In your CORT: Corticosterone and its receptors in the brain underlie mate choosiness in female Cope's gray treefrogs (Hyla chrysoscelis).

Selecting an attractive mate can involve trade-offs related to investment in sampling effort. Glucocorticoids like corticosterone (CORT) are involved in resolving energetic trade-offs. However, CORT is rarely studied in the context of mate choice, despite its elevated levels during reproductive readiness and the energetic transitions that characterize reproduction. Few systems are as well suited as anuran amphibians to evaluate how females resolve energetic trade-offs during mate choice. Phonotaxis tests provide a robust bioassay of mate choice that permit the precise measurement of inter-individual variation in traits such as choosiness-the willingness to pursue the most attractive mate despite costs. In Cope's gray treefrogs (Hyla chrysoscelis), females exhibit remarkable variation in circulating CORT as well as choosiness during mate choice, and a moderate dose of exogenous CORT rapidly (<1 h) and reliably induce large increases in choosiness. Here we measured the expression of glucocorticoid (GR) and mineralocorticoid (MR) receptors in the brains of females previously treated with exogenous CORT and tested for mate choosiness. We report a large decrease in GR expression in the hindbrain and midbrain of females that were treated with the moderate dosage of CORT-the same treatment group that exhibited a dramatic increase in choosiness following CORT treatment. This association, however, does not appear to be causal, as only forebrain GR levels, which are not affected by CORT injection, are positively associated with variation in choosiness. No strong effects were found for MR. We discuss these findings and suggest future studies to test the influence of glucocorticoids on mate choice.

Deer management influences perception of avian plumage in temperate deciduous forests.

Many animals use visual signals to communicate; birds use colorful plumage to attract mates and repel intruders. Visual signal conspicuousness is influenced by the lighting environment, which can be altered by human-induced changes. For example, deer-management efforts can affect vegetation structure and light availability. Whether these changes alter animal communication is still unknown. We investigated the effect of deer management on forest light and the contrast of understory birds against the forest background. We modeled visual perception using: (1) an ultraviolet-sensitive (UVS) avian model and plumage parameters representative of red, yellow, and blue birds (2) species-specific turkey visual and plumage parameters, and (3) individual-specific brown-headed cowbird visual and plumage parameters. Deer management led to greater light irradiance and lowered forest background reflectance. Management increased chromatic contrasts in the UVS model, primarily in deciduous forests and low understory, and across all habitat types in turkey and cowbird models. Deer management did not affect achromatic contrasts in the UVS model, but was associated with lower contrast in mixed forests for turkeys and across habitats for cowbirds. Together, this suggests that management of deer browsing is likely to impact visual signaling for a wide range of avian species. However, we also suspect that species- and individual-specific parameters increased the resolution of models, warranting consideration in future studies. Further work should determine if differences in visual perception translate to biologically relevant consequences. Our results suggest that, at least for some species, deer browsing and anthropogenic change may impose an evolutionary driver on visual communication.

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.

Effects of Frequency on the Directional Auditory Sensitivity of Northern Saw-Whet Owls (Aegolius acadicus).

Many animals use sound as a medium for detecting or locating potential prey items or predation threats. Northern saw-whet owls (Aegolius acadicus) are particularly interesting in this regard, as they primarily rely on sound for hunting in darkness, but are also subject to predation pressure from larger raptors. We hypothesized that these opposing tasks should favor sensitivity to low-frequency sounds arriving from many locations (potential predators) and high-frequency sounds below the animal (ground-dwelling prey items). Furthermore, based on the morphology of the saw-whet owl skull and the head-related transfer functions of related species, we expected that the magnitude of changes in sensitivity across spatial locations would be greater for higher frequencies than low frequencies (i.e., more "directional" at high frequencies). We used auditory-evoked potentials to investigate the frequency-specific directional sensitivity of Northern saw-whet owls to acoustic signals. We found some support for our hypothesis, with smaller-magnitude changes in sensitivity across spatial locations at lower frequencies and larger-magnitude changes at higher frequencies. In general, owls were most sensitive to sounds originating in front of and above their heads, but at 8 kHz there was also an area of high sensitivity below the animals. Our results suggest that the directional hearing of saw-whet owls should allow for both predator and prey detection.

Social Communication across Reproductive Boundaries: Hormones and the Auditory Periphery of Songbirds and Frogs.

Most animals experience reproductive transitions in their lives; for example, reaching reproductive maturity or cycling in and out of breeding condition. Some reproductive transitions are abrupt, while others are more gradual. In most cases, changes in communication between the sexes follow the time course of these reproductive transitions and are typically thought to be coordinated by steroid hormones. We know a great deal about hormonal control of communication behaviors in birds and frogs, as well as the central neural control of these behaviors. There has also been significant interest in the effects of steroid hormones on central nervous system structures that control both the production and reception of communication signals associated with reproductive behaviors. However, peripheral sensory structures have typically received less attention, although there has been growing interest in recent years. It is becoming clear that peripheral sensory systems play an important role in reproductive communication, are plastic across reproductive conditions, and, in some cases, this plasticity may be mediated by steroid hormones. In this article, we discuss recent evidence for the role of peripheral auditory structures in reproductive communication in birds and frogs, the plasticity of the peripheral auditory system, and the role of steroid hormones in mediating the effects of the peripheral auditory system on reproductive communication. We focus on both seasonal and acute reproductive transitions, introduce new data on the role of hormones in modulating seasonal patterns, and make recommendations for future work.

Moderately elevated glucocorticoids increase mate choosiness but do not affect sexual proceptivity or preferences in female gray treefrogs.

Glucocorticoids (GCs) are rarely studied in the context of female mate choice, despite the expression of receptors for these products in sexual, sensory and decision-making brain areas. Here we investigated the effects of GC concentrations on three aspects of female sexual behavior in breeding Cope's gray treefrogs (Hyla chrysoscelis): proceptivity-a measure of sexual motivation, intraspecific mate preferences, and mate choosiness. To our knowledge this is the first experimental study on the endocrine basis of mate choosiness. We predicted that mate choosiness-forfeiting an initial mate preference to pursue a suddenly more attractive mate-would be particularly impacted by elevated GCs with moderate GC levels associated with greater choosiness. We found support for this predicted inverted-U relationship. Females in the control group (no injection) showed no change in choosiness across timepoints. In contrast, females in the vehicle, Low (20 ng g-1) and High (180 ng g-1) corticosterone groups exhibited a nominal decline in choosiness after injection, suggesting that the experience of injection has little or perhaps slightly suppressive effects on female choosiness. Females in the moderate dose group (60 ng g-1), however, exhibited a significant increase (>100%) in choosiness. Further, we found no effect of elevated GCs on sexual proceptivity or the species-typical preference for longer calls. These findings may reflect a buffering of primary sensory areas in the brain against elevated GCs. The recruitment of other cognitive processes during active decision-making, however, may facilitate GC modulation of mate choosiness, thereby promoting tactical plasticity at this critical life history juncture.

Hearing in 3D: Directional Auditory Sensitivity of Northern Saw-Whet Owls (Aegolius acadicus).

Northern saw-whet owls (Aegolius acadicus) are nocturnal predators that are able to acoustically localize prey with great accuracy; an ability that is attributed to their unique asymmetrical ear structure. While a great deal of research has focused on open loop sound localization prior to flight in owls (primarily barn owls), directional sensitivity of the ears may also be important in locating moving prey on the wing. Furthermore, directionally sensitive ears may also reduce the effects of masking noise, either from the owls' wings during flight or environmental noise (e.g., wind and leaf rustling), by enhancing spatial segregation of target sounds and noise sources. Here, we investigated auditory processing of Northern saw-whet owls in three-dimensional space using auditory evoked potentials (AEPs). We simultaneously evoked auditory responses in two channels (right and left ear) with broadband clicks from a sound source that could be manipulated in space. Responses were evoked from 66 spatial locations, separated by 30° increments in both azimuth and elevation. We found that Northern saw-whet owls had increased sensitivity to sound sources directly in front of and above their beaks and decreased sensitivity to sound sources below and behind their heads. The spatial region of highest sensitivity extends from the lower beak to the crown of the head and 30° left or right of the median plane, dropping off beyond those margins. Directional sensitivity is undoubtedly useful during foraging and predator evasion, and may also reduce the effect of masking noise from the wings during flight due to the spatial segregation of the noise and targets of interest.

The paradox of hearing at the lek: auditory sensitivity increases after breeding in female gray treefrogs (Hyla chrysoscelis).

Both behavioral receptivity and neural sensitivity to acoustic mate attraction signals vary across the reproductive cycle, particularly in seasonally breeding animals. Across a variety of taxa receptivity to signals increases, as does peripheral auditory sensitivity, as females transition from a non-breeding to breeding condition. We recently documented decreases in receptivity to acoustic mate attraction signals and circulating hormone levels, but an increase in peripheral auditory sensitivity to call-like stimuli following oviposition in Cope's gray treefrogs (Hyla chrysoscelis). However, it is not known if changes in auditory sensitivity are confined to the frequency range of calls, or if they result from more generalized changes in the auditory periphery. Here, we used auditory brainstem responses (ABRs) to evaluate peripheral frequency sensitivity in female Cope's gray treefrogs before and after oviposition. We found lower ABR thresholds, greater ABR amplitudes, and shorter ABR latencies following oviposition. Changes were most pronounced and consistent at lower frequencies associated with the amphibian papilla, but were also detectable at higher frequencies corresponding to the tuning of the basilar papilla. Furthermore, only ABR latencies were correlated with circulating steroid hormones (testosterone). Changes in peripheral processing may result from changes in metabolic function or sensorineural adaptation to chorus noise.

Effects of presentation rate and onset time on auditory brainstem responses in Northern saw-whet owls (Aegolius acadicus).

Monitoring auditory brainstem responses (ABRs) is a common method of assessing auditory processing in non-model species. Although ABRs are widely used to compare auditory abilities across taxa, the extent to which different features of acoustic stimuli affect the ABR is largely unknown in most non-mammalian species. The authors investigated the effects of varying presentation rate and onset time to determine how different features of acoustic stimuli influence the ABR in Northern saw-whet owls (Aegolius acadicus), a species known for their unique auditory adaptations and hunting abilities. At presentation rates ranging from 21.1 to 51.1 s-1, there were no differences in the size or synchrony of ABRs, suggesting that stimuli can be presented at a relatively rapid rate to maximize the number of observations recorded for analysis. While increasing onset time was associated with a decrement in response size and synchrony, tonebursts with 1 ms onset times produced overgeneralized neural responses as a result of spectral splatter. This suggests that 2 to 3 ms onset times may balance the trade-off between response synchrony and frequency specificity when comparing relative neural recruitment across frequencies. These findings highlight the importance of considering stimulus parameters when interpreting ABR data.

Deer browsing alters sound propagation in temperate deciduous forests.

The efficacy of animal signals is strongly influenced by the structure of the habitat in which they are propagating. In recent years, the habitat structure of temperate forests has been increasingly subject to modifications from foraging by white-tailed deer (Odocoileus virginianus). Increasing deer numbers and the accompanying browsing have been shown to alter vegetation structure and thus the foraging, roosting, and breeding habitats of many species. However, despite a large body of literature on the effects of vegetation structure on sound propagation, we do not yet know what impact deer browsing may have on acoustic communication. Here we used playback experiments to determine whether sound fidelity and amplitude of white noise, pure tones, and trills differed between deer-browsed and deer-excluded plots. We found that sound fidelity, but not amplitude, differed between habitats, with deer-browsed habitats having greater sound fidelity than deer-excluded habitats. Difference in sound propagation characteristics between the two habitats could alter the efficacy of acoustic communication through plasticity, cultural evolution or local adaptation, in turn influencing vocally-mediated behaviors (e.g. agonistic, parent-offspring, mate selection). Reduced signal degradation suggests vocalizations may retain more information, improving the transfer of information to both intended and unintended receivers. Overall, our results suggest that deer browsing impacts sound propagation in temperate deciduous forest, although much work remains to be done on the potential impacts on communication.

The difference a day makes: Breeding remodels hearing, hormones and behavior in female Cope's gray treefrogs (Hyla chrysoscelis).

In seasonal breeders, there are behavioral, endocrine, and neural adaptations that promote the sexual receptivity of females and tune their sensory systems to detect and discriminate among advertising males and to successfully copulate. What happens immediately after this key life history event is unclear, but this transitional moment offers a window into the mechanisms that remodel sexual phenotypes. In this study of wild female Cope's gray treefrogs (Hyla chrysoscelis), we tested the hypothesis that oviposition results in a suite of coordinated changes in the sexual phenotype. Specifically, we predicted that sexual receptivity and discrimination behaviors would decline along with circulating concentrations of steroid hormones (corticosterone, estradiol, testosterone) and auditory sensitivity to the acoustic frequencies emphasized in male advertisement calls. We conducted these trait measurements before and after oviposition (ca. 24-h period). There was a 100% decrease in behavioral responsiveness after oviposition, and the concentrations of all three steroids plummeted during this brief window of time, especially testosterone. Moreover, higher concentrations of corticosterone-an important component of the endocrine stress response-were associated with longer response latencies, suggesting that adrenal hormones should be considered in future studies on the hormonal basis of mate choice. Counter to our prediction, auditory sensitivity increased following oviposition, and the amplitude of the auditory brainstem response was influenced by concentrations of estradiol. In pre-oviposition females auditory sensitivity diminished with increasing estradiol concentrations, while sensitivity increased with increasing estradiol concentrations in post-oviposition females, suggesting non-linear estrogenic modulation of peripheral auditory neural recruitment. Overall, our results indicate that there is considerable remodeling of behavioral output following oviposition that co-occurs with changes in both endocrine and sensory physiology.

Frequency sensitivity in Northern saw-whet owls (Aegolius acadicus).

Northern saw-whet owls (Aegolius acadicus) are known for their unique asymmetrical ear structure and ability to localize prey acoustically, yet few attempts have been made to explore the auditory capabilities of this species. In this study, we evoked auditory brainstem responses (ABRs) with tonebursts to assess three main hypotheses regarding the evolution of auditory sensitivity: sender-receiver matching, ecological constraints, and phylogenetic/morphological constraints. We found that ABR amplitude increased with increasing stimulus level, which is consistent with results in other avian species. ABR amplitudes, latencies, and thresholds indicate that the hearing range of Northern saw-whet owls extends from 0.7 to 8.6 kHz, with an extended frequency range of best sensitivity between 1.6 and 7.1 kHz. Sensitivity fell off rapidly above and below these frequencies. The average audiogram was structurally similar to those found in other species of owls, suggesting that phylogeny or morphology may be constraining the frequency range of auditory sensitivity. However, ABR thresholds were 10-25 dB lower than those of Eastern screech-owls (Megascops asio), with thresholds below 0 dB SPL in some individuals. The lowest thresholds were at frequencies not found in the vocalizations of Northern saw-whet owls, suggesting ecological constraints rather than conspecific vocalizations are driving absolute sensitivity.

The effects of call-like masking diminish after nightly exposure to conspecific choruses in green treefrogs (Hyla cinerea).

One of the major difficulties encountered by animals that select mates using acoustic signals is discriminating individual calls from the background noise generated by other conspecifics. Reducing the effects of conspecific masking could improve discrimination of individual calls from background noise. We used auditory evoked potentials to investigate the effects of forward masking on the responses to artificial calls in male and female treefrogs (Hyla cinerea), as well as whether hearing advertisement calls over several nights, as happens in natural frog choruses, could modify the effects of masking. We found that response amplitude decreased with decreasing interstimulus interval when the masker was equal in amplitude to the stimulus. We also found evidence of a priming effect, whereby response amplitude at lower masker amplitudes was greater than when the target stimulus was not preceded by a masker. Finally, we found that the effect of masking was diminished by 10 nights of chorus exposure (i.e. responses were stronger to target stimuli), whereas there was no change in response in the control group. Our results show that hearing dynamic social stimuli, such as frog choruses, can alter the responses of the auditory periphery in a way that could enhance the detection of and response to conspecific acoustic communication signals.

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.

Hearing conspecific vocal signals alters peripheral auditory sensitivity.

We investigated whether hearing advertisement calls over several nights, as happens in natural frog choruses, modified the responses of the peripheral auditory system in the green treefrog, Hyla cinerea. Using auditory evoked potentials (AEP), we found that exposure to 10 nights of a simulated male chorus lowered auditory thresholds in males and females, while exposure to random tones had no effect in males, but did result in lower thresholds in females. The threshold change was larger at the lower frequencies stimulating the amphibian papilla than at higher frequencies stimulating the basilar papilla. Suprathreshold responses to tonal stimuli were assessed for two peaks in the AEP recordings. For the peak P1 (assessed for 0.8-1.25 kHz), peak amplitude increased following chorus exposure. For peak P2 (assessed for 2-4 kHz), peak amplitude decreased at frequencies between 2.5 and 4.0 kHz, but remained unaltered at 2.0 kHz. Our results show for the first time, to our knowledge, that hearing dynamic social stimuli, like frog choruses, can alter the responses of the auditory periphery in a way that could enhance the detection of and response to conspecific acoustic communication signals.

Prior experience with conspecific signals enhances auditory midbrain responsiveness to conspecific vocalizations.

There is a long history in neuroethology of investigating how communication signals influence the brain and behavior. It has become increasingly clear that brain areas associated with sensory processing are plastic in adults and that this plasticity is related to reproductive condition. However, the role of communication signal reception in adult auditory plasticity has received relatively little attention. Here, we investigated whether the reception of communication signals (a frog chorus) could enhance the responsiveness of the auditory system to future reception of communication signals (a single male call). We found that animals that had been exposed to 10 days of a male chorus had stronger auditory midbrain immediate early gene expression than animals that had been exposed to 10 days of random tones when tested with 30 min of male calls or 30 min of tones. Our results suggest that exposure to dynamic social stimuli, like frog choruses, may play an important role in shaping the neural and behavioral responses to communication signals.

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.

Effects of habitat and urbanization on the active space of brown-headed cowbird song.

The ability of a receiver to detect a signal is a product of the signal characteristics at the sender, habitat-specific degradation of the signal, and properties of the receiver's sensory system. Active space describes the maximum distance at which a receiver with a given sensory system can detect a signal in a given habitat. Here the effect of habitat structure and urbanization on brown-headed cowbird (Molothrus ater) perched song active space was explored. The active space of the cowbird song was affected by both habitat type and level of urbanization. High frequency (4 to 6 kHz) portions of song resulted in the maximum active space. Surprisingly, the active space was the largest in open urban environments. The hard surfaces found in open urban areas (e.g., sidewalks, buildings) may provide a sound channel that enhances song propagation. When the introductory phrase and final phrase were analyzed separately, the active space of the introductory phrase was found to decrease in open urban environments but the active space of the final phrase increased in open urban environments. This suggests that different portions of the vocalization may be differentially influenced by habitat and level of urbanization.

The sender-receiver matching hypothesis: support from the peripheral coding of acoustic features in songbirds.

The sender-receiver matching hypothesis predicts that species-specific features of vocalizations will be reflected in species-specific auditory processing. This hypothesis has most often been invoked to explain correlations between vocal frequency ranges and the frequency range of auditory sensitivity; however, it could apply to other structural features, such as the rise time of stimuli. We explored this hypothesis in five songbird species that vary in the rise times and frequency range of their vocalizations. We recorded auditory evoked potentials (AEPs) to onset and sustained portions of stimuli that varied in both frequency and rise time. AEPs are gross potentials generated in the auditory nerve and brainstem and measured from the scalp. We found that species with shorter rise times in their vocalizations had greater amplitude and shorter latency onset AEPs than species with longer rise times. We also found that species with lower frequency and/or more tonal vocalizations had stronger sustained AEPs that follow the sound pressure changes in the stimulus (i.e. frequency following responses) than species with higher frequency and/or less tonal vocalizations. This is the first study in songbirds to show that acoustic features such as rise time and tonality are reflected in peripheral auditory processing.

Two measures of temporal resolution in brown-headed cowbirds (Molothrus ater).

Studies of auditory temporal resolution in birds have traditionally examined processing capabilities by assessing behavioral discrimination of sounds varying in temporal structure. Here, temporal resolution of the brown-headed cowbird (Molothrus ater) was measured using two auditory evoked potential (AEP)-based methods: auditory brainstem responses (ABRs) to paired clicks and envelope following responses (EFRs) to amplitude-modulated tones. The basic patterns observed in cowbirds were similar to those found in other songbird species, suggesting similar temporal processing capabilities. The amplitude of the ABR to the second click was less than that of the first click at inter-click intervals less than 10 ms, and decreased to 30% at an interval of 1 ms. EFR amplitude was generally greatest at modulation frequencies from 335 to 635 Hz and decreased at higher and lower modulation frequencies. Compared to data from terrestrial mammals these results support recent behavioral findings of enhanced temporal resolution in birds. General agreement between these AEP results and behaviorally based studies suggests that AEPs can provide a useful assessment of temporal resolution in wild bird species.