The spatiotemporal richness of hummingbird wing deformations.

Animals exhibit an abundant diversity of forms, and this diversity is even more evident when considering animals that can change shape on demand. The evolution of flexibility contributes to aspects of performance from propulsive efficiency to environmental navigation. It is, however, challenging to quantify and compare body parts that, by their nature, dynamically vary in shape over many time scales. Commonly, body configurations are tracked by labelled markers and quantified parametrically through conventional measures of size and shape (descriptor approach) or non-parametrically through data-driven analyses that broadly capture spatiotemporal deformation patterns (shape variable approach). We developed a weightless marker tracking technique and combined these analytic approaches to study wing morphological flexibility in hoverfeeding Anna's hummingbirds (Calypte anna). Four shape variables explained >95% of typical stroke cycle wing shape variation and were broadly correlated with specific conventional descriptors such as wing twist and area. Moreover, shape variables decomposed wing deformations into pairs of in-plane and out-of-plane components at integer multiples of the stroke frequency. This property allowed us to identify spatiotemporal deformation profiles characteristic of hoverfeeding with experimentally imposed kinematic constraints, including through shape variables explaining <10% of typical shape variation. Hoverfeeding in front of a visual barrier restricted stroke amplitude and elicited increased stroke frequencies together with in-plane and out-of-plane deformations throughout the stroke cycle. Lifting submaximal loads increased stroke amplitudes at similar stroke frequencies together with prominent in-plane deformations during the upstroke and pronation. Our study highlights how spatially and temporally distinct changes in wing shape can contribute to agile fluidic locomotion.

Selecting auditory alerting stimuli for eagles on the basis of auditory evoked potentials.

Development of wind energy facilities results in interactions between wildlife and wind turbines. Raptors, including bald and golden eagles, are among the species known to incur mortality from these interactions. Several alerting technologies have been proposed to mitigate this mortality by increasing eagle avoidance of wind energy facilities. However, there has been little attempt to match signals used as alerting stimuli with the sensory capabilities of target species like eagles. One potential approach to tuning signals is to use sensory physiology to determine what stimuli the target eagle species are sensitive to even in the presence of background noise, thereby allowing the development of a maximally stimulating signal. To this end, we measured auditory evoked potentials of bald and golden eagles to determine what types of sounds eagles can process well, especially in noisy conditions. We found that golden eagles are significantly worse than bald eagles at processing rapid frequency changes in sounds, but also that noise effects on hearing in both species are minimal in response to rapidly changing sounds. Our findings therefore suggest that sounds of intermediate complexity may be ideal both for targeting bald and golden eagle hearing and for ensuring high stimulation in noisy field conditions. These results suggest that the sensory physiology of target species is likely an important consideration when selecting auditory alerting sounds and may provide important insight into what sounds have a reasonable probability of success in field applications under variable conditions and background noise.

Spatial and Temporal Resolution of the Visual System of the Anna's Hummingbird (Calypte anna) Relative to Other Birds.

Hummingbirds are an emerging model for studies of the visual guidance of flight. However, basic properties of their visual systems, such as spatial and temporal visual resolution, have not been characterized. We measured both the spatial and temporal visual resolution of Anna's hummingbirds using behavioral experiments and anatomical estimates. Spatial visual resolution was determined behaviorally using the optocollic reflex and anatomically using peak retinal ganglion cell densities from retinal whole mounts and eye size. Anna's hummingbirds have a spatial visual resolution of 5-6 cycles per degree when measured behaviorally, which matches anatomical estimates (fovea: 6.26±0.12 cycles per degree; area temporalis: 5.59±0.15 cycles per degree; and whole eye average: 4.64±0.08 ). To determine temporal visual resolution, we used an operant conditioning paradigm wherein hummingbirds were trained to use a flickering light to find a food reward. The limits of temporal visual resolution were estimated as 70-80 Hz. To compare Anna's hummingbirds with other bird species, we used a phylogenetically controlled analysis of previously published data on avian visual resolutions and body size. Our measurements for Anna's hummingbird vision fall close to and below predictions based on body size for spatial visual resolution and temporal visual resolution, respectively. These results indicate that the enhanced flight performance and foraging behaviors of hummingbirds do not require enhanced spatial or temporal visual resolution. This finding is important for interpreting flight control studies and contributes to a growing understanding of avian vision.

Assessing bird avoidance of high-contrast lights using a choice test approach: implications for reducing human-induced avian mortality.

BACKGROUND: Avian collisions with man-made objects and vehicles (e.g., buildings, cars, airplanes, power lines) have increased recently. Lights have been proposed to alert birds and minimize the chances of collisions, but it is challenging to choose lights that are tuned to the avian eye and can also lead to avoidance given the differences between human and avian vision. We propose a choice test to address this problem by first identifying wavelengths of light that would over-stimulate the retina using species-specific perceptual models and by then assessing the avoidance/attraction responses of brown-headed cowbirds to these lights during daytime using a behavioral assay. METHODS: We used perceptual models to estimate wavelength-specific light emitting diode (LED) lights with high chromatic contrast. The behavioral assay consisted of an arena where the bird moved in a single direction and was forced to make a choice (right/left) using a single-choice design (one side with the light on, the other with the light off) under diurnal light conditions. RESULTS: First, we identified lights with high saliency from the cowbird visual perspective: LED lights with peaks at 380 nm (ultraviolet), 470 nm (blue), 525 nm (green), 630 nm (red), and broad-spectrum (white) LED lights. Second, we found that cowbirds significantly avoided LED lights with peaks at 470 and 630 nm, but did not avoid or prefer LED lights with peaks at 380 and 525 nm or white lights. DISCUSSION: The two lights avoided had the highest chromatic contrast but relatively lower levels of achromatic contrast. Our approach can optimize limited resources to narrow down wavelengths of light with high visual saliency for a target species leading to avoidance. These lights can be used as candidates for visual deterrents to reduce collisions with man-made objects and vehicles.

The Orientation of Visual Space from the Perspective of Hummingbirds.

Vision is a key component of hummingbird behavior. Hummingbirds hover in front of flowers, guide their bills into them for foraging, and maneuver backwards to undock from them. Capturing insects is also an important foraging strategy for most hummingbirds. However, little is known about the visual sensory specializations hummingbirds use to guide these two foraging strategies. We characterized the hummingbird visual field configuration, degree of eye movement, and orientation of the centers of acute vision. Hummingbirds had a relatively narrow binocular field (~30°) that extended above and behind their heads. Their blind area was also relatively narrow (~23°), which increased their visual coverage (about 98% of their celestial hemisphere). Additionally, eye movement amplitude was relatively low (~9°), so their ability to converge or diverge their eyes was limited. We confirmed that hummingbirds have two centers of acute vision: a fovea centralis, projecting laterally, and an area temporalis, projecting more frontally. This retinal configuration is similar to other predatory species, which may allow hummingbirds to enhance their success at preying on insects. However, there is no evidence that their temporal area could visualize the bill tip or that eye movements could compensate for this constraint. Therefore, guidance of precise bill position during the process of docking occurs via indirect cues or directly with low visual acuity despite having a temporal center of acute vision. The large visual coverage may favor the detection of predators and competitors even while docking into a flower. Overall, hummingbird visual configuration does not seem specialized for flower docking.

Visual Sensory Signals Dominate Tactile Cues during Docked Feeding in Hummingbirds.

Animals living in and interacting with natural environments must monitor and respond to changing conditions and unpredictable situations. Using information from multiple sensory systems allows them to modify their behavior in response to their dynamic environment but also creates the challenge of integrating different, and potentially contradictory, sources of information for behavior control. Understanding how multiple information streams are integrated to produce flexible and reliable behavior is key to understanding how behavior is controlled in natural settings. Natural settings are rarely still, which challenges animals that require precise body position control, like hummingbirds, which hover while feeding from flowers. Tactile feedback, available only once the hummingbird is docked at the flower, could provide additional information to help maintain its position at the flower. To investigate the role of tactile information for hovering control during feeding, we first asked whether hummingbirds physically interact with a feeder once docked. We quantified physical interactions between docked hummingbirds and a feeder placed in front of a stationary background pattern. Force sensors on the feeder measured a complex time course of loading that reflects the wingbeat frequency and bill movement of feeding hummingbirds, and suggests that they sometimes push against the feeder with their bill. Next, we asked whether the measured tactile interactions were used by feeding hummingbirds to maintain position relative to the feeder. We created two experimental scenarios-one in which the feeder was stationary and the visual background moved and the other where the feeder moved laterally in front of a white background. When the visual background pattern moved, docked hummingbirds pushed significantly harder in the direction of horizontal visual motion. When the feeder moved, and the background was stationary, hummingbirds generated aerodynamic force in the opposite direction of the feeder motion. These results suggest that docked hummingbirds are using visual information about the environment to maintain body position and orientation, and not actively tracking the motion of the feeder. The absence of flower tracking behavior in hummingbirds contrasts with the behavior of hawkmoths, and provides evidence that they rely primarily on the visual background rather than flower-based cues while feeding.

Neurons Responsive to Global Visual Motion Have Unique Tuning Properties in Hummingbirds.

Neurons in animal visual systems that respond to global optic flow exhibit selectivity for motion direction and/or velocity. The avian lentiformis mesencephali (LM), known in mammals as the nucleus of the optic tract (NOT), is a key nucleus for global motion processing [1-4]. In all animals tested, it has been found that the majority of LM and NOT neurons are tuned to temporo-nasal (back-to-front) motion [4-11]. Moreover, the monocular gain of the optokinetic response is higher in this direction, compared to naso-temporal (front-to-back) motion [12, 13]. Hummingbirds are sensitive to small visual perturbations while hovering, and they drift to compensate for optic flow in all directions [14]. Interestingly, the LM, but not other visual nuclei, is hypertrophied in hummingbirds relative to other birds [15], which suggests enhanced perception of global visual motion. Using extracellular recording techniques, we found that there is a uniform distribution of preferred directions in the LM in Anna's hummingbirds, whereas zebra finch and pigeon LM populations, as in other tetrapods, show a strong bias toward temporo-nasal motion. Furthermore, LM and NOT neurons are generally classified as tuned to "fast" or "slow" motion [10, 16, 17], and we predicted that most neurons would be tuned to slow visual motion as an adaptation for slow hovering. However, we found the opposite result: most hummingbird LM neurons are tuned to fast pattern velocities, compared to zebra finches and pigeons. Collectively, these results suggest a role in rapid responses during hovering, as well as in velocity control and collision avoidance during forward flight of hummingbirds.

Hummingbirds control hovering flight by stabilizing visual motion.

Relatively little is known about how sensory information is used for controlling flight in birds. A powerful method is to immerse an animal in a dynamic virtual reality environment to examine behavioral responses. Here, we investigated the role of vision during free-flight hovering in hummingbirds to determine how optic flow--image movement across the retina--is used to control body position. We filmed hummingbirds hovering in front of a projection screen with the prediction that projecting moving patterns would disrupt hovering stability but stationary patterns would allow the hummingbird to stabilize position. When hovering in the presence of moving gratings and spirals, hummingbirds lost positional stability and responded to the specific orientation of the moving visual stimulus. There was no loss of stability with stationary versions of the same stimulus patterns. When exposed to a single stimulus many times or to a weakened stimulus that combined a moving spiral with a stationary checkerboard, the response to looming motion declined. However, even minimal visual motion was sufficient to cause a loss of positional stability despite prominent stationary features. Collectively, these experiments demonstrate that hummingbirds control hovering position by stabilizing motions in their visual field. The high sensitivity and persistence of this disruptive response is surprising, given that the hummingbird brain is highly specialized for sensory processing and spatial mapping, providing other potential mechanisms for controlling position.