes nesting on an abandoned building. The effects of feeding were stronger in 1997 than in 1996, possibly because naturally occurring prey were of poorer quality in 1997. Consumption of supplemental herring declined as egg laying approached then increased slowly during incubation and more rapidly after hatching. All of the six components of productivity we studied were improved by supplemental feeding to some degree. Supplemental food did not significantly alter laying success in either year, although fed pairs bred at slightly higher rates than unfed pairs in 1997, the poorer food year. In 1996 and 1997, extra food noticeably increased clutch size and hatching success, but significantly so only in 1997. Fledging success and productivity were substantially augmented by feeding in both years. Fed pairs fledged twice as many chicks per nest as did unfed pairs in 1996 and three times as many in 1997. Fed and unfed pairs lost most of their potential productivity through the inability to hatch eggs, and secondarily because of their poor success at raising chicks. The benefits of supplemental feeding did not carry over from one stage of breeding to another. Pairs cut off from supplemental food after laying or hatching performed similarly to pairs that had not been previously fed. This study provides benchmark values of breeding performance attainable by kittiwakes in Alaska under optimal conditions. These values are comparable to highly productive colonies in Britain and suggest that differences in life-history characteristics between Pacific and Atlantic breeding populations are primarily controlled by food supply.     

Effects of investigator disturbance on corticosterone concentrations of Black‐legged Kittiwake chicks

ABSTRACT Recent studies indicate that young seabird chicks exposed to relatively short periods of elevated levels of plasma corticosterone may suffer lifelong cognitive impairment that is detrimental to their survivorship and fitness as adults. We examined the chronic effects of investigator disturbance on the baseline and acute stress‐induced levels of plasma corticosterone of Black‐legged Kittiwake (Rissa tridactyla) chicks in Chiniak Bay, Kodiak Island, Alaska, in 2005. Kittiwake chicks were assigned to one of three disturbance treatments: (1) routine handling, (2) exposure to investigator presence, but not handled, and (3) neither handled nor exposed to investigator presence prior to sampling. At 12–15 d posthatching, blood samples were collected to determine baseline and stress‐induced concentrations of corticosterone. We found no significant differences in baseline or stress‐induced levels of corticosterone among the three disturbance treatments. Our results suggest that Black‐legged Kittiwake chicks do not perceive investigator presence as a stressor. However, investigators studying kittiwakes at other locations should proceed with caution because sampling protocols and environmental conditions may differ, potentially causing chicks to perceive disturbances differently as well.     

Embryonic exposure to corticosterone modifies the juvenile stress response, oxidative stress and telomere length

Early embryonic exposure to maternal glucocorticoids can broadly impact physiology and behaviour across phylogenetically diverse taxa. The transfer of maternal glucocorticoids to offspring may be an inevitable cost associated with poor environmental conditions, or serve as a maternal effect that alters offspring phenotype in preparation for a stressful environment. Regardless, maternal glucocorticoids are likely to have both costs and benefits that are paid and collected over different developmental time periods. We manipulated yolk corticosterone (cort) in domestic chickens (Gallus domesticus) to examine the potential impacts of embryonic exposure to maternal stress on the juvenile stress response and cellular ageing. Here, we report that juveniles exposed to experimentally increased cort in ovo had a protracted decline in cort during the recovery phase of the stress response. All birds, regardless of treatment group, shifted to oxidative stress during an acute stress response. In addition, embryonic exposure to cort resulted in higher levels of reactive oxygen metabolites and an over-representation of short telomeres compared with the control birds. In many species, individuals with higher levels of oxidative stress and shorter telomeres have the poorest survival prospects. Given this, long-term costs of glucocorticoid-induced phenotypes may include accelerated ageing and increased mortality.     

A comparative study of the central effects of melanocortin peptides on food intake in broiler and layer chicks

Broiler chicks eat more food than layer chicks. However, the causes of the difference in food intake in the neonatal period between these strains are not clear. In this study, we examined the involvement of proopiomelanocortin (POMC)-derived melanocortin peptides α-, β- and γ-melanocyte-stimulating hormones (MSHs) in the difference in food intake between broiler and layer chicks. First, we compared the hypothalamic mRNA levels of POMC between these strains and found that there was no significant difference in these levels between broiler and layer chicks. Next, we examined the effects of central administration of MSHs on food intake in these strains. Central administration of α-MSH significantly suppressed food intake in both strains. Central administration of β-MSH significantly suppressed food intake in layer chicks, but not in broiler chicks, while central administration of γ-MSH did not influence food intake in either strain. It is therefore likely that the absence of the anorexigenic effect of β-MSH might be related to the increased food intake in broiler chicks.     

Costs of memory: lessons from 'mini' brains

Variation in learning and memory abilities among closely related species, or even among populations of the same species, has opened research into the relationship between cognition, ecological context and the fitness costs, and benefits of learning and memory. Such research programmes have long been dominated by vertebrate studies and by the assumption of a relationship between cognitive abilities, brain size and metabolic costs. Research on these 'large brained' organisms has provided important insights into the understanding of cognitive functions and their adaptive value. In the present review, we discuss some aspects of the fitness costs of learning and memory by focusing on 'mini-brain' studies. Research on learning and memory in insects has challenged some traditional positions and is pushing the boundaries of our understanding of the evolution of learning and memory.     

With a little help from my kin: barn swallow nestlings modulate solicitation of parental care according to nestmates' need

In altricial species, offspring competing for access to limiting parental resources (e.g. food) are selected to achieve an optimal balance between the costs of scrambling for food, the benefits of being fed and the indirect costs of subtracting food to relatives. As the marginal benefits of acquiring additional food decrease with decreasing levels of need, satiated offspring should be prone to favour access to food by their needy kin, thus enhancing their own indirect fitness, while concomitantly reducing costs of harsh competition with hungry broodmates. We tested this prediction in feeding trials of barn swallow (Hirundo rustica) nestlings by comparing begging behaviour and food intake of two similar-sized nestmates, one of which was food-deprived (FD). Non-food-deprived (NFD) offspring modulated begging intensity depending on their nestmate's need: when competing with FD nestmates, NFD nestlings reduced both the intensity and frequency of begging displays compared to themselves in the control trial before food deprivation. Hence, NFD nestlings reduced their competitiveness to the advantage of FD nestmates, which obtained more feedings and showed a threefold larger increase in body mass. Moderation of individual selfishness can therefore be adaptive in the presence of a needier kin, because the indirect fitness benefits of promoting its condition can outweigh the costs of forgoing being fed, and because it limits the cost of begging escalation against a vigorous competitor.     

Should males come first? The relationship between offspring hatching order and sex in the black‐headed gull Larus ridibundus

In birds with hatching asynchrony and sexual size dimorphism, chicks hatched earlier and later in the laying sequence usually suffer different mortalities due to uneven abilities to compete for food, especially in poor years. If sexes differ in vulnerability to environmental conditions, e.g., by having different food requirements due to differential growth rates, mothers can increase fitness by allocating sex according to the laying order, producing less vulnerable sex later rather than early in the clutch. By analysing variation in primary sex ratio using a PCR-based DNA technique, we tested this prediction in black-headed gull Larus ridibundus chicks where males may be the less viable sex under adverse conditions. The overall primary sex ratio of the population did not depart from parity. However, first hatched chicks were more likely to be males whereas last hatched chicks were more likely to be females. Both egg volume and hatchling body mass decreased with laying order irrespective of sex. Time of breeding had no effect on offspring sex or hatchling sex ratios.     

Robust feeding following central administration of neuropeptide Y or peptide YY in chicks, Gallus domesticus

Neuropeptide Y (NPY) and peptide YY (PYY) were injected intracerebroventricularly (ICV) in broiler chicks. Both NPY and PYY markedly increased food intake during the first hour post-injection compared to saline (SAL) controls. Food intake doubled in chicks given 5 micrograms NPY. A response surface analysis suggested that following ICV injection of NPY, maximum food intake occurred, using a dose of 9 micrograms. In contrast, an estimated dose between one and 5 micrograms PYY resulted in maximum food intake, giving the latter a slightly higher potency. Time spent drinking was not significantly different among NPY, PYY and SAL groups. Chicks given NPY or PYY also spent significantly less time standing while those given PYY spent significantly less time preening compared to controls.     

The adrenocortical stress-response of Black-legged Kittiwake chicks in relation to dietary restrictions

In this study we examined hormonal responses of Black-legged Kittiwake (Rissatridactyla) chicks to experimental variations in energy content and nutritional quality (low or high lipid to protein ratio, LPR) of their food. Starting at the age of 10 days, chicks were fed either high or low LPR fish at 30, 50, 70 and 100% of ad libitum energy intake. After 20 days of treatment, chicks were exposed to a standardized acute handling and restraint stress protocol, where a baseline sample was taken immediately after taking a chick from the nest, and three additional blood samples were taken at intervals up to 50 min. Testosterone and corticosterone titres in plasma were measured via radioimmunoassay. We found that baseline testosterone levels were not significantly affected by the experimental treatments. Food-restricted chicks had elevated baseline and acute stress-induced levels of corticosterone compared to chicks fed ad libitum. An elevation of circulating levels of corticosterone in energetically stressed individuals was further magnified by low nutritional quality of food. Baseline and acute stress-induced corticosterone levels of chicks were negatively correlated with their fat reserves. We conclude that the physiological condition of Black-legged Kittiwake chicks can be assessed reliably by measuring circulating levels of corticosterone. We discuss short- and long-term effects of elevated corticosterone secretion in food-stressed nest-bound chicks. Accepted: 13 April 1999     

Neuropeptide Y effect on food intake in broiler and layer chicks

Broiler chicks eat more food than layer chicks. In this study, we examined the involvement of orexigenic peptide neuropeptide Y (NPY) in the difference in food intake between broiler and layer chicks (Gallus gallus). First, we compared the hypothalamic mRNA levels of NPY and its receptors (Y1 and Y5 receptors) between these strains at 1, 2, 4, and 8 days of age. Daily food intake was significantly higher in broiler chicks than layer chicks after 2 days of age. However, the hypothalamic NPY mRNA level was significantly lower in broiler chicks than layer chicks except at 8 days of age. In addition, the mRNA levels of NPY receptors were also significantly lower in broiler chicks than layer chicks at 2 and 4 days of age (Y1 receptor) or 2 days of age (Y5 receptor). These results suggest that the differences in the expressions of hypothalamic NPY and its receptors do not cause the increase in food intake in broiler chicks. To compare the orexigenic effect of NPY between broiler and layer chicks, we next examined the effects of central administration of NPY on food intake in these strains. In both strains, central administration of NPY significantly increased food intake at 2, 4 and 8 days of age. All our findings demonstrated that the increase in food intake in broiler chicks is not accompanied with the over-expression of NPY or its receptor.     

Smart is the new sexy: female mountain chickadees increase reproductive investment when mated to males with better spatial cognition

Understanding the evolution of inter and intraspecific variation in cognitive abilities is one of the main goals in cognitive ecology. In scatter‐caching species, spatial memory is critical for the recovery of food caches and overwinter survival, but its effects on reproduction are less clear. Better spatial cognition may improve pre‐breeding condition allowing for earlier reproduction. Alternatively, when mated to males with better spatial memory, females may be able to invest more in reproduction which may allow increased offspring survival and hence higher fitness. Using wild food‐caching mountain chickadees, we found that when environmental conditions were favourable for breeding, females mated to males with better spatial cognition laid larger clutches and fledged larger broods than females mated to males with worse cognitive performance. Our results support the hypothesis that females may increase their reproductive investment to gain indirect, genetic benefits when mated to high‐quality males with better spatial cognitive abilities.     

Effects of begging on growth rates of nestling chicks

We investigated whether an increase in begging levels delaysgrowth of chicks. In experiment 1, we hand-reared nine pairsof ring dove squabs, divided into a control and a begging group.All squabs received similar amounts of food, but those in thebegging group had to beg for a prolonged period in order tobe fed, while squabs in the control group received food withoutbegging. Squabs stopped responding to the treatment after 10days and, at that time, there was no effect of induced beggingon their body mass. In experiment 2, we hand-reared 27 pairsof magpie chicks for 3 days. The design of experiment 2 wassimilar to that of experiment 1. Daily food intake and beggingaffected growth rates. On average, chicks in the begging groupgrew 0.8 g/day less than control chicks, which represents adecrease of 8.15% in growth rate. Because growth is usuallypositively associated with expected fitness, this demonstratesthat begging is a costly behavior, an assumption routinelymade in models of begging behavior.     

Hypothalamic gonadotropin-inhibitory hormone precursor mRNA is increased during depressed food intake in heat-exposed chicks

The regulation of food intake in chickens (Gallus gallus domesticus) represents a complex homeostatic mechanism involving multiple levels of control, and regulation during high ambient temperatures (HT) is poorly understood. In this study, we examined hypothalamic mRNA expression of gonadotropin-inhibitory hormone (GnIH) to understand the effect of HT on an orexigenic neuropeptide. We examined the effects of HT (35 °C ambient temperature for 1, 24 or 48 h) on 14-day old chicks. HT significantly increased rectal temperature and suppressed food intake, and also influenced plasma metabolites. The expression of GnIH precursor mRNA in the diencephalon was significantly increased in chicks at 24-and 48 h of HT when food intake was suppressed significantly, whilst no change was observed for GnIH precursor mRNA and food intake at 1h of HT. In situ hybridization and immunocytochemistry further revealed the cellular localization of chicken GnIH precursor mRNA and its peptide in the paraventricular nucleus (PVN) in the chick hypothalamus. We examined plasma metabolites in chicks exposed to HT for 1 or 48 h and found that triacylglycerol concentration was significantly higher in HT than control chicks at 1h. Total protein, uric acid and calcium were significantly lower in HT chicks than control chicks at 48h. These results indicate that not only a reduction in food intake and alteration in plasma metabolites but also the PVN-specific expression of GnIH, an orexigenic agent, may be induced by HT. The reduced food intake at the same time as GnIH expression was increased during HT suggests that HT-induced GnIH expression may oppose HT-induced feeding suppression, rather than promote it. We suggest that the increased GnIH expression could be a consequence of the reduced food intake, and would not be a direct response to HT.     

Context‐dependent effects of yolk androgens on nestling growth and immune function in a multibrooded passerine

Female birds may adjust their offspring phenotype to the specific requirements of the environment by differential allocation of physiologically active substances into yolks, such as androgens. Yolk androgens have been shown to accelerate embryonic development, growth rate and competitive ability of nestlings, but they can also entail immunological costs. The balance between costs and benefits of androgen allocation is expected to depend on nestling environment. We tested this hypothesis in a multibrooded passerine, the spotless starling, Sturnus unicolor. We experimentally manipulated yolk androgen levels using a between‐brood design and evaluated its effects on nestling development, survival and immune function. Both in first and replacement broods, the embryonic development period was shorter for androgen‐treated chicks than controls, but there were no differences in second broods. In replacement broods, androgen‐treated chicks were heavier and larger than those hatched from control eggs, but this effect was not observed in the other breeding attempts. Androgen exposure reduced survival with respect to controls only in second broods. Regarding immune function, we detected nonsignificant trends for androgen treatment to activate two important components of innate and adaptive immunity (IL‐6 and Ig‐A levels, respectively). Similarly, androgen‐treated chicks showed greater lymphocyte proliferation than controls in the first brood and an opposite trend in the second brood. Our results indicate that yolk androgen effects on nestling development and immunity depend on the environmental conditions of each breeding attempt. Variation in maternal androgen allocation to eggs could be explained as the result of context‐dependent optimal strategies to maximize offspring fitness.     

The stress of parenthood? Increased glucocorticoids in birds with experimentally enlarged broods

Variation in baseline glucocorticoid (cort) levels can be attributed, at least in part, to differences in energetic demands confronting individuals. Elevated baseline cort levels are routinely interpreted as indicating individuals in poor condition, with low relative fitness. However, when greater reproductive effort increases energetic demands, individuals with high cort might paradoxically be those with the highest fitness. Here, we experimentally test the hypothesis that increased reproductive demand causes increases in baseline cort (the Cort-Adaptation hypothesis). We measured maternal baseline cort before and after experimentally enlarging and reducing brood sizes in tree swallows (Tachycineta bicolor). Females with experimentally enlarged broods had greater increases in baseline cort and fledged more offspring than females with reduced broods. Additionally, females with greater increases in baseline cort had higher offspring-provisioning rates than females with lower changes in cort. These findings demonstrate that increased reproductive demand can cause increased baseline cort. As yet, we do not know if these increases in cort cause increased allocation of resources towards reproduction, but the positive relationship between parental behaviour and cort suggests that increased cort does not always interfere with reproductive investment, and might instead facilitate it.     

Triiodothyronine (T3) stimulates food intake via enhanced hypothalamic AMP-activated kinase activity

Thyroid hormone regulates food intake. We previously reported that rats with triiodothyronine (T3)-induced thyrotoxicosis display hyperphagia associated with suppressed circulating leptin levels, increased hypothalamic neuropeptide Y (NPY) mRNA and decreased hypothalamic pro-opiomelanocortin (POMC) mRNA. AMP-activated kinase (AMPK) is a serine/threonine protein kinase that is activated when cellular energy is depleted. We hypothesized that T3 causes an increase in hypothalamic AMPK activity, which in turn contributes to the development of T3-induced hyperphagia. Rats that were given s.c. injections of T3 (4.5 nmol/kg) had increased food intake 2 h later without alterations in NPY and POMC mRNA levels, but with increased hypothalamic phosphorylated AMPK (169%) and phosphorylated acetyl-CoA carboxylase (194%). To determine the more chronic effects of T3, rats were given 6 daily s.c. injection of T3 or the vehicle. Food intake was significantly increased. Multiple T3 injections increased hypothalamic phosphorylated AMPK (278%) and phosphorylated acetyl-CoA carboxylase (335%) compared to the controls. Intracerebroventricular administration of compound C, an AMPK inhibitor, blocked the food intake induced by a single or multiple injections of T3. Taken together, these results suggest that enhanced hypothalamic AMPK phosphorylation contributes to T3-induced hyperphagia. Hypothalamic AMPK plays an important role in the regulation of food intake and body weight.