Seasonal variation in avian auditory evoked responses to tones: a comparative analysis of Carolina chickadees,tufted titmice,and white-breasted nuthatches

We tested for seasonal plasticity of the peripheral auditory system of three North American members of the Sylvioidea: Carolina chickadees (Poecile carolinensis), tufted titmice (Baeolophus bicolor), and white-breasted nuthatches (Sitta carolinensis). We measured three classes of auditory evoked responses (AER) to tone stimuli: sustained receptor/neural responses to pure-tone condensation waveforms, the frequency-following response (FFR), and the earliest peak of the AER to stimulus onset (tone onset response). Seasonal changes were detected in all classes of AERs in chickadees and nuthatches. Seasonal changes in titmice were restricted to the tone onset response. Interestingly, changes detected in chickadees (and to a lesser extent in titmice) were generally in an opposite direction to changes seen in nuthatches, with chickadees exhibiting greater amplitude AER responses in the spring than in winter, and nuthatches exhibiting greater amplitude AER responses in winter than in spring. In addition, the seasonal differences in the sustained responses tended to be broad-band in the chickadees but restricted to a narrower frequency range in nuthatches. In contrast, seasonal differences in the onset response were over a broader frequency range in titmice than in chickadees and nuthatches. We discuss some possible mechanistic and functional explanations for these seasonal changes.     

Traffic noise and responses to a simulated approaching avian predator in mixed-species flocks of chickadees,titmice, and nuthatches

Traffic noise likely reaches a wide range of species and populations throughout the world, but we still know relatively little about how it affects anti-predator behavior of populations. We tested for possible effects of traffic noise on responses to predator acoustic cues in Carolina chickadees (Poecile carolinensis), tufted titmice (Baeolophus bicolor), and white-breasted nuthatches (Sitta carolinensis) near 14 independent feeding stations in eastern Tennessee. We compared anti-predator calling and seed-taking behavior in response to playbacks of predator stimuli (screech owl calls) at sites naturally exposed to traffic noise and at sites that faced relatively little traffic noise. The screech owl call playback was designed to simulate the approach of this dangerous predator to a feeder being used by these small songbirds. We found that chickadees responded consistently to the owl stimuli across different levels of traffic noise. However, titmice, and nuthatches exhibited different behavioral responses to the predator stimulus, suggesting that traffic noise masked these low-frequency predator calls. Overall, chickadees and nuthatches showed the broadest anti-predator behavioral responses in comparison to titmice, corroborating earlier published work with an Indiana population. Finally, populations exposed to traffic noise overall seemed less able to detect predator cues potentially masked by that noise, and future work will need to assess likely seasonal variation in these responses as well as species-level variation in anti-predator responses in mixed-species groups.     

A comparative study of avian auditory brainstem responses: correlations with phylogeny and vocal complexity, and seasonal effects

We conducted a comparative study of the peripheral auditory system in six avian species (downy woodpeckers, Carolina chickadees, tufted titmice, white-breasted nuthatches, house sparrows, and European starlings). These species differ in the complexity and frequency characteristics of their vocal repertoires. Physiological measures of hearing were collected on anesthetized birds using the auditory brainstem response to broadband click stimuli. If auditory brainstem response patterns are phylogenetically conserved, we predicted woodpeckers, sparrows, and starlings to be outliers relative to the other species, because woodpeckers are in a different Order (Piciformes) and, within the Order Passeriformes, sparrows and starlings are in different Superfamilies than the nuthatches, chickadees, and titmice. However, nuthatches and woodpeckers have the simplest vocal repertoires at the lowest frequencies of these six species. If auditory brainstem responses correlate with vocal complexity, therefore, we would predict nuthatches and woodpeckers to be outliers relative to the other four species. Our results indicate that auditory brainstem responses measures in the spring broadly correlated with both vocal complexity and, in some cases, phylogeny. However, these auditory brainstem response patterns shift from spring to winter due to species-specific seasonal changes. These seasonal changes suggest plasticity at the auditory periphery in adult birds.     

Interspecific differences in the visual system and scanning behavior of three forest passerines that form heterospecific flocks

Little is known as to how visual systems and visual behaviors vary within guilds in which species share the same micro-habitat types but use different foraging tactics. We studied different dimensions of the visual system and scanning behavior of Carolina chickadees, tufted titmice, and white-breasted nuthatches, which are tree foragers that form heterospecific flocks during the winter. All species had centro-temporally located foveae that project into the frontal part of the lateral visual field. Visual acuity was the highest in nuthatches, intermediate in titmice, and the lowest in chickadees. Chickadees and titmice had relatively wide binocular fields with a high degree of eye movement right above their short bills probably to converge their eyes while searching for food. Nuthatches had narrower binocular fields with a high degree of eye movement below their bills probably to orient the fovea toward the trunk while searching for food. Chickadees and titmice had higher scanning (e.g., head movement) rates than nuthatches probably due to their wider blind areas that limit visual coverage. The visual systems of these three species seem tuned to the visual challenges posed by the different foraging and scanning strategies that facilitate the partitioning of resources within this guild.     

Social context affects risk taking by a satellite species in a mixed-species foraging group

Mixed-species flocks of birds form during winter in the easterndeciduous forests of North America. These flocks consist oftwo flock-leading nuclear species, tufted titmouse (Baeolophusbicolor) and Carolina chickadee (Poecile carolinensis), andseveral follower, or satellite, species, including downy woodpecker(Picoides pubescens) and white-breasted nuthatch (Sitta carolinensis).Hypotheses explaining the adaptiveness of participation in suchmixed-species foraging groups have focused on increased foragingsuccess and/or decreased predation risk. We tested the predictionthat if nuthatches join nuclear species to reduce predationrisk, they should be more reluctant to visit an exposed feederin the absence of titmice than in their presence. When the feederwas positioned 16 m from forest cover, latency to visit thefeeder was greater for both male and female nuthatches whentitmice were absent. Removal of titmice had no effect on latencyat 8 m. In the absence of titmice, nuthatches visited the feederless frequently at both distances. These results indicate thatreduced predation risk is a benefit that satellite species gainby flocking with nuclear species.     

Chick-a-dee call variation in Carolina chickadees and recruiting flockmates to food

The "chick-a-dee" call of many Paridae species (titmice, tits,and chickadees) is structurally complex and functions in socialcohesion. Studies with different Parid species suggest thatvariation in the note composition of calls relates to a widevariety of contexts. An earlier study with Carolina chickadees(Poecile carolinensis), the focal species of the present study,found that receivers responded differently to playback callsdiffering in note composition in feeding contexts. Here, weaddressed whether signalers actually produce calls differingin note composition in feeding contexts and whether those callsmight serve a recruitment function. In a first study, we foundthat the first chickadee to take seed from a feeding stationproduced calls with a greater number of D notes before the secondchickadee arrived to take seed, compared with after the secondchickadee arrived to take seed. This suggests that calls witha large number of D notes might serve a general recruitmentfunction. We tested this idea in a second study, using playbacksof calls containing a large number of D notes or a small numberof D notes at different sites. We found that the latency fora first chickadee to come into a site and take seed was shorterfor playback variants containing a large number of D notes.Thus, in Carolina chickadees, chick-a-dee calls containing alarge number of D notes may function to recruit other flockmembers to a discovered food source.     

Differential Response to Interspecific and Intraspecific Signals Amongst Chickadees

Black‐capped chickadees (Poecile atricapillus) and mountain chickadees (P. gambeli) have a similar vocal repertoire and share many other life history traits; yet, black‐capped chickadees are socially dominant to mountain chickadees where populations overlap. Previous research suggested that in contact zones, both species respond weakly to heterospecific songs during the breeding season, and have suggested minimal interspecific competition. However, both black‐capped and mountain chickadees discriminate between conspecific and heterospecific chick‐a‐dee calls, suggesting attention is paid to interspecific signals. We compared the responses of both black‐capped and mountain chickadees to conspecific and heterospecific chick‐a‐dee calls during the winter, when both species compete for the same food resources. We conducted an aviary playback experiment exposing both species to playback composed of heterospecific and conspecific chick‐a‐dee calls, which had been recorded in the context of finding food sources. Responses from the tested birds were measured by recording vocalizations and behaviour. Black‐capped chickadees responded significantly more to conspecific than to heterospecific stimuli, whereas the subordinate mountain chickadees responded to both mountain and black‐capped chickadee calls. Based upon the reactions to playbacks, our results suggest these two closely related species may differ in their perception of the relative threat associated with intra‐ versus interspecific competitors.     

Phenotypic flexibility in passerine birds: Seasonal variation of aerobic enzyme activities in skeletal muscle

Improved winter cold tolerance is widespread among small passerines resident in cold climates and is generally associated with elevated summit metabolic rate (M_sum=maximum thermoregulatory metabolic rate) and improved shivering endurance with increased reliance on lipids as fuel. Elevated M_sum and improved cold tolerance may result from greater metabolic intensity, due to mass-specific increase in oxidative enzyme capacity, or increase in the masses of thermogenic tissues. To examine the mechanisms underlying winter increases in M_sum, we investigated seasonal changes in mass-specific and total activities of the key aerobic enzymes citrate synthase (CS) and β-hydroxyacyl CoA-dehydrogenase (HOAD) in pectoralis, supracoracoideus and mixed leg muscles of three resident passerine species, black-capped chickadee (Poecile atricapillus), house sparrow (Passer domesticus), and white-breasted nuthatch (Sitta carolinensis). Activities of CS were generally higher in winter than in summer muscles for chickadees and house sparrows, but not nuthatches. Mass-specific HOAD activity was significantly elevated in winter relative to summer in all muscles for chickadees, but did not vary significantly with season for sparrows or nuthatches, except for sparrow leg muscle. These results suggest that modulation of substrate flux and cellular aerobic capacity in muscle contribute to seasonal metabolic flexibility in some species and tissues, but such changes play varying roles among small passerines resident in cold climates.     

Call-based species recognition in black-capped chickadees

Species recognition is essential for efficient communication between conspecifics. For this to occur, species information must be unambiguously encoded in the repertoire of each species’ vocalizations. Until now, the study of species recognition in songbirds has been focused mainly on male songs and male territorial behaviour. Species recognition of other learned vocalizations, such as calls, have not been explored, and could prove useful as calls are used in a wider range of contexts. Here, we present an experimental field study investigating the coding of species information in a learned vocalization, the ‘chick-a-dee’ call of the black-capped chickadee (Poecile atricapillus). By modifying natural calls in both temporal and spectral domains and by observing the vocal responses of black-capped chickadees following the playback of these modified calls, we demonstrate that species recognition in chickadees relies on several acoustic features including syntax, frequency modulation, amplitude modulation, and to a lesser extent, call rhythmicity and frequency range.     

Songbirds tradeoff auditory frequency resolution and temporal resolution

Physical tradeoffs may in some cases constrain the evolution of sensory systems. The peripheral auditory system, for example, performs a spectral decomposition of sound that should result in a tradeoff between frequency resolution and temporal resolution. We assessed temporal resolution in three songbird species using auditory brainstem responses to paired click stimuli. Temporal resolution was greater in house sparrows (Passer domesticus) than Carolina chickadees (Poecile carolinensis) and white-breasted nuthatches (Sitta carolinensis), as predicted based on previous observations of broader auditory filters (lower frequency resolution) in house sparrows. Furthermore, within chickadees, individuals with broader auditory filters had greater temporal resolution. In contrast to predictions however, temporal resolution was similar between chickadees and nuthatches despite broader auditory filters in chickadees. These results and the results of a model simulation exploring the effect of broadened auditory filter bandwidth on temporal resolution in the auditory periphery strongly suggest that frequency resolution constrains temporal resolution in songbirds. Furthermore, our results suggest that songbirds have greater temporal resolution than some mammals, in agreement with recent behavioral studies. Species differences in temporal resolution may reflect adaptations for efficient processing of species-specific vocalizations, while individual differences within species may reflect experience-based developmental plasticity or hormonal effects.     

Winter dialects in the bronzed cowbird and their relationship to breeding-season dialects

Studies of geographical variation in animal signals generally focus on breeding-season behaviour but, in many species, signalling persists throughout the year. In passerine birds, patterns of variation in the nonbreeding season might provide opportunities for vocal learning that have been neglected by a historic focus on breeding-season behaviour. This study provides the first example of dialect variation outside of the breeding season. Quantitative analysis of acoustic similarity showed discrete differences between the songs of bronzed cowbirds, Molothrus aeneus, in four winter flocks. Most songs produced by members of a given flock were classified as belonging to the same dialect. Songs from one of the four winter dialects were indistinguishable from songs recorded in the breeding season in the same region. Depending on migratory patterns, dialects in one season may be a consequence of dialects in the other season, or the two seasonal patterns may be the result of independent social or evolutionary forces. Because the nonbreeding season is an important period of vocal learning in some bird species, winter dialects might limit the range of signals available for individuals to learn to produce. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Reproductive isolation and cryptic introgression in a sky island enclave of Appalachian birds

Reproductive isolation is central to the speciation process, and cases where the strength of reproductive isolation varies geographically can inform our understanding of speciation mechanisms. Although generally treated as separate species, Black‐capped chickadees (Poecile atricapillus) and Carolina chickadees (P. carolinensis) hybridize and undergo genetic introgression in many areas where they come into contact across the eastern United States and in the northern Appalachian Mountains. The Great Smoky Mountains harbor the last large breeding population of atricapillus in the southern Appalachians, isolated from the species’ main range by nearly 200 km. This population is believed to be reproductively isolated from local carolinensis due to an unusual, behaviorally mediated elevational range gap, which forms during the breeding season and may function as an incipient reproductive isolating mechanism. We examined the effectiveness of this putative isolating mechanism by looking for genetic introgression from carolinensis in Great Smoky Mountain atricapillus. We characterized this population and parental controls genetically using hundreds of amplified fragment length polymorphism (AFLP) loci as well as mitochondrial DNA (mtDNA) sequence data from cytochrome‐b. Great Smoky Mountain atricapillus have experienced nuclear genetic introgression from carolinensis, but at much lower levels than other populations near the hybrid zone to the north. No mitochondrial introgression was detected, in contrast to northern contact areas. Thus, the seasonal elevational range gap appears to have been effective in reducing gene flow between these closely related taxa.     

Seasonal metabolic acclimatization in mountain chickadees and juniper titmice

Mountain chickadees and juniper titmice from northern Utah were examined to determine metabolic and body-composition characteristics associated with seasonal acclimatization. These species use behavioral adaptations and nocturnal hypothermia, which reduce energetic costs. These adjustments could reduce the need for extensive metabolic adjustments typically found in small passerines that overwinter in cold regions. In addition, these species live at higher altitudes, which may also decrease metabolic acclimatization found in birds. Winter birds tolerated colder test temperatures than summer birds. This improved cold tolerance was associated with an increase in maximal thermogenic capacity or summit metabolism (M(sum)). Winter M(sum) exceeded summer M(sum) by 26.1% in chickadees and 16.2% in titmice. Basal metabolic rates (BMR) were also significantly higher in winter birds compared with summer birds. Pectoralis wet muscle mass increased 33.3% in chickadees and 24.1% in titmice in winter and paralleled the increased M(sum) and BMR. Dry mass of contour plumage increased in winter for both species and was associated with decreased thermal conductance in winter chickadees compared to summer chickadees. Chickadees and titmice show metabolic acclimatization similar to other temperate species.     

Humpback whale songs during winter in subarctic waters

The songs of the male humpback whales (Megaptera novaeangliae) have traditionally been associated with mating at tropical and subtropical mating grounds during winter. However, songs also occur out of mating season, both on feeding grounds in spring, late summer and fall. This study provides the first report of humpback whale singing behaviour in the subarctic waters of Northeast Iceland (Skjálfandi Bay) using long-term bottom-moored acoustic recorders during September 2008–February 2009 and from April to September 2009. Singing started in late November and peaked in February, within the breeding season. No songs were detected from spring to fall, despite visual detections of humpback whales. Non-song sound signals from humpback whales were detected during all recording months. Songs were partly composed of fundamental units common with other known mating grounds, and partly of song units likely unique to the study area. The variety of song unit types in the songs increased at the end of the winter recordings, indicating a gradual change in the songs throughout the winter season; as has been shown on traditional mating grounds. The relative proportion of songs compared with non-song signals was higher during dark hours than daylight hours. The short light periods of the winter, and where food is available, likely influence the daily occurrence of humpback whales’ songs in the subarctic.     

Impact of season and social challenge on testosterone and corticosterone levels in a year-round territorial bird

Plasma testosterone increases during breeding in many male vertebrates and has long been implicated in the promotion of aggressive behaviors relating to territory and mate defense. Males of some species also defend territories outside of the breeding period. For example, the European nuthatch (Sitta europaea) defends an all-purpose territory throughout the year. To contribute to the growing literature regarding the hormonal correlates of non-breeding territoriality, we investigated the seasonal testosterone and corticosterone profile of male (and female) nuthatches and determined how observed hormone patterns relate to expression of territorial aggression. Given that non-breeding territoriality in the nuthatch relates to the reproductive context (i.e., defense of a future breeding site), we predicted that males would exhibit surges in plasma testosterone throughout the year. However, we found that males showed elevated testosterone levels only during breeding. Thus, testosterone of gonadal origin does not appear to be involved in the expression of non-breeding territoriality. Interestingly, territorial behaviors of male nuthatches were stronger in spring than in autumn, suggesting that in year-round territorial species, breeding-related testosterone elevations may upregulate male-male aggression above non-breeding levels. In females, plasma testosterone was largely undetectable. We also examined effects of simulated territorial intrusions (STIs) on testosterone and corticosterone levels of breeding males. We found that STIs did not elicit a testosterone response, but caused a dramatic increase in plasma corticosterone. These data support the hypothesis that corticosterone rather than testosterone may play a role in the support of behavior and/or physiology during acute territorial encounters in single-brooded species.     

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.     

Variation in chick‐a‐dee calls of bridled titmice (Baeolophus wollweberi): Frequent use of non‐combinatorial calls in a combinatorial calling system

Chick‐a‐dee calls of Poecile (chickadee) and Baeolophus (titmouse) species are complex in terms of the structural composition of note types and the diversity of messages. Studies so far have mainly focused on the calls of various chickadee and just one titmouse species—the tufted titmouse (B. bicolor). To begin to address this lack of titmouse data, our study investigated variation in note composition of calls of bridled titmice (B. wollweberi). We obtained calls from 26 flocks in the Chiricahua Mountains of Arizona in the overwintering flocking period. Bridled titmice produce proportionally more non‐combinatorial call variants than combinatorial call variants. The number of the single noted calls furthermore exceeded the number of multinote calls. In general, structural variation in the combinatorial calls appears to be comparable to calls of better‐studied chickadees and of tufted titmice, although bridled titmice appear to have a unique call length distribution. We also analyzed some behavioral associations with call variation and found that flight behavior and close interactions between individuals were associated with use of specific note types. Finally, we found microgeographic variation in note type use in these calls. We discuss some possible explanations for call complexity in this species.     

Seasonal variation of vocal behaviour in a temperate songbird: assessing the effects of laboratory housing on wild-caught, seasonally breeding birds

Many laboratories are conducting research using songbirds as their animal model. In particular, songbirds are widely used for studying the behavioural and neural mechanisms underlying vocal learning. Many researchers use wild-caught birds to conduct this research, although few studies of behaviour have been conducted to determine the effects of captive housing on these species. We investigated the vocal production pattern of wild-caught black-capped chickadees (Poecile atricapillus) over an entire season in laboratory housing. We documented the frequency of production of four vocalizations (fee-bee song, chick-a-dee calls, dee calls, and gargle calls) across seasons and diurnal pattern and compared the observed pattern of laboratory vocalizations to those previously observed and reported in the wild. Laboratory-housed chickadees had seasonal and diurnal vocal production shifts that were related to both photoperiodic changes (season) and diurnal pattern. For instance, there was significantly more fee-bee song in the spring than summer, autumn, and winter with the most fee-bee song occurring at spring dawn as seen in the wild. Our results also confirmed that the general pattern of vocalizations was consistent between wild and laboratory populations, with no significant differences for either the seasonal or diurnal pattern of fee-bee song production between populations. Differences between settings were observed in the pattern of chick-a-dee calls at dawn and sunset between field and laboratory populations. However, differences in the quantity of vocalization types between laboratory and wild populations suggest that housing conditions are influencing the normal vocal behavioural patterns.     

Mobbing behaviour in a passerine community increases with prevalence in predator diet

Mobbing behaviour against predators is well documented but less is known about the factors influencing variation in behavioural response between prey species. We conducted a series of playback experiments to examine how the mobbing responses of prey species differed according to their relative risk of predation by the Eurasian Pygmy Owl Glaucidium passerinum, a predator of passerines. We found that mobbing among 22 passerine prey species was positively correlated with their prevalence in the Pygmy Owl diet. To compare mobbing behaviour between two seasons, we conducted playback experiments during spring (breeding season) and autumn (non‐breeding season). Contrary to previous studies, we found that mobbing intensity was greater during autumn than in spring. Our study shows a differential mobbing response of 22 species to the calls from one predator species and underscores the importance of considering seasonal variation in mobbing behaviour. Mobbing response differences observed among bird species strongly suggest different cooperation behaviour at the community level.     

The seasonal hippocampus of food-storing birds

Food storing is seasonal in birds like chickadees, nuthatches and jays, occurring at high levels in fall and winter and low levels in spring and summer. Memory for cache sites is hippocampus dependent in chickadees and both the recruitment of new neurons into the hippocampus and the total size of the hippocampus change seasonally. Unlike seasonal change in the vocal control nuclei of songbirds, however, change in the hippocampus appears not to be controlled by photoperiod. The annual timing of hippocampal neuronal recruitment and change in hippocampal size is quite variable, reaching maximum levels at different times of year in different studies. The amount of food-storing activity by chickadees is known to be influenced by flock dominance structure, energy balance, food availability, and other seasonally varying factors. The variable timing of seasonal change in the hippocampus may indicate that the hippocampus of food-storing birds changes annually in response to change in the intensity of food storing behaviour itself.