Roslyn Dakin

Visual guidance of forward flight in hummingbirds reveals control based on image features instead of pattern velocity

Significance Birds can steer a precise course at high speed, but little is known about how they avoid collisions with surrounding objects and the ground. We manipulated the visual environment of hummingbirds as they flew across a long chamber to evaluate how they use visual information for course control. We found that lateral course control is based on the vertical size of features, rather than the strategy observed in insects of regulating fore–aft image velocity. However, like insects, birds use image velocity in the vertical axis for altitude control. Our results suggest that in natural settings, birds may avoid collisions by monitoring the vertical size, expansion, and relative position of obstacles. Information about self-motion and obstacles in the environment is encoded by optic flow, the movement of images on the eye. Decades of research have revealed that flying insects control speed, altitude, and trajectory by a simple strategy of maintaining or balancing the translational velocity of images on the eyes, known as pattern velocity. It has been proposed that birds may use a similar algorithm but this hypothesis has not been tested directly. We examined the influence of pattern velocity on avian flight by manipulating the motion of patterns on the walls of a tunnel traversed by Anna’s hummingbirds. Contrary to prediction, we found that lateral course control is not based on regulating nasal-to-temporal pattern velocity. Instead, birds closely monitored feature height in the vertical axis, and steered away from taller features even in the absence of nasal-to-temporal pattern velocity cues. For vertical course control, we observed that birds adjusted their flight altitude in response to upward motion of the horizontal plane, which simulates vertical descent. Collectively, our results suggest that birds avoid collisions using visual cues in the vertical axis. Specifically, we propose that birds monitor the vertical extent of features in the lateral visual field to assess distances to the side, and vertical pattern velocity to avoid collisions with the ground. These distinct strategies may derive from greater need to avoid collisions in birds, compared with small insects.

Burst muscle performance predicts the speed, acceleration, and turning performance of Anna’s hummingbirds

Despite recent advances in the study of animal flight, the biomechanical determinants of maneuverability are poorly understood. It is thought that maneuverability may be influenced by intrinsic body mass and wing morphology, and by physiological muscle capacity, but this hypothesis has not yet been evaluated because it requires tracking a large number of free flight maneuvers from known individuals. We used an automated tracking system to record flight sequences from 20 Annas hummingbirds flying solo and in competition in a large chamber. We found that burst muscle capacity predicted most performance metrics. Hummingbirds with higher burst capacity flew with faster velocities, accelerations, and rotations, and they used more demanding complex turns. In contrast, body mass did not predict variation in maneuvering performance, and wing morphology predicted only the use of arcing turns and high centripetal accelerations. Collectively, our results indicate that burst muscle capacity is a key predictor of maneuverability. DOI: http://dx.doi.org/10.7554/eLife.11159.001

Starvation-Induced Depotentiation of Bitter Taste in Drosophila

Nutrient deprivation can lead to dramatic changes in feeding behavior, including acceptance of foods that are normally rejected. In flies, this behavioral shift depends in part on reciprocal sensitization and desensitization of sweet and bitter taste, respectively. However, the mechanisms for bitter taste modulation remain unclear. Here, we identify a set of octopaminergic/tyraminergic neurons, named OA-VLs, that directly modulate bitter sensory neuron output in response to starvation. OA-VLs are in close proximity to bitter sensory neuron axon terminals and show reduced tonic firing following starvation. We find that octopamine and tyramine potentiate bitter sensory neuron responses, suggesting that starvation-induced reduction in OA-VL activity depotentiates bitter taste. Consistent with this model, artificial silencing of OA-VL activity induces a starvation-like reduction in bitter sensory neuron output. These results demonstrate that OA-VLs mediate a critical step in starvation-dependent bitter taste modulation, allowing flies to dynamically balance the risks associated with bitter food consumption against the threat of severe starvation.

Analysis of the Optimal Duration of Behavioral Observations Based on an Automated Continuous Monitoring System in Tree Swallows (Tachycineta bicolor): Is One Hour Good Enough?

Studies of animal behavior often rely on human observation, which introduces a number of limitations on sampling. Recent developments in automated logging of behaviors make it possible to circumvent some of these problems. Once verified for efficacy and accuracy, these automated systems can be used to determine optimal sampling regimes for behavioral studies. Here, we used a radio-frequency identification (RFID) system to quantify parental effort in a bi-parental songbird species: the tree swallow (Tachycineta bicolor). We found that the accuracy of the RFID monitoring system was similar to that of video-recorded behavioral observations for quantifying parental visits. Using RFID monitoring, we also quantified the optimum duration of sampling periods for male and female parental effort by looking at the relationship between nest visit rates estimated from sampling periods with different durations and the total visit numbers for the day. The optimum sampling duration (the shortest observation time that explained the most variation in total daily visits per unit time) was 1h for both sexes. These results show that RFID and other automated technologies can be used to quantify behavior when human observation is constrained, and the information from these monitoring technologies can be useful for evaluating the efficacy of human observation methods.

Biomechanics of the Peacock’s Display: How Feather Structure and Resonance Influence Multimodal Signaling

Courtship displays may serve as signals of the quality of motor performance, but little is known about the underlying biomechanics that determines both their signal content and costs. Peacocks (Pavo cristatus) perform a complex, multimodal “train-rattling” display in which they court females by vibrating the iridescent feathers in their elaborate train ornament. Here we study how feather biomechanics influences the performance of this display using a combination of field recordings and laboratory experiments. Using high-speed video, we find that train-rattling peacocks stridulate their tail feathers against the train at 25.6 Hz, on average, generating a broadband, pulsating mechanical sound at that frequency. Laboratory measurements demonstrate that arrays of peacock tail and train feathers have a broad resonant peak in their vibrational spectra at the range of frequencies used for train-rattling during the display, and the motion of feathers is just as expected for feathers shaking near resonance. This indicates that peacocks are able to drive feather vibrations energetically efficiently over a relatively broad range of frequencies, enabling them to modulate the feather vibration frequency of their displays. Using our field data, we show that peacocks with longer trains use slightly higher vibration frequencies on average, even though longer train feathers are heavier and have lower resonant frequencies. Based on these results, we propose hypotheses for future studies of the function and energetics of this display that ask why its dynamic elements might attract and maintain female attention. Finally, we demonstrate how the mechanical structure of the train feathers affects the peacock’s visual display by allowing the colorful iridescent eyespots–which strongly influence female mate choice–to remain nearly stationary against a dynamic iridescent background.

Deceptive Copulation Calls Attract Female Visitors to Peacock Leks

Theory holds that dishonest signaling can be stable if it is rare. We report here that some peacocks perform specialized copulation calls (hoots) when females are not present and the peacocks are clearly not attempting to copulate. Because these solo hoots are almost always given out of view of females, they may be dishonest signals of male mating attempts. These dishonest calls are surprisingly common, making up about a third of all hoot calls in our study populations. Females are more likely to visit males after they give a solo hoot call, and we confirm using a playback experiment that females are attracted to the sound of the hoot. Our findings suggest that both sexes use the hoot call tactically: females to locate potential mates and males to attract female visitors. We suggest that the solo hoot may be a deceptive signal that is acquired and maintained through reward-based learning.

Morphology, muscle capacity, skill, and maneuvering ability in hummingbirds

Making quick turns Hummingbirds are well known for their impressive maneuvering during flight. Dakin et al. used a computer vision approach to characterize the details of flight in >200 hummingbirds from 25 species (see the Perspective by Wainwright). Larger species had enhanced agility owing to increased muscle mass. In all species, muscles dictated transitional movement, whereas wing shape facilitated sharp turns and rapid rotations. Species, and individuals within species, played on their strengths by combining inherent traits and learned skills. Science, this issue p. 653; see also p. 636 Hummingbirds use strength and skill to shape their rapid movements. How does agility evolve? This question is challenging because natural movement has many degrees of freedom and can be influenced by multiple traits. We used computer vision to record thousands of translations, rotations, and turns from more than 200 hummingbirds from 25 species, revealing that distinct performance metrics are correlated and that species diverge in their maneuvering style. Our analysis demonstrates that the enhanced maneuverability of larger species is explained by their proportionately greater muscle capacity and lower wing loading. Fast acceleration maneuvers evolve by recruiting changes in muscle capacity, whereas fast rotations and sharp turns evolve by recruiting changes in wing morphology. Both species and individuals use turns that play to their strengths. These results demonstrate how both skill and biomechanical traits shape maneuvering behavior.

Weather matters: begging calls are temperature- and size-dependent signals of offspring state

Begging calls provide a way for parents to gauge offspring state. Although temperature is known to affect call production, previous studies have not examined the influence of ambient temperature at the nest. We recorded ambient temperature and begging calls of 3 day-old tree swallows ( Tachycineta bicolor ). Our results indicate that typical daily temperature flux can dramatically alter a brood’s begging calls, depending on body size. Broods with small (low body mass) nestlings decreased the rate and length of their calls at colder temperatures, consistent with a biophysical constraint. In contrast, broods with large (high body mass) nestlings increased the rate of their calls at colder temperatures. Parents responded in a context-dependent manner, returning more rapidly after smaller nestlings gave longer begging calls. Our results suggest that the function of offspring begging calls is highly dynamic, with environmental conditions altering the relationship between begging calls and offspring state.