Sex allocation in black-capped chickadees Poecile atricapilla

Optimal sex allocation for individuals can be predicted from a number of different hypotheses. Fisherian models of sex allocation predict equal investment in males and females up to the end of parental care and predict brood compositions based on the relative costs of producing males and females. The Trivers-Willard hypothesis predicts that individual females should alter the sex ratio of their broods based on their own condition if it has a differential impact on the lifetime reproductive success of their sons and daughters. The Charnov model of sex allocation predicts that females should alter sex allocation based on paternal attributes that may differentially benefit sons versus daughters. Because females are the heterogametic sex in birds, many recent studies have focussed on primary sex ratio biases. In black-capped chickadees Poecile atricapilla , males are larger than females suggesting they may be more costly to raise than females. Female condition affects competitive ability in contests for mates, and thus may be related to variance in fecundity. Females prefer high-ranking males as both social and extrapair partners. These observations suggest that females might vary the sex ratio of their broods based on the predictions of any of the above models. Here, we report on the results of PCR based sex determination of 1093 nestlings in 175 broods sampled from 1992 to 2001. Population-wide, we found a mean brood sex ratio of 0.525±0.016, with no significant deviation from a predicted binomial distribution. We found no effect of clutch size, female condition, hatch date, parental rank or paternity. Our results reject the idea that female black-capped chickadees systematically vary sex allocation in their broods.     

Seasonal acclimatization to extreme climatic conditions by black-capped chickadees (Poecile atricapilla) in interior Alaska (64 degrees N).

Winters in interior Alaska (64 degrees N) are characterized by short photoperiod (5L : 19D) and chronic subfreezing temperatures. To determine if seasonal acclimatization of black-capped chickadees (Poecile atricapilla) at high latitude differs from that of conspecifics at lower latitudes, standard metabolic rates (SMR), metabolic response to low temperature (-30 degrees C), nocturnal hypothermia, body mass, fat reserves, and conductance were measured over two winters and one summer in three groups of seasonally acclimatized birds. Body mass and conductance did not vary with season, although furcular fat levels were higher in winter. Birds used nocturnal hypothermia when exposed to -30 degrees C in summer or winter. Although SMR did not vary seasonally, winter SMRs differed between the two winters of the study. Nocturnal hypothermia in summer and decreased SMR in response to extreme conditions may either reflect plasticity inherent to all populations of black-capped chickadees or may result from individual variation within this northern population.     

Food hoarding behaviour of black-capped chickadees (Poecile atricapillus ) in relation to forest edges

In temperate forests, small birds avoid the use of forest edges in adverse winter weather suggesting high foraging costs in terms of energetic requirements. Since hoarding species will often retrieve caches during adverse winter weather, they may perceive forest edges, especially exposed ones, as low quality hoarding sites. We tested whether black-capped chickadees ( Poecile atricapillus) inhabiting fragmented forests modify and reduce hoarding activity near forest edges. We also tested whether hoarding behaviour will be most affected in sites with forest edges more exposed to extreme weather. Black-capped chickadees taking food from a feeder 30 m from the nearest forest edges hoarded items mostly towards the forest interior, whereas no preference in hoarding location was observed with birds taking food from a feeder placed >100 m from the edge. Furthermore, birds avoided direct flights towards forest edges and, at sites exposed to prevailing winds, hoarding trips were shorter than at other locations. These results suggest that individuals avoid hoarding near forest edges and there, they lower their investment in terms of hoarding effort. The observed difference in hoarding behaviour was more evident near forest edges delimiting wide unforested areas than in edges delimiting narrower unforested areas. Edge exposure to prevailing winds influenced hoarding behaviour much less. We suggest that hoarding birds may partially overcome the ecological costs of habitat loss and fragmentation due to abiotic edge effects. By hoarding food away from forest edges in good weather, they may use forest interiors as low-cost retrieval sites under adverse weather.     

Frequency sensitivity in the auditory periphery of male and female black-capped chickadees (Poecile atricapillus)

The black-capped chickadee is a songbird that has been used extensively as a model of animal communication in field and laboratory settings. Although many studies have focused on the complex call and song systems of the black-capped chickadee, relatively fewer studies have focused on chickadee audition. However, we do know from behavioral and molecular work that chickadees (and auditory processing areas in their brains) discriminate between artificially generated tones, between conspecific and heterospecific vocalizations, and among different types of conspecific vocalizations. In this paper we investigate peripheral auditory processing of frequency in the black-capped chickadee and the potential influence of sex on frequency sensitivity using a technique called auditory evoked potentials. We found that male and female black-capped chickadees did not differ in any measure of frequency sensitivity. Both sexes had the greatest sensitivity to frequencies between 2 and 4 kHz. This range of frequencies is well represented in black-capped chickadee song, partially supporting the idea that sender and receiver coevolve. Finally, we suggest that the call and song system of North American parids make them an ideal taxonomic group for comparative work exploring the relationship between call systems and the evolution of auditory processing.     

Evidence of accelerated beak growth associated with avian keratin disorder in black-capped chickadees (Poecile atricapillus)

We recently documented an epizootic of beak deformities in more than 2,000 Blackcapped Chickadees (Poecile atricapillus) and other wild bird species in North America. This emerging avian disease, which has been termed avian keratin disorder, results in gross overgrowth of the rhamphotheca, the outer, keratinized layer of the beak. To test the hypothesis that the beak deformities characteristic of this disorder are associated with accelerated keratin production, we measured rates of beak growth and wear in affected Black-capped Chickadees (n=16) and a control sample of unaffected chickadees (n=14) collected from south-central (61°09'-61°38'N, 149°11' -149°48'W) and interior Alaska (64°51' -64°53'N, 147°49' -147°59'W). Rates of absolute growth were 50-100% higher in affected birds than they were in control birds and exceeded records from other passerine species. These results suggest that abnormally rapid epidermal growth is the primary physical mechanism by which beak deformities develop and are maintained in affected chickadees. Although beak overgrowth typically worsened over time, differential patterns of wear influenced the severity and morphology of deformities. In some cases, the effects of accelerated keratin growth were partially mitigated by frequent breakage of rhamphothecal tips. However, mortalities occurred in 9 of 16 birds (56%) with beak deformities during the study, suggesting that avian keratin disorder results in severe health consequences for affected birds. Additional study of factors that control beak keratin production is needed to understand the pathogenesis of this debilitating disease in wild birds.     

No effect of social group composition or size on hippocampal formation morphology and neurogenesis in mountain chickadees (Poecile gambeli)

Brain plasticity and adult neurogenesis may play a role in many ecologically important processes including mate recognition, song learning and production, and spatial memory processing. In a number of species, both physical and social environments appear to influence attributes (e.g., volume, neuron number, and neurogenesis) of particular brain regions. The hippocampus in particular is well known to be especially sensitive to such changes. Although social grouping in many taxa includes the formation of male and female pairs, most studies of the relationship between social environment and the hippocampus have typically considered only solitary animals and those living in same‐sex groups. Thus, the aim of this study was to compare the volume of the hippocampal formation, the total number of hippocampal neurons, and the number of immature neurons in the hippocampus (as determined by doublecortin expression) in mountain chickadees (Poecile gambeli) housed in groups of males and females, male–female pairs, same sex pairs of either males or females, and as solitary individuals. The different groups were visually and physically, but not acoustically, isolated from each other. We found no significant differences between any of our groups in hippocampal volume, the total number of hippocampal neurons, or the number of immature neurons. Our results thus provided no support to the hypothesis that social group composition and/or size have an effect on hippocampal morphology and neurogenesis. © 2010 Wiley Periodicals, Inc. Develop Neurobiol 70:538–547, 2010     

Seasonal and diurnal patterns of black-capped chickadee (Poecile atricapillus) vocal production

Changes in vocal behaviour observed in temperate songbirds have been linked to changes in photoperiod. Research has focused on the fluctuation of hormones that lead to photosensitivity, photostimulation and photorefractoriness, as well as the 'dawn chorus' observed in numerous species. However, photoperiod in the natural environment is a complex event that occurs as seasons change. To determine the natural relationships between photoperiod and vocal behaviour we sampled vocal production of black-capped chickadees for three major vocal classes over one year at dawn, meridian and sunset. Fee-bee song production increased twice, once in the winter and once in the spring, and occurred almost exclusively at dawn. Chick-a-dee call production was highest in autumn and winter generally at the meridian. Gargle production did not differ significantly by season; however, the most gargle production occurred during the winter at the meridian.     

Effects of demanding foraging conditions on cache retrival accuracy in food-caching mountain chickadees (Poecile gambeli)

Birds rely, at least in part, on spatial memory for recovering previously hidden caches but accurate cache recovery may be more critical for birds that forage in harsh conditions where the food supply is limited and unpredictable. Failure to find caches in these conditions may potentially result in death from starvation. In order to test this hypothesis we compared the cache recovery behaviour of 24 wild-caught mountain chickadees (Poecile gambeli), half of which were maintained on a limited and unpredictable food supply while the rest were maintained on an ad libitum food supply for 60 days. We then tested their cache retrieval accuracy by allowing birds from both groups to cache seeds in the experimental room and recover them 5 hours later. Our results showed that birds maintained on a limited and unpredictable food supply made significantly fewer visits to non-cache sites when recovering their caches compared to birds maintained on ad libitum food. We found the same difference in performance in two versions of a one-trial associative learning task in which the birds had to rely on memory to find previously encountered hidden food. In a non-spatial memory version of the task, in which the baited feeder was clearly marked, there were no significant differences between the two groups. We therefore concluded that the two groups differed in their efficiency at cache retrieval. We suggest that this difference is more likely to be attributable to a difference in memory (encoding or recall) than to a difference in their motivation to search for hidden food, although the possibility of some motivational differences still exists. Overall, our results suggest that demanding foraging conditions favour more accurate cache retrieval in food-caching birds.     

Post-contest behaviour in black-capped chickadees (<Emphasis Type="Italic">Poecile atricapillus</Emphasis>): loser displays,not victory displays,follow asymmetrical countersinging exchanges

Victory displays are behaviours that occur after the conclusion of a signaling contest, performed solely by the contest winner. Victory displays may reinforce the dominance of the winner either to the loser or to other conspecifics within signaling range. Victory displays are poorly studied despite the significant consequences that post-conflict behaviour may have on the individuals involved. We examined the period immediately following 50 territorial countersinging contests between males in 10 neighbourhoods of black-capped chickadees (Poecile atricapillus) of known dominance rank. We characterized the post-contest singing behaviour of chickadees and evaluated whether post-contest behaviour is consistent with victory displays. Using a 16-microphone acoustic location system to simultaneously record entire neighbourhoods of breeding chickadees, we isolated 50 dyadic countersinging contests and measured the vocal behaviour of the contestants in the minutes following each interaction. Eighty-six percent of contests were followed by a period of solo singing by one of the contestants, while 14% were followed by silence. The post-contest singer was most often the contestant who held a subordinate dominance position in the previous winter’s dominance hierarchy; dominant males performed post-contest song bouts significantly less often. Asymmetry in overlapping between contestants did not predict which bird sang a post-contest bout. However, in a significant majority of cases, the post-contest singer was pitch-matched by his opponent during the contest more than he pitch-matched his opponent. Our results indicate that male chickadees do not perform acoustic victory displays after countersinging contests. In contrast, the post-contest behaviour of territorial chickadees is more consistent with a “loser display”.     

Failure to detect seasonal changes in the song system nuclei of the black-capped chickadee (Poecile atricapillus)

Most temperate songbird species sing seasonally, and the brain areas involved in producing song (the song system) vary in size alongside the changes in behavior. Black-capped chickadees (Poecile atricapillus) also sing seasonally, and we find that there are changes in the stereotypy and the length of the fee-bee song from the nonbreeding to the breeding season. Yet despite these changes, we fail to find any evidence of seasonal changes in the song system. The song system of males is larger than that of females, as is typical in songbirds, but the ratio between the sexes is small compared to other species. We suggest three hypotheses to explain our failure to find seasonal variation in the chickadee song system.     

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.     

Foraging and Calling Behavior of Carolina chickadees (Poecile carolinensis) in Response to the Head Orientation of Potential Predators

When animals detect predators they modify their behavior to avoid predation. However, less is known about whether prey species modify their behavior in response to predator body and behavioral cues. Recent studies indicated that tufted titmice, a small songbird, decreased their foraging behavior and increased their calling rates when they detected a potential predator facing toward a feeder they were using, compared to a potential predator facing away from that feeder. Here, we tested whether related Carolina chickadees, Poecile carolinensis, were also sensitive not just to the presence of a predator model, but to its facial/head orientation. Although chickadees are closely related to titmice, recent studies in different populations suggest chickadees respond to risky contexts involving predators differently than titmice. We conducted two field studies near feeders the birds were exploiting. In Study One, a mask‐wearing human observer stood near the feeder. In Study Two, a model of a domestic cat was positioned near the feeder. In both studies, the potential threatening stimulus either faced toward or faced away from the feeder. Chickadees avoided the feeder more in both studies when the potential predator was present, and showed strongest feeder avoidance when the potential predator faced toward the feeder. Chickadee calling behavior was also affected by the facial orientation of the potential predator in Study 1. These results suggest that, like titmice, chickadees exhibit predation‐risk‐sensitive foraging and calling behavior, in relation to facial and head orientation of potential threats. These small birds seem to attend to the likely visual space of potential predators. Sensitivity to predator cues like behavior and body posture must become more central to our theories and models of anti‐predator behavioral systems.     

Exploration of a novel space is associated with individual differences in learning speed in black-capped chickadees, Poecile atricapillus

Individual variation in exploratory behaviour has been demonstrated in a diverse array of animal species. Understanding the evolutionary antecedents and ecological consequences of this variation is an active research area within animal behaviour. Here we investigate whether different exploration styles exhibited by black-capped chickadees (Poecile atricapillus) in a novel environment are related to how quickly these birds learn an acoustic discrimination task. We found that birds that readily enter a novel environment learn an acoustic discrimination task faster than birds that do not readily enter a novel environment. This result contrasts with previous work suggesting no correlation between exploration style and learning a spatial or associative task in great tits (Parus major), a close relative of the black-capped chickadee.     

Differential migration and an endocrine response to stress in wintering dark-eyed juncos (Junco hyemalis)

The dark-eyed junco (junco hyemalis) exhibits differential migration in autumn that, in general, results in females overwintering south of males, and young within each sex overwintering north of older birds. Individuals overwintering at higher latitudes face less predictable and more challenging environmental conditions. Rapid increases in circulating levels of the energy-regulating glucocorticosteroid, corticosterone, occur in response to environmental stressors. To establish whether the strength of acute corticosterone secretion was correlated with the probability of encountering poor environmental conditions, we compared the corticosterone stress response (e.g. initial plasma concentrations at the time of capture and 30 min later) in dark-eyed juncos overwintering in Mississippi (MS), USA, near the southern limit of their wintering range, with juncos overwintering in New York (NY), USA, near the northern limit of their wintering range. During two winters, 22 males and one female were sampled in NY; 13 males, 12 females and one bird of undetermined sex were sampled in MS. Not unexpectedly, NY birds carried greater fat reserves that resulted in a significantly higher value of energetic condition (mass corrected for wing cord cubed). There was no difference between the two winters sampled at either site, nor was there an effect of sex on patterns of corticosterone secretion in MS birds. With sexes pooled, MS and NY birds had similar baseline corticosterone levels. However, as predicted, NY birds exhibited significantly higher corticosterone concentrations 30 min after capture. These results support the hypothesis that birds wintering in less predictable, more extreme environments show a higher amplitude corticosterone response, which may enable them to adjust their behaviour and physiology more rapidly in response to environmental stressors such as storms. Adrenocortical sensitivity may be a part of the physiological milieu associated with differential migration in juncos; whether it results from endogenous differences in the migratory programmes of individuals or from acclimatization to local environmental conditions remains to be determined.     

Prolonged moderate elevation of corticosterone does not affect hippocampal anatomy or cell proliferation rates in mountain chickadees (Poecile gambeli)

Chronic stress and corresponding chronic elevations of glucocorticoid hormones have been widely assumed to have deleterious effects on brain anatomy and functions such as learning and memory. In particular, it has been suggested that chronic elevations of glucocorticoid hormones result in death of hippocampal neurons and in reduced rates of hippocampal neurogenesis. It is not clear, however, if any increase in glucocorticoid levels has negative effects on hippocampal anatomy as many animals regularly maintain moderately elevated levels of glucocrticoids over long periods of time under natural energetically demanding conditions. We used unbiased stereological methods to investigate whether mountain chickadees (Poecile gambeli) implanted for 49 days with continuous time-release corticosterone pellets, designed to approximately double the baseline corticosterone levels, differed from placebo-implanted chickadees in their hippocampal anatomy and cell proliferation rates. We found no significant differences between corticosterone and placebo-implanted birds in either telencephalon volume, volume of the hippocampal formation, or the total number of hippocampal neurons. Cell proliferation rates, measured as the total number of BrdU-labeled cells in the ventricular zone adjacent either to the hippocampus or to the mesopallium, were also not significantly different between corticosterone and placebo-implanted chickadees. Our results suggest that prolonged moderate elevation of corticosterone might not provide the suggested deleterious effects on hippocampal anatomy and neurogenesis in food-caching birds and, as we have shown previously, it actually enhances spatial memory.     

Fecal corticosterone, body mass, and caching rates of Carolina chickadees (Poecile carolinensis) from disturbed and undisturbed sites

We tested for hormonal and behavioral differences between Carolina chickadees (Poecile carolinensis) taken from a disturbed (recently logged) forest, an undisturbed forest, or a residential site. We measured fecal corticosterone and body mass levels in the field, and fecal corticosterone, body mass, and caching behavior in an aviary experiment. In the field, birds from the disturbed forest exhibited significantly higher fecal corticosterone levels than birds from either the undisturbed forest or from the residential site. Birds from the disturbed forest also exhibited lower body mass than those from the undisturbed forest but higher body mass than those from the residential site. Our aviary results suggest that these physiological differences between field sites are the result of short-term responses to ecological factors: neither body mass nor fecal corticosterone levels varied between birds captured at different sites. Aviary sample sizes were sufficient to detect seasonal variation in fecal corticosterone (lowest in summer), body mass (highest in spring), and rate of gain in body mass (highest in winter). Under "closed-economy" aviary conditions (all food available from a feeder in the aviary), there were no site differences in the percent of seeds taken from the feeder that were cached. However, under "open-economy" conditions (food occasionally available ad libitum), significantly fewer seeds were cached by birds from the disturbed forest compared to the undisturbed or residential sites. On average, there was only a two-fold difference in population levels of fecal corticosterone. This difference is about the same as an increase in fecal corticosterone induced by a 2-h increase in food deprivation and cannot be considered to be an acute stress response to disturbance.     

Changes in spatial memory mediated by experimental variation in food supply do not affect hippocampal anatomy in mountain chickadees (Poecile gambeli)

Earlier reports suggested that seasonal variation in food-caching behavior (caching intensity and cache retrieval accuracy) might correlate with morphological changes in the hippocampal formation, a brain structure thought to play a role in remembering cache locations. We demonstrated that changes in cache retrieval accuracy can also be triggered by experimental variation in food supply: captive mountain chickadees (Poecile gambeli) maintained on limited and unpredictable food supply were more accurate at recovering their caches and performed better on spatial memory tests than birds maintained on ad libitum food. In this study, we investigated whether these two treatment groups also differed in the volume and neuron number of the hippocampal formation. If variation in memory for food caches correlates with hippocampal size, then our birds with enhanced cache recovery and spatial memory performance should have larger hippocampal volumes and total neuron numbers. Contrary to this prediction we found no significant differences in volume or total neuron number of the hippocampal formation between the two treatment groups. Our results therefore indicate that changes in food-caching behavior and spatial memory performance, as mediated by experimental variations in food supply, are not necessarily accompanied by morphological changes in volume or neuron number of the hippocampal formation in fully developed, experienced food-caching birds.