James D. Crall

Linking biomechanics and ecology through predator–prey interactions: flight performance of dragonflies and their prey

SUMMARY Aerial predation is a highly complex, three-dimensional flight behavior that affects the individual fitness and population dynamics of both predator and prey. Most studies of predation adopt either an ecological approach in which capture or survival rates are quantified, or a biomechanical approach in which the physical interaction is studied in detail. In the present study, we show that combining these two approaches provides insight into the interaction between hunting dragonflies (Libellula cyanea) and their prey (Drosophila melanogaster) that neither type of study can provide on its own. We performed >2500 predation trials on nine dragonflies housed in an outdoor artificial habitat to identify sources of variability in capture success, and analyzed simultaneous predator–prey flight kinematics from 50 high-speed videos. The ecological approach revealed that capture success is affected by light intensity in some individuals but that prey density explains most of the variability in success rate. The biomechanical approach revealed that fruit flies rarely respond to approaching dragonflies with evasive maneuvers, and are rarely successful when they do. However, flies perform random turns during flight, whose characteristics differ between individuals, and these routine, erratic turns are responsible for more failed predation attempts than evasive maneuvers. By combining the two approaches, we were able to determine that the flies pursued by dragonflies when prey density is low fly more erratically, and that dragonflies are less successful at capturing them. This highlights the importance of considering the behavior of both participants, as well as their biomechanics and ecology, in developing a more integrative understanding of organismal interactions.

Resilin in dragonfly and damselfly wings and its implications for wing flexibility

Although there is mounting evidence that passive mechanical dynamics of insect wings play an integral role in insect flight, our understanding of the structural details underlying insect wing flexibility remains incomplete. Here, we use comparative morphological and mechanical techniques to illuminate the function and diversity of two mechanisms within Odonata wings presumed to affect dynamic wing deformations: flexible resilin vein‐joints and cuticular spikes. Mechanical tests show that joints with more resilin have lower rotational stiffness and deform more in response to a load applied to an intact wing. Morphological studies of 12 species of Odonata reveal that resilin joints and cuticular spikes are widespread taxonomically, yet both traits display a striking degree of morphological and functional diversity that follows taxonomically distinct patterns. Interestingly, damselfly wings (suborder Zygoptera) are mainly characterized by vein‐joints that are double‐sided (containing resilin both dorsally and ventrally), whereas dragonfly wings (suborder Epiprocta) are largely characterized by single‐sided vein‐joints (containing resilin either ventrally or dorsally, but not both). The functional significance and diversity of resilin joints and cuticular spikes could yield insight into the evolutionary relationship between form and function of wings, as well as revealing basic principles of insect wing mechanical design. J. Morphol., 2011.

Rolling with the flow: Bumblebees flying in unsteady wakes

SUMMARY Our understanding of how variable wind in natural environments affects flying insects is limited because most studies of insect flight are conducted in either smooth flow or still air conditions. Here, we investigate the effects of structured, unsteady flow (the von Karman vortex street behind a cylinder) on the flight performance of bumblebees (Bombus impatiens). Bumblebees are ‘all-weather’ foragers and thus frequently experience variable aerial conditions, ranging from fully mixed, turbulent flow to unsteady, structured vortices near objects such as branches and stems. We examined how bumblebee flight performance differs in unsteady versus smooth flow, as well as how the orientation of unsteady flow structures affects their flight performance, by filming bumblebees flying in a wind tunnel under various flow conditions. The three-dimensional flight trajectories and orientations of bumblebees were quantified in each of three flow conditions: (1) smooth flow, (2) the unsteady wake of a vertical cylinder (inducing strong lateral disturbances) and (3) the unsteady wake of a horizontal cylinder (inducing strong vertical disturbances). In both unsteady conditions, bumblebees attenuated the disturbances induced by the wind quite effectively, but still experienced significant translational and rotational fluctuations as compared with flight in smooth flow. Bees appeared to be most sensitive to disturbance along the lateral axis, displaying large lateral accelerations, translations and rolling motions in response to both unsteady flow conditions, regardless of orientation. Bees also displayed the greatest agility around the roll axis, initiating voluntary casting maneuvers and correcting for lateral disturbances mainly through roll in all flow conditions. Both unsteady flow conditions reduced the upstream flight speed of bees, suggesting an increased cost of flight in unsteady flow, with potential implications for foraging patterns and colony energetics in natural, variable wind environments.

Dynamics of animal movement in an ecological context: dragonfly wing damage reduces flight performance and predation success.

Much of our understanding of the control and dynamics of animal movement derives from controlled laboratory experiments. While many aspects of animal movement can be probed only in these settings, a more complete understanding of animal locomotion may be gained by linking experiments on relatively simple motions in the laboratory to studies of more complex behaviours in natural settings. To demonstrate the utility of this approach, we examined the effects of wing damage on dragonfly flight performance in both a laboratory drop–escape response and the more natural context of aerial predation. The laboratory experiment shows that hindwing area loss reduces vertical acceleration and average flight velocity, and the predation experiment demonstrates that this type of wing damage results in a significant decline in capture success. Taken together, these results suggest that wing damage may take a serious toll on wild dragonflies, potentially reducing both reproductive success and survival.

BEEtag: A Low-Cost, Image-Based Tracking System for the Study of Animal Behavior and Locomotion

A fundamental challenge common to studies of animal movement, behavior, and ecology is the collection of high-quality datasets on spatial positions of animals as they change through space and time. Recent innovations in tracking technology have allowed researchers to collect large and highly accurate datasets on animal spatiotemporal position while vastly decreasing the time and cost of collecting such data. One technique that is of particular relevance to the study of behavioral ecology involves tracking visual tags that can be uniquely identified in separate images or movie frames. These tags can be located within images that are visually complex, making them particularly well suited for longitudinal studies of animal behavior and movement in naturalistic environments. While several software packages have been developed that use computer vision to identify visual tags, these software packages are either (a) not optimized for identification of single tags, which is generally of the most interest for biologists, or (b) suffer from licensing issues, and therefore their use in the study of animal behavior has been limited. Here, we present BEEtag, an open-source, image-based tracking system in Matlab that allows for unique identification of individual animals or anatomical markers. The primary advantages of this system are that it (a) independently identifies animals or marked points in each frame of a video, limiting error propagation, (b) performs well in images with complex backgrounds, and (c) is low-cost. To validate the use of this tracking system in animal behavior, we mark and track individual bumblebees (Bombus impatiens) and recover individual patterns of space use and activity within the nest. Finally, we discuss the advantages and limitations of this software package and its application to the study of animal movement, behavior, and ecology.

Bumblebee flight performance in cluttered environments: effects of obstacle orientation, body size and acceleration.

ABSTRACT Locomotion through structurally complex environments is fundamental to the life history of most flying animals, and the costs associated with movement through clutter have important consequences for the ecology and evolution of volant taxa. However, few studies have directly investigated how flying animals navigate through cluttered environments, or examined which aspects of flight performance are most critical for this challenging task. Here, we examined how body size, acceleration and obstacle orientation affect the flight of bumblebees in an artificial, cluttered environment. Non-steady flight performance is often predicted to decrease with body size, as a result of a presumed reduction in acceleration capacity, but few empirical tests of this hypothesis have been performed in flying animals. We found that increased body size is associated with impaired flight performance (specifically transit time) in cluttered environments, but not with decreased peak accelerations. In addition, previous studies have shown that flying insects can produce higher accelerations along the lateral body axis, suggesting that if maneuvering is constrained by acceleration capacity, insects should perform better when maneuvering around objects laterally rather than vertically. Our data show that bumblebees do generate higher accelerations in the lateral direction, but we found no difference in their ability to pass through obstacle courses requiring lateral versus vertical maneuvering. In sum, our results suggest that acceleration capacity is not a primary determinant of flight performance in clutter, as is often assumed. Rather than being driven by the scaling of acceleration, we show that the reduced flight performance of larger bees in cluttered environments is driven by the allometry of both path sinuosity and mean flight speed. Specifically, differences in collision-avoidance behavior underlie much of the variation in flight performance across body size, with larger bees negotiating obstacles more cautiously. Thus, our results show that cluttered environments challenge the flight capacity of insects, but in surprising ways that emphasize the importance of behavioral and ecological context for understanding flight performance in complex environments. Highlighted Article: Large bumblebees exhibit impaired flight performance in cluttered environments compared with small bees; this is not due to the scaling of acceleration performance, however, and may be driven by the allometry of collision avoidance.

Hummingbird flight stability and control in freestream turbulent winds

ABSTRACT Airflow conditions close to the Earths surface are often complex, posing challenges to flight stability and control for volant taxa. Relatively little is known about how well flying animals can contend with complex, adverse air flows, or about the flight control mechanisms used by animals to mitigate wind disturbances. Several recent studies have examined flight in the unsteady von Kármán vortex streets that form behind cylinders, generating flow disturbances that are predictable in space and time; these structures are relatively rare in nature, because they occur only the immediate, downstream vicinity of an object. In contrast, freestream turbulence is characterized by rapid, unpredictable flow disturbances across a wide range of spatial and temporal scales, and is nearly ubiquitous in natural habitats. Hummingbirds are ideal organisms for studying the influence of freestream turbulence on flight, as they forage in a variety of aerial conditions and are powerful flyers. We filmed ruby-throated hummingbirds (Archilochus colubris) maintaining position at a feeder in laminar and strongly turbulent (intensity ∼15%) airflow environments within a wind tunnel and compared their mean kinematics of the head, body, tail and wing, as well as variability in these parameters. Hummingbirds exhibited remarkably stable head position and orientation in both smooth and turbulent flow while maintaining position at the feeder. However, the hummingbirds body was less stable in turbulent flow and appeared to be most sensitive to disturbances along the mediolateral axis, displaying large lateral accelerations, translations and rolling motions during flight. The hummingbirds mitigated these disturbances by increasing mean wing stroke amplitude and stroke plane angle, and by varying these parameters asymmetrically between the wings and from one stroke to the next. They also actively varied the orientation and fan angle of the tail, maintaining a larger mean fan angle when flying in turbulent flow; this may improve their passive stability, but probably incurs an energetic cost as a result of increased drag. Overall, we observed many of the same kinematic changes noted previously for hummingbirds flying in a von Kármán vortex street, but we also observed kinematic changes associated with high force production, similar to those seen during load-lifting or high-speed flight. These findings suggest that flight may be particularly costly in fully mixed, freestream turbulence, which is the flow condition that hummingbirds are likely to encounter most frequently in natural habitats. Summary: Hummingbirds are exceptional flyers that employ a combination of mean and transient flight control mechanisms to enable them to maintain flight in highly turbulent wind environments.

Foraging in an unsteady world: bumblebee flight performance in field-realistic turbulence

Natural environments are characterized by variable wind that can pose significant challenges for flying animals and robots. However, our understanding of the flow conditions that animals experience outdoors and how these impact flight performance remains limited. Here, we combine laboratory and field experiments to characterize wind conditions encountered by foraging bumblebees in outdoor environments and test the effects of these conditions on flight. We used radio-frequency tags to track foraging activity of uniquely identified bumblebee (Bombus impatiens) workers, while simultaneously recording local wind flows. Despite being subjected to a wide range of speeds and turbulence intensities, we find that bees do not avoid foraging in windy conditions. We then examined the impacts of turbulence on bumblebee flight in a wind tunnel. Rolling instabilities increased in turbulence, but only at higher wind speeds. Bees displayed higher mean wingbeat frequency and stroke amplitude in these conditions, as well as increased asymmetry in stroke amplitude—suggesting that bees employ an array of active responses to enable flight in turbulence, which may increase the energetic cost of flight. Our results provide the first direct evidence that moderate, environmentally relevant turbulence affects insect flight performance, and suggest that flying insects use diverse mechanisms to cope with these instabilities.

Social context modulates idiosyncrasy of behaviour in the gregarious cockroach Blaberus discoidalis

Individuals are different, but they can work together to perform adaptive collective behaviours. Despite emerging evidence that individual variation strongly affects group performance, it is less clear to what extent individual variation is modulated by participation in collective behaviour. We examined light avoidance (negative phototaxis) in the gregarious cockroach Blaberus discoidalis, in both solitary and group contexts. Cockroaches in groups exhibited idiosyncratic light-avoidance performance that persisted across days, with some individual cockroaches avoiding a light stimulus 75% of the time, and others avoiding the light just above chance (i.e. ∼50% of the time). These individual differences were robust to group composition. Surprisingly, these differences did not persist when individuals were tested in isolation, but returned when testing was once again done in groups. During the solo testing phase cockroaches exhibited individually consistent light-avoidance tendencies, but these differences were uncorrelated with performance in any group context. Therefore, we have observed not only that individual variation affects group-level performance, but also that whether or not a task is performed collectively can have a significant, predictable effect on how an individual behaves. That individual behavioural variation is modulated by whether a task is performed collectively has major implications for understanding variation in behaviours that are facultatively social, and it is essential that ethologists consider social context when evaluating individual behavioural differences.

Spatial fidelity of workers predicts collective response to disturbance in a social insect

Individuals in social insect colonies cooperate to perform collective work. While colonies often respond to changing environmental conditions by flexibly reallocating workers to different tasks, the factors determining which workers switch and why are not well understood. Here, we use an automated tracking system to continuously monitor nest behavior and foraging activity of uniquely identified workers from entire bumble bee (Bombus impatiens) colonies foraging in a natural outdoor environment. We show that most foraging is performed by a small number of workers and that the intensity and distribution of foraging is actively regulated at the colony level in response to forager removal. By analyzing worker nest behavior before and after forager removal, we show that spatial fidelity of workers within the nest generates uneven interaction with relevant localized information sources, and predicts which workers initiate foraging after disturbance. Our results highlight the importance of spatial fidelity for structuring information flow and regulating collective behavior in social insect colonies.How do social insect colonies regulate tasks after the developmental stage and in response to changing environments? Here, Crall et al. use automated individual tracking to reveal that task switching after a major colony disturbance helps to maintain collective foraging performance in bumble bees.