Black-capped Chickadees Research Articles

Chickadees sing different songs in sympatry versus allopatry.

Character displacement theory predicts that closely-related co-occurring species should diverge in relevant traits to reduce costly interspecific interactions such as competition or hybridization. While many studies document character shifts in sympatry, few provide corresponding evidence that these shifts are driven by the costs of co-occurrence. Black-capped (Poecile atricapillus) and mountain chickadees (P. gambeli) are closely-related, ecologically similar, and broadly distributed songbirds with both allopatric and sympatric populations. In sympatry, both species appear to suffer costs of their co-occurrence: 1) both species are in worse body condition compared to allopatry and 2) hybridization sometimes yields sterile offspring. Here, we explored character displacement in the songs of black-capped and mountain chickadees by characterizing variation in male songs from sympatric and allopatric populations. We found that mountain chickadees sing differently in sympatry versus allopatry. Specifically, they produced more notes per song, were more likely to include an extra introductory note, and produced a smaller glissando in their first notes compared to all other populations. Combined with previous research on social dominance and maladaptive hybridization between black-capped and mountain chickadees, we posit that differences in sympatric mountain chickadee song are population-wide shifts to reduce aggression from dominant black-capped chickadees and/or prevent maladaptive hybridization.

Age, sex, and temperature shape off-territory feeder use in black-capped chickadees.

Spatial ecology tends to focus on average movement patterns within animal groups; however, recent studies highlight the value of considering movement decisions both within and among individuals. We used a marked population of black-capped chickadees (Poecile atricapillus), to assess the causes and consequences of within- and among-individual differences in chickadee space use. Individuals that used feeders in addition to their most-visited "core feeder" were defined as engaging in off-territory feederuse. We found that females were more likely than males to visit off-territory feeders as ambient temperatures decrease and energetic demands increase. This may be due to sex-related differences in dominance, where males which are the dominant sex in chickadees, have priority access to feeders, while females must increase their foraging areas to meet higher energetic demand. We also found that independent of temperature, adult males were less likely than juvenile males and both juvenile and adult females to forage off-territory. We suggest that this may be due to age-specific benefits of space use in males, where un-paired juvenile males may increase feeder exploration to gain information about potential mates. Finally, we found that chickadees that had a higher propensity to visit off-territory feeders were less likely to survive to the next fall. Overall, our results suggest that dominance hierarchies and individual energetics impact within- and among-individual variation in off-territory feeder use. We provide suggestions for future studies to further investigate fitness-related consequences of within- and among-individual variation in space use.

Gene expression variation in geographically diverse populations of two North American songbird species

The range distributions of many bird species cover extensive geographic distances, exposing each local population to unique ecological challenges. Understanding the molecular basis of how species adapt to diverse habitats across their geographic range is crucial for identifying populations at risk and implementing effective conservation strategies. In this study, we employed two passerine species, the black-capped chickadee (Poecile atricapillus) and the American goldfinch (Spinus tristis), which are widely distributed across North America. This study focused on examining changes in gene expression within their distinct populations inhabiting diverse habitats across various geographical locations. A comparative transcriptomic study was conducted on wild-caught birds from two geographically separate locations, Boston, Massachusetts, and Kent, Ohio, characterized by considerable annual variability in winter severity. We tested the hypothesis that populations of both species in Kent and Boston would show differential gene expression patterns in their brains in response to unique local environmental conditions. Analyzing the differentially expressed genes (DEGs) in black-capped chickadees revealed associations with neural processes such as the generation and maintenance of neurons, activity-dependent plasticity, and cognitive ability. Many of these genes were linked to brain variation in chickadee populations related to spatial cognition associated with food caching. We also compared changes in gene expression levels with coding sequence variability to explore the underlying basis of differential gene expression patterns. We tested the hypothesis that expression differences are driven by underlying genetic variation. A population genetic analysis on transcriptome data from both species revealed no highly divergent genetic variants (single nucleotide polymorphisms or SNPs) in the coding regions of genes identified as differentially expressed. However, some of the DEGs themselves were transcription factors or regulatory molecules, as were some of the genes with highly divergent SNPs. These findings suggest that the genetic architecture underlying the differential gene expression patterns is mostly regulatory rather than protein-coding changes.

Vernal growth of vocal control nucleus Area X, but not HVC, precedes gonadal recrudescence in wild black-capped chickadees (Poecile atricapillus).

In temperate-zone songbirds, the neuroanatomical changes which occur in advance of breeding, including the growth of nuclei of the vocal control system, are believed to occur downstream of gonadal recrudescence. However, evidence from wild birds is mixed. Here, we captured black-capped chickadees from the wild in early spring (March-April), summer (August-September), and winter (December-January); in addition to measuring the volumes of two vocal control nuclei (Area X and HVC), we also quantified two indicators of reproductive state (gonads and circulating gonadal steroids). Most birds captured in early spring had regressed gonads and low levels of circulating gonadal steroids, indicating these birds were not yet in full breeding condition. However, these early spring birds still had a significantly larger Area X than winter birds, while HVC did not differ in size across groups. Using data from a previously published seasonal study of black-capped chickadees (Phillmore et al., Developmental Neurobiology, 2015;75:203-216), we then compared Area X and HVC volumes from our early spring group to a breeding group of chickadees captured 3-4 weeks later in the spring. While Area X volume did not differ between the studies, breeding males in Phillmore et al. (2015) had a significantly larger HVC. Taken together, this suggests that the vernal growth of Area X occurs ahead of HVC in black-capped chickadees, and that the overall vernal changes in the vocal control system occur at least partially in advance of the breeding-associated upregulation of the hypothalamic-pituitary-gonadal axis.

Effects of ghrelin on food caching behaviour and body composition in black-capped chickadees (Poecile atricapillus)

Several metabolic hormones signal an organism’s energy balance to the brain and modulate feeding behaviours accordingly. These metabolic signals may also regulate other behaviour related to energy balance, such as food caching or hoarding. Ghrelin is one such hormone, but it appears to exert different effects on appetite and fat levels in birds and mammals. Ghrelin treatment inhibits food intake and decreases fat stores in some bird species, but these effects may differ between acylated and unacylated (des-acyl) forms of ghrelin. The effect of ghrelin on food caching in birds has been examined in only one study, that found both leptin and unacylated ghrelin reduced food caching and mass gain in coal tits (Periparus ater). We expanded on this to test how both forms of ghrelin affect food caching and body composition in black-capped chickadees (Poecile atricapillus). We injected each bird with acylated ghrelin, unacylated ghrelin, and a saline control and then measured food caching every 20 min for two hours post-injection. We also measured body mass fat levels the day before, and after treatment using quantitative magnetic resonance (QMR). Contrary to prior work, we found no effects of either form of ghrelin on food caching, or body or fat mass. Future work is required to determine if the difference between our results and those of the prior study stems from species differences in response to ghrelin and/or in the motivation to cache food, or ghrelin effects being modulated by energy reserves.

RADseq data reveal widespread historical introgression in four familiar North American songbirds.

Population genetic structure is influenced by a combination of contemporary and historical events; however, this structure can be complicated by ongoing gene flow. While it is well known that contemporary hybridization occurs frequently among many closely related species, it often remains uncertain as to which populations are involved in introgression events, and this can be even more difficult to infer when introgression is historical. Here we use restriction-site associated DNA sequencing to look at the level of introgression among four species of songbirds in North America: the black-capped, mountain, boreal, and chestnut-backed chickadee. Samples from both sympatric and allopatric sites across the species' ranges supported limited ongoing mixing among the four species with Bayesian clustering and principal component analyses. In contrast, f4-statistics and admixture graphs revealed extensive historical introgression among geographically structured populations. Almost all historical admixture events were among populations west of the Rocky Mountains, and almost all populations west of the Rocky Mountains, excluding island and coastal populations, showed evidence of historical admixture. The inclusion of all four chickadee species proved crucial in differentiating which species were involved in hybridization events to avoid erroneous conclusions. Taken together, the results suggest a complex pattern of divergence with gene flow.

Functional neurogenomic responses to acoustic threats, including a heterospecific referential alarm call and its referent, in the auditory forebrain of red-winged blackbirds

In animal communication, functionally referential alarm calls elicit the same behavioral responses as their referents, despite their typically distinct bioacoustic traits. Yet the auditory forebrain in at least one songbird species, the black-capped chickadee Poecile atricapillus, responds similarly to threat calls and their referent predatory owl calls, as assessed by immediate early gene responses in the secondary auditory forebrain nuclei. Whether and where in the brain such perceptual and cognitive equivalence is processed remains to be understood in most other avian systems. Here, we studied the functional neurogenomic (non-) equivalence of acoustic threat stimuli perception by the red-winged blackbird Agelaius phoeniceus in response to the actual calls of the obligate brood parasitic brown-headed cowbird Molothrus ater and the referential anti-parasitic alarm calls of the yellow warbler Setophaga petechia, upon which the blackbird is known to eavesdrop. Using RNA-sequencing from neural tissue in the auditory lobule (primary and secondary auditory nuclei combined), in contrast to previous findings, we found significant differences in the gene expression profiles of both an immediate early gene, ZENK (egr-1), and other song-system relevant gene-products in blackbirds responding to cowbird vs. warbler calls. In turn, direct cues of threats (including conspecific intruder calls and nest-predator calls) elicited higher ZENK and other differential gene expression patterns compared to harmless heterospecific calls. These patterns are consistent with a perceptual non-equivalence in the auditory forebrain of adult male red-winged blackbirds in response to referential calls and the calls of their referents.

Information Gathering Is Associated with Increased Survival: A Field Experiment in Black-Capped Chickadees (Poecile atricapillus).

AbstractSampling, investing time or energy to learn about the environment, allows organisms to track changes in resource distribution and quality. The use of sampling is predicted to change as a function of energy expenditure, food availability, and starvation risk, all of which can vary both within and among individuals. We studied sampling behavior in a field study with black-capped chickadees (Poecile atricapillus) and show that individuals adjust their use of sampling as a function of ambient temperature (a proxy for energy expenditure), the presence of an alternative food source (yes or no, a proxy for risk of energy shortfall), and their interaction, as predicted by models of optimal sampling. We also observed repeatable differences in sampling. Some individuals consistently sampled more, and individuals that sampled more overall also had a higher annual survival. These results are consistent with among-individual differences in resource acquisition (e.g., food caches or dominance-related differences in priority access to feeders), shaping among-individual differences in both sampling and survival, with greater resource acquisition leading to both higher sampling and higher survival. Although this explanation requires explicit testing, it is in line with several recent studies suggesting that variation in resource acquisition is a key mechanism underlying animal personality.

Do standard behavioral assays predict foraging behavior of individual Black-capped chickadees (Poecile atricapillus) in response to a predator model or calls?

Black-capped chickadees (Poecile atricapillus) and other species that feed at bird feeders balance the benefit of easy foraging with the added risk of predation. Individual birds respond differently to risky situations, and these differences have been attributed to the birds' personalities, which researchers commonly assess with an "open-field" behavioral assay. However, these behavioral assays in birds have not been compared to behavior in the wild in the context of foraging in the presence of a predator (i.e., risk-taking behavior). We color-banded chickadees in a wild population and conducted behavioral assays in the field. We later used foraging trials to investigate these color-banded individuals' responses to a predator (Cooper's hawk, Accipiter cooperii) model or a series of Cooper's hawk calls. We found that foraging black-capped chickadees responded more strongly to the presence of a predator model than to predator calls. Individual birds differed in their responses, and the behavioral assays (activity and exploration) predicted individual behavior in the wild during the foraging experiments. Activity and exploration assay scores were only weakly related, suggesting these two assays represent different traits. Both highly active birds and fast explorers exhibited some reluctance to visit the feeder (either reduced number of visits or greater latency to visit) when the predator model was present, a relationship that was somewhat unexpected. Our results suggest that standard behavioral assays predict behavior in the wild, but care should be taken when generalizing among species and studies. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Supplemental Material for Do Standard Behavioral Assays Predict Foraging Behavior of Individual Black-Capped Chickadees (Poecile atricapillus) in Response to a Predator Model or Calls?

Supplemental Material for Do Standard Behavioral Assays Predict Foraging Behavior of Individual Black-Capped Chickadees (Poecile atricapillus) in Response to a Predator Model or Calls?

Thermal acclimation in a non-migratory songbird occurs via changes to thermogenic capacity, but not conductance.

Thermoregulatory performance can be modified through changes in various subordinate traits, but the rate and magnitude of change in these traits is poorly understood. We investigated flexibility in traits that affect thermal balance between black-capped chickadees (Poecile atricapillus) acclimated for six weeks to cold (-5˚C) or control (23˚C) environments (n=7 per treatment). We made repeated measurements of basal and summit metabolic rates via flow-through respirometry and of body composition using quantitative magnetic resonance of live birds. At the end of the acclimation, we measured thermal conductance of the combined feathers and skins. Cold-acclimated birds had a higher summit metabolic rate, reflecting a greater capacity for endogenous heat generation, and an increased lean mass. However, birds did not alter their thermal conductance. These results suggest that chickadees respond to cold stress by increasing their capacity for heat production rather than increasing heat retention, an energetically expensive strategy.

Interspecific differences in the effects of masking and distraction on anti-predator behavior in suburban anthropogenic noise.

Predation is a common threat to animal survival. The detection of predators or anti-predator communication signals can be disrupted by anthropogenic noise; however, the mechanism by which responses are affected is unclear. Masking and distraction are the two hypotheses that have emerged as likely explanations for changes in behavior in noise. Masking occurs when the signal and noise fall within the same sensory domain; noise overlapping the energy in the signal reduces signal detection. Distraction can occur when noise in any sensory domain contributes to a greater cognitive load, thereby reducing signal detection. Here, we used a repeated measures field experiment to determine the relative contributions of masking and distraction in mediating reduced anti-predator responses in noise. We recorded the approaches and vocalizations of black-capped chickadees (Poecile atricapillus), tufted titmice (Baeolophus bicolor), and white-breasted nuthatches (Sitta carolinensis) to both visual and acoustic cues of predator presence, either with or without simultaneous exposure to anthropogenic noise. Titmice increased their calling to both visual and acoustic cues of predator presence. However, there was no significant effect of noise on the calling responses of titmice regardless of stimulus modality. Noise appeared to produce a distraction effect in chickadees; however, this effect was small, suggesting that chickadees may be relatively unaffected by low levels of anthropogenic noise in suburban environments. White-breasted nuthatch calling behavior was affected by the interaction of the modality of the predator stimulus and the noise condition. Nuthatches had a delayed response to the predator presentations, with a greater calling rate following the presentation of the acoustic stimulus in quiet compared to the presentation of the acoustic stimulus in noise. However, there was no difference in calling rate between the quiet and noise conditions for the visual stimulus. Together this suggests that even moderate levels of noise have some masking effect for white-breasted nuthatches. We suggest that the mechanisms through which noise influences anti-predator behavior may depend on the social roles, foraging ecology and auditory capabilities of each species.

Topography of inputs into the hippocampal formation of a food-caching bird.

The mammalian hippocampal formation (HF) is organized into domains associated with different functions. These differences are driven in part by the pattern of input along the hippocampal long axis, such as visual input to the septal hippocampus and amygdalar input to the temporal hippocampus. HF is also organized along the transverse axis, with different patterns of neural activity in the hippocampus and the entorhinal cortex. In some birds, a similar organization has been observed along both of these axes. However, it is not known what role inputs play in this organization. We used retrograde tracing to map inputs into HF of a food-caching bird, the black-capped chickadee. We first compared two locations along the transverse axis: the hippocampus and the dorsolateral hippocampal area (DL), which is analogous to the entorhinal cortex. We found that pallial regions predominantly targeted DL, while some subcortical regions like the lateral hypothalamus (LHy) preferentially targeted the hippocampus. We then examined the hippocampal long axis and found that almost all inputs were topographic along this direction. For example, the anterior hippocampus was preferentially innervated by thalamic regions, while the posterior hippocampus received more amygdalar input. Some of the topographies we found bear a resemblance to those described in the mammalian brain, revealing a remarkable anatomical similarity of phylogenetically distant animals. More generally, our work establishes the pattern of inputs to HF in chickadees. Some of these patterns may be unique to chickadees, laying the groundwork for studying the anatomical basis of these birds' exceptional hippocampal memory.

Traffic noise inhibits inhibitory control in wild-caught songbirds

Anthropogenic noise is ubiquitous across environments and can have negative effects on animals, ranging from physiology to community structure. Recent work with captive-bred zebra finches demonstrated that traffic noise also affects cognitive performance. We examined whether these results extend to animals that have experienced noise in the wild. We collected black-capped chickadees from areas frequently exposed to road traffic noise and tested them on a detour reaching task, a commonly used measure of inhibitory control. Those chickadees exposed to traffic noise playback had much lower performance on the task than control birds, indicating that noise negatively impacts inhibitory control. These data corroborate previous findings in lab-reared zebra finches. Furthermore, these results suggest that prior experience with traffic noise is not sufficient for animals to habituate to noise and overcome its negative effects on cognitive performance. Instead, noise-induced cognitive effects might have broad impacts on animal species living in noise-polluted habitats.

Black-capped chickadees (Poecile atricapillus) discriminate between naturally-ordered and scramble-ordered chick-a-dee calls and individual preference is related to rate of learning

Though many forms of animal communication are not reliant on the order in which components of signals are combined to be effective, there is evidence that order does matter for some communication systems. In the light of differential responding to calls of varying note-order observed in black-capped chickadees in the field, we set out to determine whether chickadees recognize syntactically-ordered and incorrectly-ordered chick-a-dee calls as separate and distinct conceptual categories using both an auditory preference task and go/no-go operant conditioning paradigm. Results show that chickadees spent more time on the perch that did not produce sound (i.e., silent perch) than on either of the acoustic perches (i.e., natural and scrambled order chick-a-dee call playback) and visited the perch associated with naturally-ordered calls more often than the perch associated with scrambled-order calls. Birds in both the True natural- and scrambled-order call groups continued to respond according to the contingencies that they learned in Discrimination training, indicating that black-capped chickadees are capable of perceiving and acting upon the categories of natural- versus scrambled-ordered calls.

An investigation of personality-related recapture bias in black-capped chickadees, Poecile atricapillus

An investigation of personality-related recapture bias in black-capped chickadees, Poecile atricapillus

Diverse data sources and new statistical models offer prospects for improving the predictability of anthropogenic hybridization.

Human disturbance can theoretically influence the rates of hybridization, but few studies have convincingly identified a causal link. Grabenstein et al. (2022) used a genomic and phenotypic study of chickadees to associate hybridization with human disturbance. Additionally, this is consistent with citizen science reports of chickadee hybrids across the range. We highlight the exciting aspects of this work and make suggestions about a role for broad geographic and genomic sampling, and new statistical methods to better connect hybridization outcomes to anthropogenic disturbance in diverse study systems.

Hybridization between closely related songbirds is related to human habitat disturbance.

Human habitat disturbances can promote hybridization between closely related, but typically reproductively isolated, species. We explored whether human habitat disturbances are related to hybridization between two closely related songbirds, black-capped and mountain chickadees, using both genomic and citizen science data sets. First, we genotyped 409 individuals from across both species' ranges using reduced-representation genome sequencing and compared measures of genetic admixture to a composite measure of human landscape disturbance. Then, using eBird observations, we compared human landscape disturbance values for sites where phenotypically diagnosed hybrids were observed to locations where either parental species was observed to determine whether hybrid chickadees are reported in more disturbed areas. We found that hybridization between black-capped and mountain chickadees positively correlates with human habitat disturbances. From genomic data, we found that (1) hybrid index (HI) significantly increased with habitat disturbance, (2) more hybrids were sampled in disturbed habitats, (3) mean HIs were higher in disturbed habitats versus wild habitats, and (4) hybrids were detected in habitats with significantly higher disturbance values than parentals. Using eBird data, we found that both hybrid and black-capped chickadees were significantly more disturbance-associated than mountain chickadees. Surprisingly, we found that nearly every black-capped chickadee we sampled contained some proportion of hybrid ancestry, while we detected very few mountain chickadee backcrosses. Our results highlight that hybridization between black-capped and mountain chickadees is widespread, but initial hybridization is rare (few F1s were detected). We conclude that human habitat disturbances can erode pre-zygotic reproductive barriers between chickadees and that post-zygotic isolation is incomplete. Understanding what becomes of recently hybridizing species following large-scale habitat disturbances is a new, but pressing, consideration for successfully preserving genetic biodiversity in a rapidly changing world.

Limited movement of an avian hybrid zone in relation to regional variation in magnitude of climate change.

Studies of natural hybrid zones can provide documentation of range shifts in response to climate change and identify loci important to reproductive isolation. Using a temporal (36-38 years) comparison of the black-capped (Poecile atricapillus) and Carolina (P. carolinensis) chickadee hybrid zone, we investigated movement of the western portion of the zone (western Missouri) and assessed whether loci and pathways underpinning reproductive isolation were similar to those in the eastern portion of the hybrid zone. Using 92 birds sampled along the hybrid zone transect in 2016 and 68 birds sampled between 1978 and 1980, we generated 11,669 SNPs via ddRADseq. These SNPs were used to assess movement of the hybrid zone through time and to evaluate variation in introgression among loci. We demonstrate that the interface has moved ~5km to the northwest over the last 36-38 years, that is, at only one-fifth the rate at which the eastern portion (e.g., Pennsylvania, Ohio) of the hybrid zone has moved. Temperature trends over the last 38 years reveal that eastern areas have warmed 50% more than western areas in terms of annual mean temperature, possibly providing an explanation for the slower movement of the hybrid zone in Missouri. Our results suggest hybrid zone movement in broadly distributed species, such as chickadees, will vary between areas in response to local differences in the impacts of climate change.

Seed size selection in Black-capped Chickadees (Poecile atricapillus)

Los comportamientos de forrajeo de animales que promueven la eficiencia pueden ser explicados por la teoría del forrajeo óptimo. Investigaciones previas sugieren que factores asociados a la nutrición (ej., contenido de aceites) o tamaño (ej., espesor y peso de las semillas) influyen en los comportamientos de forrajeo del carbonero cabecinegro (Poecile atricapillus). En febrero y marzo del 2020 examinamos la selección de semillas del carbonero cabecinegro. Específicamente, colectamos semillas de girasol de aceite negro descartadas de un comedero de tubo para aves por el carbonero cabecinegro y las comparamos con semillas seleccionadas al azar del comedero. Medimos el espesor, largo, ancho y peso de 180 semillas de girasol. Encontramos que el tamaño y el peso de las semillas eran factores importantes para los carboneros al seleccionar las semillas. Además, los carboneros prefirieron semillas que eran significativamente más pesadas al ajustar las medidas por tamaño de semilla. Estos hallazgos sugieren que los carboneros cabecinegros seleccionan las semillas con base en el tamaño y el peso para maximizar el contenido nutricional que ingieren. Los carboneros deben entonces poder distinguir pequeñas diferencias de peso de las semillas, lo que podría maximizar su energía adquirida y a la vez disminuiría los riesgos de depredación a los que se someten los individuos durante el forrajeo. Palabras clave: aceite negro, comedero de aves, forrajeo óptimo, semilla de girasol.