Individual variation and the biomechanics of maneuvering flight in hummingbirds.

An animal's maneuverability will determine the outcome of many of its most important interactions. A common approach to studying maneuverability is to force the animal to perform a specific maneuver or to try to elicit maximal performance. Recently, the availability of wider-field tracking technology has allowed for high-throughput measurements of voluntary behavior, an approach that produces large volumes of data. Here, we show how these data allow for measures of inter-individual variation that are necessary to evaluate how performance depends on other traits, both within and among species. We use simulated data to illustrate best practices when sampling a large number of voluntary maneuvers. Our results show how the sample average can be the best measure of inter-individual variation, whereas the sample maximum is neither repeatable nor a useful metric of the true variation among individuals. Our studies with flying hummingbirds reveal that their maneuvers fall into three major categories: simple translations, simple rotations and complex turns. Simple maneuvers are largely governed by distinct morphological and/or physiological traits. Complex turns involve both translations and rotations, and are more subject to inter-individual differences that are not explained by morphology. This three-part framework suggests that different wingbeat kinematics can be used to maximize specific aspects of maneuverability. Thus, a broad explanatory framework has emerged for interpreting hummingbird maneuverability. This framework is general enough to be applied to other types of locomotion, and informative enough to explain mechanisms of maneuverability that could be applied to both animals and bio-inspired robots.

Lunge filter feeding biomechanics constrain rorqual foraging ecology across scale.

Fundamental scaling relationships influence the physiology of vital rates, which in turn shape the ecology and evolution of organisms. For diving mammals, benefits conferred by large body size include reduced transport costs and enhanced breath-holding capacity, thereby increasing overall foraging efficiency. Rorqual whales feed by engulfing a large mass of prey-laden water at high speed and filtering it through baleen plates. However, as engulfment capacity increases with body length (engulfment volume∝body length3.57), the surface area of the baleen filter does not increase proportionally (baleen area∝body length1.82), and thus the filtration time of larger rorquals predictably increases as the baleen surface area must filter a disproportionally large amount of water. We predicted that filtration time should scale with body length to the power of 1.75 (filter time∝body length1.75). We tested this hypothesis on four rorqual species using multi-sensor tags with corresponding unoccupied aircraft systems-based body length estimates. We found that filter time scales with body length to the power of 1.79 (95% CI: 1.61-1.97). This result highlights a scale-dependent trade-off between engulfment capacity and baleen area that creates a biomechanical constraint to foraging through increased filtration time. Consequently, larger whales must target high-density prey patches commensurate to the gulp size to meet their increased energetic demands. If these optimal patches are absent, larger rorquals may experience reduced foraging efficiency compared with smaller whales if they do not match their engulfment capacity to the size of targeted prey aggregations.

Why whales are big but not bigger: Physiological drivers and ecological limits in the age of ocean giants.

The largest animals are marine filter feeders, but the underlying mechanism of their large size remains unexplained. We measured feeding performance and prey quality to demonstrate how whale gigantism is driven by the interplay of prey abundance and harvesting mechanisms that increase prey capture rates and energy intake. The foraging efficiency of toothed whales that feed on single prey is constrained by the abundance of large prey, whereas filter-feeding baleen whales seasonally exploit vast swarms of small prey at high efficiencies. Given temporally and spatially aggregated prey, filter feeding provides an evolutionary pathway to extremes in body size that are not available to lineages that must feed on one prey at a time. Maximum size in filter feeders is likely constrained by prey availability across space and time.

Body Flexibility Enhances Maneuverability in the World's Largest Predator.

Blue whales are often characterized as highly stable, open-ocean swimmers who sacrifice maneuverability for long-distance cruising performance. However, recent studies have revealed that blue whales actually exhibit surprisingly complex underwater behaviors, yet little is known about the performance and control of these maneuvers. Here, we use multi-sensor biologgers equipped with cameras to quantify the locomotor dynamics and the movement of the control surfaces used by foraging blue whales. Our results revealed that simple maneuvers (rolls, turns, and pitch changes) are performed using distinct combinations of control and power provided by the flippers, the flukes, and bending of the body, while complex trajectories are structured by combining sequences of simple maneuvers. Furthermore, blue whales improve their turning performance by using complex banked turns to take advantage of their substantial dorso-ventral flexibility. These results illustrate the important role body flexibility plays in enhancing control and performance of maneuvers, even in the largest of animals. The use of the body to supplement the performance of the hydrodynamically active surfaces may represent a new mechanism in the control of aquatic locomotion.

Using Digital Tags With Integrated Video and Inertial Sensors to Study Moving Morphology and Associated Function in Large Aquatic Vertebrates.

The anatomy of large cetaceans has been well documented, mostly through dissection of dead specimens. However, the difficulty of studying the world's largest animals in their natural environment means the functions of anatomical structures must be inferred. Recently, non-invasive tracking devices have been developed that measure body position and orientation, thereby enabling the detailed reconstruction of underwater trajectories. The addition of cameras to the whale-borne tags allows the sensor data to be matched with real-time observations of how whales use their morphological structures, such as flukes, flippers, feeding apparatuses, and blowholes for the physiological functions of locomotion, feeding, and breathing. Here, we describe a new tag design with integrated video and inertial sensors and how it can be used to provide insights to the function of whale anatomy. This technology has the potential to facilitate a wide range of discoveries and comparative studies, but many challenges remain to increase the resolution and applicability of the data. Anat Rec, 300:1935-1941, 2017. © 2017 Wiley Periodicals, Inc.

How Baleen Whales Feed: The Biomechanics of Engulfment and Filtration.

Baleen whales are gigantic obligate filter feeders that exploit aggregations of small-bodied prey in littoral, epipelagic, and mesopelagic ecosystems. At the extreme of maximum body size observed among mammals, baleen whales exhibit a unique combination of high overall energetic demands and low mass-specific metabolic rates. As a result, most baleen whale species have evolved filter-feeding mechanisms and foraging strategies that take advantage of seasonally abundant yet patchily and ephemerally distributed prey resources. New methodologies consisting of multi-sensor tags, active acoustic prey mapping, and hydrodynamic modeling have revolutionized our ability to study the physiology and ecology of baleen whale feeding mechanisms. Here, we review the current state of the field by exploring several hypotheses that aim to explain how baleen whales feed. Despite significant advances, major questions remain about the processes that underlie these extreme feeding mechanisms, which enabled the evolution of the largest animals of all time.