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.     

Seasonal plasticity in auditory processing of the envelope and temporal fine structure of sounds in three songbirds

Songs mediate mate attraction and territorial defence in songbirds during the breeding season. Outside of the breeding season, the avian vocal repertoire often includes calls that function in foraging, antipredator and social behaviours. Songs and calls can differ substantially in their spectral and temporal content. Given seasonal variation in the vocal signals, the sender–receiver matching hypothesis predicts seasonal changes in auditory processing that match the physical properties of songs during the breeding season and calls outside of it. We tested this hypothesis in white-breasted nuthatches, Sitta carolinensis, tufted titmice, Baeolophus bicolor, and Carolina chickadees, Poecile carolinensis. We measured the envelope-following response (EFR), which quantifies phase locking to the amplitude envelope, and the frequency-following response (FFR), which quantifies phase locking to the temporal fine structure of sounds. Because songs and calls of nuthatches are amplitude modulated at different rates, we predicted seasonal changes in EFRs that match the rates of amplitude fluctuation in songs and calls. In chickadees and titmice, we predicted stronger FFRs during the spring and stronger EFRs during the winter because songs are tonal and calls include amplitude-modulated elements. In all three species, we found seasonal changes in EFRs and FFRs. EFRs varied across seasons and matched the amplitude modulations of songs and calls in nuthatches. In addition, female chickadees had stronger EFRs in the winter than in the spring. In all three species, FFRs during the spring tended to be stronger in females than in males. We also found species differences in EFRs and FFRs in both seasons; EFRs and FFRs tended to be higher in nuthatches than in chickadees and titmice. We discuss the potential mechanisms underlying seasonality in EFRs and FFRs and the implications of our results for communication during the breeding season and outside of it, when these three species form mixed-species flocks.     

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.     

Linking social complexity and vocal complexity: a parid perspective

The Paridae family (chickadees, tits and titmice) is an interesting avian group in that species vary in important aspects of their social structure and many species have large and complex vocal repertoires. For this reason, parids represent an important set of species for testing the social complexity hypothesis for vocal communication--the notion that as groups increase in social complexity, there is a need for increased vocal complexity. Here, we describe the hypothesis and some of the early evidence that supported the hypothesis. Next, we review literature on social complexity and on vocal complexity in parids, and describe some of the studies that have made explicit tests of the social complexity hypothesis in one parid--Carolina chickadees, Poecile carolinensis. We conclude with a discussion, primarily from a parid perspective, of the benefits and costs of grouping and of physiological factors that might mediate the relationship between social complexity and changes in signalling behaviour.     

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.     

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.     

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.     

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.     

Greater hippocampal neuronal recruitment in food-storing than in non-food-storing birds

Previous research has shown heightened recruitment of new neurons to the chickadee hippocampus in the fall. The present study was conducted to determine whether heightened fall recruitment is associated with the seasonal onset of food-storing by comparing neurogenesis in chickadees and a non-food-storing species, the house sparrow. Chickadees and house sparrows were captured in the wild in fall and spring and received multiple injections of the cell birth marker bromodeoxyuridine (BrdU). Birds were held in captivity and the level of hippocampal neuron recruitment was assessed after 6 weeks. Chickadees showed significantly more hippocampal neuronal recruitment than house sparrows. We found no seasonal differences in hippocampal neuronal recruitment in either species. In chickadees and in house sparrows, one-third of new cells labeled for BrdU also expressed the mature neuronal protein, NeuN. In a region adjacent to the hippocampus, the hyperpallium apicale, we observed no significant differences in neuronal recruitment between species or between seasons. Hippocampal volume and total neuron number both were greater in spring than in fall in chickadees, but no seasonal differences were observed in house sparrows. Enhanced neuronal recruitment in the hippocampus of food-storing chickadees suggests a degree of neurogenic specialization that may be associated with the spatial memory requirements of food-storing behavior.     

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.     

Evaluating the accuracy and biological meaning of visits to RFID‐enabled bird feeders using video

Radio‐frequency identification (RFID) technology has gained popularity in ornithological studies as a way to collect large quantities of data to answer specific biological questions, but few published studies report methodologies used for validating the accuracy of RFID data. Further, connections between the RFID data and the behaviors of interest in a study are not always clearly established. These methodological deficiencies may seriously impact a study''s results and subsequent interpretation. We built RFID‐equipped bird feeders and mounted them at three sites in Tompkins County, New York. We deployed passive integrated transponder tags on black‐capped chickadees, tufted titmice, and white‐breasted nuthatches and used a GoPro video camera to record the three tagged species at the feeders. We then reviewed the video to determine the accuracy of the RFID reader and understand the birds’ behavior at the feeders. We found that our RFID system recorded only 34.2% of all visits by tagged birds (n = 237) and that RFID detection increased with the length of a visit. We also found that our three tagged species and two other species that visited the feeders, American goldfinch and hairy woodpecker, retrieved food in 79.5% of their visits. Chickadees, titmice, nuthatches, and woodpeckers spent, on average, 2.3 s at feeders to collect one seed per visit. In contrast, goldfinches spent an average of 9.0 s at feeders and consumed up to 30 seeds per visit. Our results demonstrate the importance of confirming detection accuracy and that video can be used to identify behavioral characteristics associated with an RFID reader''s detections. This simple—yet time‐intensive—method for assessing the accuracy and biological meaning of RFID data is useful for ornithological studies but can be used in research focusing on various taxa and study systems.     

Songbird frequency selectivity and temporal resolution vary with sex and season

Many species of songbirds exhibit dramatic seasonal variation in song output. Recent evidence suggests that seasonal changes in auditory processing are coincident with seasonal variation in vocal output. Here, we show, for the first time, that frequency selectivity and temporal resolution of the songbird auditory periphery change seasonally and in a sex-specific manner. Male and female house sparrows (Passer domesticus) did not differ in their frequency sensitivity during the non-breeding season, nor did they differ in their temporal resolution. By contrast, female house sparrows showed enhanced frequency selectivity during the breeding season, which was matched by a concomitant reduction of temporal resolution. However, males failed to show seasonal plasticity in either of these auditory properties. We discuss potential mechanisms generating these seasonal patterns and the implications of sex-specific seasonal changes in auditory processing for vocal communication.     

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.     

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.     

Prescribed Fire Effects on Wintering,Bark-Foraging Birds in Northern Arizona

ABSTRACT We examined effects of prescribed fire on 3 wintering, bark-foraging birds, hairy woodpeckers (Picoides villosus), pygmy nuthatches (Sitta pygmaea), and white-breasted nuthatches (S. carolinensis), in ponderosa pine (Pinus ponderosa) forests of northern Arizona, USA. During winters of 2004–2006, we compared bird density, foraging behavior, and bark beetle activity among burned treatment and unburned control units. Hairy woodpecker density was 5 times greater in burn units, whereas white-breasted nuthatches and pygmy nuthatches had similar densities between treatments. Compared to available trees, trees used by foraging hairy woodpeckers had 9 times greater odds of having bark beetles in control units and 12 times greater odds in burn units. Tree diameter appeared to be the main factor bark-foraging birds used in selecting winter foraging trees. Our results suggest that forest managers can use prescribed fire treatments without detrimental effects to wintering nuthatches, while providing additional food to hairy woodpeckers.     

Peripheral auditory processing changes seasonally in Gambel’s white-crowned sparrow

Song in oscine birds is a learned behavior that plays important roles in breeding. Pronounced seasonal differences in song behavior and in the morphology and physiology of the neural circuit underlying song production are well documented in many songbird species. Androgenic and estrogenic hormones largely mediate these seasonal changes. Although much work has focused on the hormonal mechanisms underlying seasonal plasticity in songbird vocal production, relatively less work has investigated seasonal and hormonal effects on songbird auditory processing, particularly at a peripheral level. We addressed this issue in Gambel’s white-crowned sparrow (Zonotrichia leucophrys gambelii), a highly seasonal breeder. Photoperiod and hormone levels were manipulated in the laboratory to simulate natural breeding and non-breeding conditions. Peripheral auditory function was assessed by measuring the auditory brainstem response (ABR) and distortion product otoacoustic emissions (DPOAEs) of males and females in both conditions. Birds exposed to breeding-like conditions demonstrated elevated thresholds and prolonged peak latencies when compared with birds housed under non-breeding-like conditions. There were no changes in DPOAEs, however, which indicates that the seasonal differences in ABRs do not arise from changes in hair cell function. These results suggest that seasons and hormones impact auditory processing as well as vocal production in wild songbirds.     

The effect of pinealectomy on circadian plasma melatonin levels in house sparrows and European starlings.

We determined 24-hr plasma melatonin profiles in intact, sham-pinealectomized, and pinealectomized European starlings (Sturnus vulgaris) and house sparrows (Passer domesticus) in a light-dark (LD) cycle and in constant darkness (DD). In the intact and sham-pinealectomized birds of both species, a melatonin rhythm was found, with low levels during the day and high levels during the night. Pinealectomy abolished the nighttime peak of melatonin in both species; hence, levels were low at all times sampled. This uniform response of plasma melatonin to pinealectomy contrasts with the differential response of circadian activity rhythms to pinealectomy for these two species. In DD, locomotor activity in pinealectomized house sparrows is usually arrhythmic, whereas in starlings a rhythm usually persists. This suggests that in the latter species free-running circadian rhythms are not necessarily dependent on a rhythm in plasma melatonin. The same is true for the synchronized activity rhythm observed in pinealectomized birds of both species in LD, as well as for the damped rhythm that persists in pinealectomized house sparrows following an LD-to-DD transfer. The results are consistent with the hypothesis that the pineal and its periodic output of melatonin constitute only one component in a system of at least two coupled pacemakers. They also suggest that there are species differences in the relative role played by the pineal and other pacemakers in controlling circadian rhythms in behavior.     

Microgeographic Variation and Sharing of the Gargle Vocalization and Its Component Syllables in Black-Capped Chickadee (Aves, Paridae, Poecile atricapillus) Populations

Throughout the year during agonistic encounters, black‐capped chickadees (Poecile atricapillus) emit a vocal signal known as the gargle call. Each bird has a repertoire of structurally differing gargle calls; some are shared with others in the local area. As a basis for understanding the cultural evolution of this social signal, we initiated a study of gargle call repertoires of birds living in a narrow belt of continuous riparian habitat occupied throughout by a resident population of chickadees. During two consecutive winter seasons, we sampled repertoires at three locations over a distance of 8.4 km to quantify micro‐geographical variation. Analyses of vocal sharing and population differentiation were carried out on whole gargle calls and on the individual acoustic units (syllables) from which the whole calls are constructed. We analysed 28 380 calls of 46 subjects in the two seasons of study. Birds averaged 7.6 different calls in their gargle repertoires. Calls were composed of about 10 syllables on average. Fifty‐six different syllables were used to construct the calls of all birds. Each study site had some gargle calls unique to the local birds and some that were shared with one or both of the other two sites. There was significantly greater sharing of both calls and syllables among birds within sample sites than between sample sites. The frequencies of the different kinds of gargles and syllables were significantly correlated across the 2 yr of the study, but the correlation was stronger (r² = 0.93) for syllables than for whole gargle calls (r² = 0.61).     

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.     

Validation of the doubly labeled water technique for measuring energy metabolism in starlings and sparrows

I have tested the idea that doubly labeled water (DLW) can accurately predict CO2 production in savannah sparrows, song sparrows, white-throated sparrows, starlings, and a single house sparrow by comparing DLW estimates with those obtained simultaneously by capturing expired CO2 in Ascarite. In addition I used the energy balance method to see if metabolic rates generated from DLW measurements accurately reflected the actual metabolic rates of these birds. I found close agreement in DLW and the gravimetric and energy balance methods, with DLW underestimating CO2 production on average by -3.5% in sparrows, and -7.1% in starlings. Similarly, the energy balance method indicated a -3.1% underestimate by DLW for sparrows and a -5.1% for starlings. The DLW method can yield reasonable estimates of CO2 production in a variety of passerine birds.