Vladimir V. Pravosudov

Long-term moderate elevation of corticosterone facilitates avian food-caching behaviour and enhances spatial memory

It is widely assumed that chronic stress and corresponding chronic elevations of glucocorticoid levels have deleterious effects on animals brain functions such as learning and memory. Some animals, however, appear to maintain moderately elevated levels of glucocorticoids over long periods of time under natural energetically demanding conditions, and it is not clear whether such chronic but moderate elevations may be adaptive. I implanted wild–caught food–caching mountain chickadees (Poecile gambeli), which rely at least in part on spatial memory to find their caches, with 90–day continuous time–release corticosterone pellets designed to approximately double the baseline corticosterone levels. Corticosterone–implanted birds cached and consumed significantly more food and showed more efficient cache recovery and superior spatial memory performance compared with placebo–implanted birds. Thus, contrary to prevailing assumptions, long–term moderate elevations of corticosterone appear to enhance spatial memory in food–caching mountain chickadees. These results suggest that moderate chronic elevation of corticosterone may serve as an adaptation to unpredictable environments by facilitating feeding and food–caching behaviour and by improving cache–retrieval efficiency in food–caching birds.

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 others 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.

Toward a general theory of energy management in wintering birds

Once a bird of a species that caches food becomes independent from its parents, it has four possible sources of energy and nutrients: (1) food it has not found, (2) food it has collected and placed in cache sites the locations of which it has forgotten, (3) food it has collected and placed in cache sites the locations of which it has remembered, (4) food it has collected, ingested and cached internally as depot fat. Non-caching birds have only sources (1) and (4). In virtually all cases, a natural diet adequate in energy is also adequate in all specific nutrients (reviewed by Grubb 1989), so hereafter we will use the term energy to mean both energy and nutrients. Nonbreeding birds are assumed to manage the various forms of energy at their command in ways promoting survival until the next breeding season. Given the unitary nature of the selective force involved, namely increased survivorship, we should not expect management strategies for the various forms of energy to be independent. However, such an expectation tacitly underlies much theory and empirical study. Our intention here is first to review briefly the components of energy management that are currently drawing attention from researchers, then to focus on several promising lines of research for discovering the linkages necessary for a general theory. The bulk of our attention will be devoted to food-caching small passerines such as tits.

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 dominance and energy reserves in wintering Woodland birds

To understand animals tactics for surviving the winter season, we need to know how they manage their energy reserves. Fat reserves in small birds in winter generally increase with starvation risk. Studies have documented higher fat reserves in response to various sources of variability in energy intake or expenditure. Using three woodland species, Carolina Chickadee (Poecile carolinensis), Tufted Titmouse (Baeolophus bicolor), and White-breasted Nuthatch (Sitta carolinensis), we tested the prediction that the more predictable food supply of socially dominant animals enables them to maintain lower energetic reserves than subordinate conspecifics. We inferred dominance from age and sex categories. The hypothesis was fully supported. In all three species, dominants carried relatively lower fat reserves than subordinates.

Effects of dominance on vigilance in Avian Social Groups

During winter, many temperate-zone animals must survive harsh environmental conditions of low ambient temperatures, long nights, and unpredictable food supplies. Two evolutionary forces are thought to affect an individuals survivorship during winter: risk of starvation and risk of predation (Lima 1986, McNamara and Houston 1990, Grubb and Pravosudov 1994a, Pravosudov and Grubb 1997). Foraging and vigilance for predators appear to be mutually exclusive forms of behavior that an animal must trade off (Lima 1986). To reduce the risk of starvation, an animal must maximize the rate of foraging and energy intake, but to reduce the risk of predation, it must maximize its vigilance. Social foraging has been thought to benefit all members of a group by allowing each member to increase its foraging efficiency while sharing vigilance with the rest of the group (Elgar 1989). Vigilance in social groups of birds may be directed at predators or dominant group members (Waite 1987a, b; Elgar 1989). Recent studies have suggested that vigilance toward dominant individuals could be directed at both conspecifics and heterospecifics in multispecies groups (Popp 1988, Carrascal and Moreno 1992, Sasvari 1992). Ekman (1987) reported that subordinate Willow Tits (Parus montanus) were more vigilant than dominant individuals. Hogstad (1988a), on the other hand, reported the opposite trend, with dominant Willow Tits being more vigilant than subordinates. The latter report, however, was equivocal because in some instances juvenile females, which always have the lowest dominance rank, had the highest vigilance rates (Hogstad 1988a). However, the absolute rate of vigilance might not be the best measure of benefits for group members. Both studies of Willow Tits examined vigilance of group members within groups but did not provide comparative records for solitary individuals. Because parids seldom (if ever) are solitary in nature, only a manipulative study can provide records for solitary birds under controlled circumstances. Although dominance-related vigilance within the same species occasionally has been studied in controlled experiments (Waite 1987a, b), the effect of heterospecific group members on vigilance has been

Vigilance in the tufted titmouse varies independently with air temperature and conspecific group size

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Management of fat reserves in tufted titmice (Parus bicolor ): evidence against a trade-off with food hoards

Abstract Caching species can manage their energy supply by adjusting body fat, number of caches, or both. It has been hypothesized that because body fat has a higher fitness cost than caches, small food-hoarding birds respond to increased starvation risk by increasing the number of their caches rather than their fat load. This hypothesis predicts that when birds cannot cache they should compensate for the loss of external energy storage by (1) shifting the time of their daily body mass accumulation toward earlier in the day and (2) increasing the overall level of their fat reserves. During the winter of 1995–1996, we tested these predictions with a caching species, the tufted titmouse (Parus bicolor). Each of six experimental birds was fed a diet of uncachable sunflower seed powder for 6 days, preceded and followed by 6-day control periods during which they were fed cachable sunflower seeds. The daily pattern of body mass gain was unaffected by the opportunity to cache. Furthermore, when unable to cache, the birds did not increase either their mean daily body mass, body mass in the middle of the day, or evening body mass compared to the two control periods. These results argue against the hypothesis of a trade-off between fat reserves and food caches in tufted titmice, and suggest that fat reserves are managed independently of external food caches.

No latitudinal differences in adrenocortical stress response in wintering black-capped chickadees (Poecile atricapilla).

Birds respond to deterioration in environmental conditions by elevating their corticosterone levels, which can enhance their survival. It is less clear if animals constantly living in energetically challenging environment show similar increases in adrenocortical function. Previous work has demonstrated that under controlled conditions black-capped chickadees (Poecile atricapilla) from northern latitudes cache more food and perform better on spatial memory tasks than their southern conspecifics. As elevated levels of corticosterone have been shown previously to correlate with spatial memory performance in chickadees, this study aimed to investigate whether black-capped chickadees from northern latitudes have elevated baseline levels of corticosterone and/or a stronger adrenocortical stress response than their southern conspecifics, irrespective of their immediate environment. We found no differences between Alaskan and Colorado chickadees maintained under identical conditions for 3 months in either baseline levels of corticosterone or maximum levels of corticosterone achieved during the stress response. Baseline corticosterone levels were negatively correlated with relative body mass across both groups of birds. Our results suggest that the population differences in food catching behavior and spatial memory were not related to differences in corticosterone levels. We conclude that many reported population differences in baseline levels and in strength of adrenocortical stress response may often reflect differences in local environmental conditions rather than population-specific physiological traits.

Body mass, ambient temperature, time of day, and vigilance in tufted titmice

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