Nocturnal loss of body reserves reveals high survival risk for subordinate great tits wintering at extremely low ambient temperatures

Winter acclimatization in birds is a complex of several strategies based on metabolic adjustment accompanied by long-term management of resources such as fattening. However, wintering birds often maintain fat reserves below their physiological capacity, suggesting a cost involved with excessive levels of reserves. We studied body reserves of roosting great tits in relation to their dominance status under two contrasting temperature regimes to see whether individuals are capable of optimizing their survival strategies under extreme environmental conditions. We predicted less pronounced loss of body mass and body condition and lower rates of overnight mortality in dominant great tits at both mild and extremely low ambient temperatures, when ambient temperature dropped down to ?43 °C. The results showed that dominant great tits consistently maintained lower reserve levels than subordinates regardless of ambient temperature. However, dominants responded to the rising risk of starvation under low temperatures by increasing their body reserves, whereas subdominant birds decreased reserve levels in harsh conditions. Yet, their losses of body mass and body reserves were always lower than in subordinate birds. None of the dominant great tits were found dead, while five young females and one adult female were found dead in nest boxes during cold spells when ambient temperatures dropped down to ?43 °C. The dead great tits lost up to 23.83 % of their evening body mass during cold nights while surviving individuals lost on average 12.78 % of their evening body mass. Our results show that fattening strategies of great tits reflect an adaptive role of winter fattening which is sensitive to changes in ambient temperatures and differs among individuals of different social ranks.     

Social context, competitive interactions and the dynamic nature of antipredator responses of juvenile rainbow trout Oncorhynchus mykiss

The effects of food ration and social context, as well as possible interactions, on the antipredator behaviour of juvenile rainbow trout Onchorhynchus mykiss were investigated in a pair of laboratory studies. In experiment 1, pairs of dominant and subordinate O. mykiss were exposed to conspecific alarm cues when maintained under high or low food rations. Under high food rations, dominant individuals responded to predation risk, whereas subordinates used the opportunity to feed. Under low food ration, however, the opposite pattern was observed, where subordinates responded to predation cues and dominants did not. Experiment 2 consisted of performing the same experiment, however separating the dominant and subordinate O. mykiss 3 h before testing. When tested separately, dominant and subordinate individuals did not differ in their responses to alarm cues, regardless of food ration. These results demonstrate that there is a complex interaction between current energy status and social context on decision making by prey animals.     

Social influences on food caching in willow tits: a field experiment

We studied the food hoarding behavior of willow tits (Parusmontanus), a scatter-hoarding passerine wintering in dominance-structuredflocks. We examined social influences on microhabitat selectionand spatial cache distribution at temporary feeders. Dominantadult males stored food closer to die feeder and at a greaterrate than did subordinates. When alone, the birds stored foodcloser to the feeder than when accompanied by conspecifics.Conifers were preferred over deciduous trees as cache trees.The subordinates cached more in die outer parts of branchesthan dominants. There were no significant differences in dierelative or absolute heights of die caches, nor in the verticalor horizontal hoarding niche breadths between dominants andsubordinates. We experimentally removed die dominants from dieflock for 90 min and recorded the behavior of die remainingsubordinates immediately after die removal. The removal resultedin a decrease in die hoarding distance of die remaining birds,indicating that die presence of dominants directly affecteddie behavior of subordinates and suggesting that kleptopar-asitismby dominants may be prevented by rarhing farther away. Withdie dominants removed, die subordinates cached at a greaterrate than before die removal. The decrease in die hoarding distanceand increase in die hoarding rate were die only significanteffects of die experiment, perhaps suggesting that, during ashort absence of dominants, die subordinates do not benefitfrom changing dieir caching microhabitat They might be excludedfrom those new, possibly safer, microhabitats after die dominantbird rejoins die flock.     

The relationship between dominance, corticosterone, memory, and food caching in mountain chickadees (Poecile gambeli)

It has been hypothesized that in avian social groups subordinate individuals should maintain more energy reserves than dominants, as an insurance against increased perceived risk of starvation. Subordinates might also have elevated baseline corticosterone levels because corticosterone is known to facilitate fattening in birds. Recent experiments showed that moderately elevated corticosterone levels resulting from unpredictable food supply are correlated with enhanced cache retrieval efficiency and more accurate performance on a spatial memory task. Given the correlation between corticosterone and memory, a further prediction is that subordinates might be more efficient at cache retrieval and show more accurate performance on spatial memory tasks. We tested these predictions in dominant-subordinate pairs of mountain chickadees (Poecile gambeli). Each pair was housed in the same cage but caching behavior was tested individually in an adjacent aviary to avoid the confounding effects of small spaces in which birds could unnaturally and directly influence each other's behavior. In sharp contrast to our hypothesis, we found that subordinate chickadees cached less food, showed less efficient cache retrieval, and performed significantly worse on the spatial memory task than dominants. Although the behavioral differences could have resulted from social stress of subordination, and dominant birds reached significantly higher levels of corticosterone during their response to acute stress compared to subordinates, there were no significant differences between dominants and subordinates in baseline levels or in the pattern of adrenocortical stress response. We find no evidence, therefore, to support the hypothesis that subordinate mountain chickadees maintain elevated baseline corticosterone levels whereas lower caching rates and inferior cache retrieval efficiency might contribute to reduced survival of subordinates commonly found in food-caching parids.     

Fattening strategies of wintering great tits support the optimal body mass hypothesis under conditions of extremely low ambient temperature

1.  In a seasonal environment, subcutaneous energy reserves of resident animals often increase in winter and decline again in summer reflecting gradual seasonal changes in their fattening strategies. We studied changes in body reserves of wintering great tits in relation to their dominance status under two contrasting temperature regimes to see whether individuals are capable of optimizing their body mass even under extreme environmental conditions.
2.  We predicted that dominant individuals will carry a lesser amount of body reserves than subordinate great tits under mild conditions and that the body reserves of the same dominant individuals will increase and exceed the amount of reserves of subordinates under conditions of extremely low ambient temperatures, when ambient temperature dropped down to −37 °C.
3.  The results confirmed the predictions showing that dominant great tits responded to the rising risk of starvation under low temperatures by increasing their body reserves and this was done at the expense of their safety.
4.  Removal experiments revealed that lower body reserves of subordinate flock members are due to the increased intraspecific competition for food under low ambient temperatures.
5.  Our results also showed that fattening strategies of great tits may change much quicker than previously considered, reflecting an adaptive role of winter fattening which is sensitive to changes in ambient temperatures.     

Fat reserves and perceived predation risk in the great tit, Parus major

The fat reserves of small birds are built up daily as insurance against starvation. They are believed to reflect a trade-off between the risks of starvation and predation such that in situations of high predation risk birds are expected either to reduce their fat reserves in response to mass-dependent predation risk or to increase them in response to foraging interruptions. We assessed the effect on fat reserves of experimentally altering the perceived (but not the actual) risk of predation of wild great tits at a winter feeding site. The perceived predation risk was alternated between 'safe' and 'risky'. Increasing the perceived risk of predation involved 'swooping' a model sparrowhawk over the feeder at four unpredictable times each day using a remote mechanism We produce evidence that the experiment was suceessfull in altering the perceived risk of predation. As predicted from the hypothesis of mass-dependent predation risk, great tits (Parus major) carried significantly reduced fat reserves during the 'risky' treatment. Furthermore, dominant individuals were able to reduce their reserves more than subordinates. As birds returned to feeders within seconds after a predator 'attack', the reduction in fat reserves cannot be attributed to an interruption in feeding.     

Coal tits increase evening body mass in response to tawny owl calls

Current theory predicts small birds should have a reduced body mass when daytime predation risk is high. However, the influence that nighttime predators might have on changes in body mass or daytime foraging behaviour has not been addressed. We therefore studied the effect of changes in perceived nocturnal predation risk on the body mass of captive coal tits. In a soundproof room, eight coal tits were housed in individual cages and an experiment was performed in which the birds were subjected to two treatments. First, morning and evening body mass was monitored following nights that were quiet. Second, these parameters were measured following nights when the call of a tawny owl had been played once per hour. Evening body mass was 3% greater on days following owl-disturbed nights, but morning body masses did not differ between treatments. To ensure this result was a response to the owl calls per se, and not a general response to increased disturbance, a second experiment was necessary. Here the coal tits were exposed hourly to the calls of a nightjar, a non-predatory nocturnal bird, but no increases in body mass were observed compared to quiet nights. We suggest the coal tits increased body mass in response to owl calls to offset increased nighttime energy expenditure in attentive behaviour. Received: 26 July 1999 / Received in revised form: 30 October 1999 / Accepted: 29 November 1999     

Social interactions modulate the virulence of avian malaria infection

There is an increasing understanding of the context-dependent nature of parasite virulence. Variation in parasite virulence can occur when infected individuals compete with conspecifics that vary in infection status; virulence may be higher when competing with uninfected competitors. In vertebrates with social hierarchies, we propose that these competition-mediated costs of infection may also vary with social status. Dominant individuals have greater competitive ability than competing subordinates, and consequently may pay a lower prevalence-mediated cost of infection. In this study we investigated whether costs of malarial infection were affected by the occurrence of the parasite in competitors and social status in domestic canaries (Serinus canaria). We predicted that infected subordinates competing with non-infected dominants would pay higher costs than infected subordinates competing with infected dominants. We also predicted that these occurrence-mediated costs of infection would be ameliorated in infected dominant birds. We found that social status and the occurrence of parasites in competitors significantly interacted to change haematocrit in infected birds. Namely, subordinate and dominant infected birds differed in haematocrit depending on the infection status of their competitors. However, in contrast to our prediction, dominants fared better with infected subordinates, whereas subordinates fared better with uninfected dominants. Moreover, we found additional effects of parasite occurrence on mortality in canaries. Ultimately, we provide evidence for costs of parasitism mediated by social rank and the occurrence of parasites in competitors in a vertebrate species. This has important implications for our understanding of the evolutionary processes that shape parasite virulence and group living.     

Food supplementation and predation risk in harsh climate: interactive effects on abundance and body condition of tit species

Food availability and predation risk can have drastic impacts on animal behaviour and populations. The tradeoff between foraging and predator avoidance is crucial for animal survival and will strongly affect individual body mass, since large fat reserves are beneficial to reduce starvation but may increase predation risk. However, two‐factor experiments simultaneously investigating the interactive effects of food and predation risk, are still rare. We studied the effects of food supplementation and natural predation risk imposed by pygmy owls Glaucidium passerinum on the abundance and fat reserves of tit species in boreal forests of north Europe, from January to March in 2012 and in 2013. Food supplementation increased the number of individuals present in a given forest patch, whereas the level of predation risk had no clear impact on the abundance of tit species. The stronger impact of food supply respect to predation risk could be the consequence of the harsh winter conditions in north Europe, with constant below‐zero temperatures and only few (5–7 h) daylight hours available for foraging. Predation risk did not have obvious effects on tit abundance but influenced food consumption and, together with food supplementation, affected the deposition of subcutaneous fat in great tits Parus major. High owl predation risk had detrimental effects on body fat reserves, which may reduce over‐winter survival, but the costs imposed by pygmy owl risk were compensated when food was supplemented. The starvation–predation tradeoff faced by great tits in winter may thus be mediated through variation in body fat reserves. In small species living in harsh environment, this tradeoff appeared thus to be biased towards avoidance of starvation, at the cost of increasing predation risk.     

The effect of social dominance on fattening and food-caching behaviour in Carolina chickadees, Poecile carolinensis

Subordinates often have to wait for dominants to obtain food. As a result, their foraging success should be less predictable and they should therefore maintain a higher level of energy reserves compared with dominants. A corollary of this prediction is that subordinates should gain mass earlier in the day and maintain higher mass than dominants. We tested these predictions with captive Carolina chickadees. In two different experiments (one where birds were given ad libitum access to food and the other with food access limited to 60 min/day), we formed social flocks of two previously unfamiliar birds and compared their energy management (body fat and food caches) while they were in the flock with energy management when housed alone. Results from both experiments failed to support the predictions. Of all the parameters of body mass and food caching we measured only the following results were significant: (1) On the ad libitum food schedule, both subordinates and dominants accumulated more mass over the day when in a flock compared with when they were solitary, and there were no differences in mass gain between dominants and subordinates. (2) When analysed separately, dominants showed a higher evening mass in the flock compared with the solitary condition, a trend that runs opposite to the prediction. Our results suggest that when in favourable foraging conditions, social interactions might cause dominant and subordinate birds to accumulate more energy reserves as a result of competition. On the other hand, if food supply is limited, both dominants and subordinates may be forced to maintain similar fat reserves as an insurance against increased risk of starvation. Copyright 2000 The Association for the Study of Animal Behaviour.     

Social stability and daily body mass gain in great tits

This paper presents the results of an experiment on the influenceof changes in flock composition and social rank on the patternof daily mass gain in captive wintering great tits. We createdflocks of three male great tits and scored dominance when rankshad stabilized after a few days. We then moved the dominantbird from each flock into a neighboring flock, thus creatinga certain amount of social instability and unpredictable resourceaccess. Both before and after moving the dominants, we collectedindividual body mass data three times a day. When the hierarchieshad stabilized in the second flocks, individual ranks were scored.After the dominant birds were moved, the rate of daily massgain increased for the average individual. There was also adecrease in average morning body mass, so the birds startedthe day at a lower mass and ended at a slightly higher massthan previously. Dominants were on average heavier than subordinates,but we found no statistically significant effect of rank changeon body mass. The pattern of daily mass gain was linear overtime both before and after treatment. We conclude that an impressionof unpredictable resource access can be created by disturbingthe social structure in a flock, with similar effect as fromrestricting individual access to feeders. Within a flock, instabilityof the social hierarchy thus seems to have an influence on bodymass management in addition to that of environmental stochasticity.     

Effect of the Presence of Subordinates on Dominant Female Behaviour and Fitness in Hierarchies of the Dwarf Angelfish Centropyge bicolor

In many hierarchical animal societies, dominant individuals control group membership owing to their power to evict subordinates. In such groups, the presence of subordinates, and therefore group stability, is continually dependent on subordinates being tolerated by dominants. The dominant decision to tolerate or evict is, in turn, dependent on the costs and benefits to dominants of subordinate presence. We investigated the effect of subordinate presence on dominants in the female dominance hierarchy of the dwarf angelfish Centropyge bicolor, using both observations of natural groups and experimental removals of subordinates. We found that the presence of subordinates had no effect on dominant access to resources, as measured by dominant foraging rates and home range areas, nor on dominant fitness, as measured by growth rates and spawning frequencies. Our results suggest that the presence of subordinates has a neutral effect on the current fitness of dominants, so that dominants have no great incentive to evict subordinates. We discuss the possibility that tolerance of subordinates might be further explained by considering future fitness, as dominant females in these haremic protogynous angelfish stand to inherit the male position, whereupon subordinate females change from potential competition to useful mates.     

The function of threat display in wintering great tits

It is generally accepted that threat displays have signal function and serve to repel opponents, but why they should have such an effect is a matter of debate. Using videotaped interactions from 2 years and nine flocks each year, we analysed the pattern of occurrence of agonistic displays and attacks in captive flocks of wintering great tits, Parus major. One currently influential perspective is to view threat interactions as sequences of distinct moves and countermoves, in which stronger threats can reliably indicate aggressive motivation because they carry a cost of eliciting counterattacks from certain opponents. We found little evidence for this kind of mechanism operating in great tits. Another possibility is that social dominance is important in ensuring reliable communication, for instance because an individual needs both to display and to attack to maintain its rank. It would be hard to test the importance of this kind of mechanism directly, but our observations were consistent with such an idea. Dominants won the majority of bouts of interaction and had higher rates of display and attack than subordinates, but a subordinate could temporarily overcome a dominant through intense aggression. We also found that the level of displaying in one bout provided information about the rate of aggression in following bouts. As a general interpretation of great tit aggressive behaviour, we suggest that particular displays form part of a graded signal of motivational state, so that a greater rate of displaying or a greater proportion of intense displays, together with a greater rate of attacking, correspond to a greater aggressive motivation. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Predation risk is unlikely to account for the failure of subordinate speckled warblers Chthonicola sagittata to help at the nest

The predator avoidance hypothesis suggests that the failure of subordinate birds to provision nestlings in communally breeding species is a consequence of increased predation risk. Parents exclude subordinates from the nest area and thus reduce the frequency of predator-attracting visits when the nest is most vulnerable, leading to increased reproductive success. I evaluated this hypothesis for the speckled warbler Chthonicola sagittata , a group-living member of the Pardalotidae in which subordinate males never feed nestlings or fledglings even though they are unrelated to the primary pair, compete for copulations and sometimes sire young in the brood. Parents did not modify provisioning behaviour relative to the risk of nest predation; provisioning rates to 10 d-old nestlings were similar on high and low risk territories. Furthermore, there was no evidence that parents modified the timing of deliveries or adjusted the relative size of deliveries in relation to predation risk. The condition (residual mass) of nestlings differed between high and low risk territories because nestlings on high risk territories had smaller tarsi but similar body mass to those at low risk. Tarsus length was the result of parental phenotype, not modified provisioning behaviour. Given that parents were unresponsive to predation risk, it seems unlikely that predation can account for the failure of subordinates to provision at the nest.     

Dominance, competition, and energetic reserves in the European starling, Sturnus vulgaris

We investigated the relationships between social dominance,competition for food, and strategies of body mass and fat regulationin the European starling (Sturnus vulgaris). In birds housedin groups of three, subdominant birds stored more fat than dominants.A removal experiment established a causal link between socialdominance and fat reserves; in groups that had the dominantindividual removed, the remaining birds reduced body mass andfat, relative to control groups that had the subordinate removed.In a second experiment, we investigated the influences of degreeof competition for food and dominance on body mass and fat reserves.Birds under high competition increased fat reserves and tendedto have higher body mass than birds under low competition. Theincrease in fat reserves was higher in the subdominants thanin the dominants. These results are consistent with hypothesesconcerning dominance-dependent access to food; subdominant birds,or birds under increased competition, may store more fat asan insurance against periods when food cannot be obtained. However,relations between dominance, body mass, and fat reserves mayalso arise through other proximate factors relating to dominance-dependentcosts and benefits of fat storage, such as predation risk andenergetic expenditure.     

The cost of dominance: suppressing subordinate reproduction affects the reproductive success of dominant female banded mongooses

Social species show considerable variation in the extent to which dominant females suppress subordinate reproduction. Much of this variation may be influenced by the cost of active suppression to dominants, who may be selected to balance the need to maximize the resources available for their own offspring against the costs of interfering with subordinate reproduction. To date, the cost of reproductive suppression has received little attention, despite its potential to influence the outcome of conflict over the distribution of reproduction in social species. Here, we investigate possible costs of reproductive suppression in banded mongooses, where dominant females evict subordinates from their groups, thereby inducing subordinate abortion. We show that evicting subordinate females is associated with substantial costs to dominant females: pups born to females who evicted subordinates while pregnant were lighter than those born after undisturbed gestations; pups whose dependent period was disrupted by an eviction attained a lower weight at independence; and the proportion of a litter that survived to independence was reduced if there was an eviction during the dependent period. To our knowledge, this is the first empirical study indicating a possible cost to dominants in attempting to suppress subordinate breeding, and we argue that much of the variation in reproductive skew both within and between social species may be influenced by adaptive variation in the effort invested in suppression by dominants.     

Familiarity Breeds Tolerance: the Development of Social Stability in Flocking Siskins (Carduelis spinus)

Behavioural integration associated with the fusion of two flocks is analyzed in captive siskins (Carduelis spinus) by quantifying changes in social behaviour with time since joining. In general there was an increase in the incidence of tolerant behaviour, supplanting attacks and hopping withdrawals with time since fusion of the flocks. However, the number of displays and flights showed the opposite, negative, trend. Taking dominance status into account, the greatest change in behaviour with time since joining is an increase in tolerance by dominants of new flock companions. Factorial analysis of correspondences was used to study how different birds changed their behaviour with time since joining a flock. This analysis showed that the introduction of new birds did not disrupt relationships with familiar birds, and that residents are dominant in interactions with the incoming new flock companions. The analysis also demonstrated that relationships within the new flock had stabilized 20 days after the flocks had joined. The characteristics of the socially integrated group of siskins are quite similar to those described by Rohwer & Ewald (1981) in their shepherds hypothesis: dominants tolerate their subordinates feeding in close proximity, offering them a profitable feeding area, but also supplant them to obtain food; both dominants and subordinates benefit from being in a flock. As a consequence, constant changes of membership in flocks is costly not only because birds lose dominance status, but also the advantages of clear dominant and subordinate roles.     

Reproductive skew in birds: models, problems and prospects

In recent years there has been a resurgence of interest in models to explain the partitioning of direct reproduction ('reproductive skew') among members of one sex within social groups. We review models of skew, identify problems of testing models, and consider how to make progress. One series of models assumes that dominants have complete control of subordinate reproduction, but may allow subordinates some reproduction as a way of enticing them to help or getting them to share the cost of reproduction. Another series of models assume that dominants have limited control of subordinate reproduction. Reproductive skew may also be affected by incest avoidance or control by the opposite sex. Models are largely untested because no study of birds has quantified all relevant parameters, and we see no prospect of this happening soon. A common simplifying approach is to test qualitative predictions about the effect on skew of relatedness among group members. However, these data alone cannot distinguish among models because models do not make unique predictions, partly because skew is also affected by other factors. A major problem in cooperatively-breeding birds is that any effect of relatedness will often be confounded by covariation with relatedness asymmetry and subordinate competitiveness. Progress can be made with the development of theory, controlling confounding variables through the choice of study species or types of social group, and, most importantly, testing assumptions underlying hypotheses.     

Allostatic load, social status and stress hormones: the costs of social status matter

Cooperation and social support are the major advantages of living in social groups. However, there are also disadvantages arising from social conflict and competition. Social conflicts may increase allostatic load, which is reflected in increased concentrations of glucocorticoids. We applied the emerging concept of allostasis to investigate the relation between social status and glucocorticoid concentrations. Animals in a society experience different levels of allostatic load and these differences may predict relative glucocorticoid concentrations of dominant and subordinate individuals. We reviewed the available data from free-ranging animals and generated, for each sex separately, phylogenetic independent contrasts of allostatic load and relative glucocorticoid concentrations. Our results suggest that the relative allostatic load of social status predicts whether dominants or subordinates express higher or lower concentrations of glucocorticoids. There was a significant correlation between allostatic load of dominance and relative glucocorticoid concentrations in both females and males. When allostatic load was higher in dominants than in subordinates, dominants expressed higher levels of glucocorticoids; when allostatic load was similar in dominants and subordinates, there were only minor differences in glucocorticoid concentrations; and when allostatic load was lower in dominants than in subordinates, subordinates expressed higher levels of glucocorticoids than dominants. To our knowledge, this is the first model that consistently explains rank differences in glucocorticoid concentrations of different species and sexes. The heuristic concept of allostasis thus provides a testable framework for future studies of how social status is reflected in glucocorticoid concentrations.     

How climate change might influence the starvation–predation risk trade-off response

Climate change within the UK will affect winter starvation risk because higher temperatures reduce energy budgets and are likely to increase the quality of the foraging environment. Mass regulation in birds is a consequence of the starvation–predation risk trade-off: decreasing starvation risk because of climate change should decrease mass, but this will be countered by the effects of predation risk, because high predation risk has a negative effect on mass when foraging conditions are poor and a positive effect on mass when foraging conditions are good. We tested whether mass regulation in great tits (Parus major) across the UK was related to temporal changes in starvation risk (winter temperature 1995–2005) and spatial changes in predation risk (sparrowhawk Accipiter nisus abundance). As predicted, great tits carried less mass during later, warmer, winters, demonstrating that starvation risk overall has decreased. Also, the effects of predation risk interacted with the effects of temperature (as an index of foraging conditions), so that in colder winters higher sparrowhawk abundance led to lower mass, whereas in warmer, later, winters higher sparrowhawk abundance led to higher mass. Mass regulation in a small bird species may therefore provide an index of how environmental change is affecting the foraging environment.