Megan D. Gall

Visual systems and vigilance behaviour of two ground-foraging avian prey species: white-crowned sparrows and California towhees

Predator–prey interactions are regulated by the ability of individuals to detect, and then approach or avoid, each other. In visually guided organisms, the prevalent view is that predators have large binocular visual fields and high acuity, whereas prey have wide lateral areas and low acuity, which could affect vigilance behaviour. We characterized the configuration of the visual system (visual fields, retinal topography, visual acuity) and vigilance behaviour (head movement rate) of two ground-foraging avian prey (white-crowned sparrow, Zonotrichia leucophrys, California towhee, Pipilo crissalis) with laterally placed eyes. We found that the binocular field of both species (45°) was actually wider than those of some of their avian predators. Both species also had a single retinal specialization (high ganglion cell density area) located in the centro-temporal sector of the retina, which projected into the lateral and frontal part of the head. Wide binocular fields may increase binocular contrast to detect and visually guide the bill towards prey items. Both species had wider lateral visual fields and faster head movement rates than some of their predators, probably to enhance detection and visual tracking of predators. California towhees made faster sideways movements of the head than did white-crowned sparrows, probably to cover visual space more quickly with their retinal specialization because of the comparatively lower spatial resolution of their retinal periphery. Alternatively, California towhees might move their heads more rapidly to monitor for potential risks (e.g. competitors, predators), as they rely mostly on personal information because of their degree of territoriality. Our findings suggest that the visual system and vigilance behaviour of these two avian prey species combine traits to enhance predator detection through large visual coverage and fast head movements, but also to enhance food detection at close range through enhanced binocular vision.

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.

Visual fields, eye movements, and scanning behavior of a sit-and-wait predator, the black phoebe (Sayornis nigricans).

Foraging mode influences the dominant sensory modality used by a forager and likely the strategies of information gathering used in foraging and anti-predator contexts. We assessed three components of visual information gathering in a sit-and-wait avian predator, the black phoebe (Sayornis nigricans): configuration of the visual field, degree of eye movement, and scanning behavior through head-movement rates. We found that black phoebes have larger lateral visual fields than similarly sized ground-foraging passerines, as well as relatively narrower binocular and blind areas. Black phoebes moved their eyes, but eye movement amplitude was relatively smaller than in other passerines. Black phoebes may compensate for eye movement constraints with head movements. The rate of head movements increased before attacking prey in comparison to non-foraging contexts and before movements between perches. These findings suggest that black phoebes use their lateral visual fields, likely subtended by areas of high acuity in the retina, to track prey items in a three-dimensional space through active head movements. These head movements may increase depth perception, motion detection and tracking. Studying information gathering through head movement changes, rather than body posture changes (head-up, head-down) as generally presented in the literature, may allow us to better understand the mechanisms of information gathering from a comparative perspective.

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 Physical and Visual Access to Prey on Patch Selection and Food Search Effort in a Sit-and-Wait Predator, the Black Phoebe

Abstract. For sit-and-wait predators, a key factor influencing foraging decisions is the ability to detect and track prey, which is expected to vary with the physical and light properties of the environment. We assessed how changes in visual and physical prey availability altered perch selection and visual search activity (head-movement rate and bout length) in the Black Phoebe (Sayornis nigricans), a sit-and-wait flycatcher. We used an observational approach by studying individuals in foraging areas that varied in the ecological factors of interest across an urbanized landscape. Black Phoebes selected perches with high levels of tree and grass cover and low light intensity, which could increase access to prey and reduce predation risk. Visual searching for prey decreased as grass cover increased and tree cover decreased, likely because of less physical and visual obstruction. Visual searching increased with light intensity, probably as a result of the effects of glare, but chromatic contrast did not exert a significant influence. We suggest that for Black Phoebes in urbanized areas physical access to prey may be mediated through the availability of an open understory and visual access through illuminance rather than discrimination of prey against the background.

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

SUMMARY 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.

Song structure, not high‐frequency song content, determines high‐frequency auditory sensitivity in nine species of New World sparrows (Passeriformes: Emberizidae)

Summary The evolution of vocal signals can be constrained by a host of factors including habitat effects on sound propagation, morphology of sound-producing structures and phylogenetic relationships among species. Here, we asked whether auditory sensitivity over a broad range of frequencies correlates with the spectral content of conspecific vocalizations, or whether it is constrained by the overall structure of vocalizations, habitat effects on sound propagation or relatedness among species. We studied nine New World sparrows (Passeriformes: Emberizidae) including three open-habitat species, three scrub-like habitat species and three forest species. For each habitat, one species had pure-trilled songs, another had tonal songs and another had complex songs with tones, trills and amplitude-modulated buzzes. As predicted by the acoustic adaptation hypothesis, song spectral properties (specifically frequency and entropy) had the highest values in open-habitat species and the lowest values in forest species. Based on our results from song analyses, and the sender–receiver matching hypothesis, we predicted that open-habitat species would be more sensitive to high-frequency sounds compared to forest species. Contrary to this prediction, habitat and high-frequency song content had little effect on audiogram shape. Song type, however, had a strong effect, with species that produce complex songs showing higher sensitivity to high-frequency sounds than all other species. Our results suggest that the use of song frequency by receivers depends on song structure and not necessarily on song spectral content. Therefore, our current understanding of how signal-processing mechanisms should match signal properties appears to be too simple. When thinking about the evolution of signal-processing mechanisms, the multidimensionality of signals, and how the different dimensions can interact, should be considered.

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 receivers 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.

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.

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.