Many species carry out their most interesting activities where they cannot readily be observed or monitored. Marine mammals are extreme among this group, accomplishing their most astounding activities both distant from land and deep in the sea. Collection, storage and transmission of data about these activities are constrained by the energy requirements and size of the recording loggers and transmitters. The more bits of information collected, stored and transmitted, the more battery is required and the larger the tag must be. We therefore need to be selective about the information we collect, while maintaining detail and fidelity. To accomplish this in the study of marine mammals, we have designed “intelligent” data logger/transmitters that provide context-driven data compression, data relay, and automated data base storage. We later combine these data with remotely sensed environmental information and other oceanographic data sets to recreate the environmental context for the animal's activity, and we display the combined data using computer animation techniques. In this way, the system can provide near real time “observation” of animal behavior and physiology from the remotest parts of the globe.

Vertebrates show a diverse array of social behaviors associated with territoriality. Field and laboratory experiments indicate that underlying themes—including mechanisms—may exist. For example in birds, extensive evidence over many decades has implicated a role for testosterone in the activation of territorial aggression in reproductive contexts. Territoriality at other times of the year appeared to be independent of gonadal hormone control. One obvious question is—why this diversity of control mechanisms for an apparently similar behavior? Control of testosterone secretion during the breeding season must balance the need to compete with other males (that tends to increase testosterone secretion), and the need to provide parental care (that requires lower testosterone concentrations). Regulation of aggressive behaviors by testosterone in the non-breeding season may incur substantial costs. A series of experiments on the male song sparrow, Melospiza melodia morphna, of western Washington State have revealed possible mechanisms to avoid these costs. Song sparrows are sedentary and defend territories in both breeding and non-breeding seasons. Dominance interactions, territorial aggression and song during the non-breeding season are essentially identical to those during the breeding season. Although in the non-breeding season plasma testosterone and estradiol levels are very low, treatment with an aromatase inhibitor decreases aggression and simultaneous implantation of estradiol restores territorial behavior. These data suggest that the mechanism by which testosterone regulates territorial behavior at the neural level remains intact throughout the year. How the hormonal message to activate such behavior gets to the brain in different season does, however, appear to be different.

Stable isotopes are becoming an increasingly powerful tool for studying the physiological ecology of animals. The ¹³C/¹²C ratios of animal tissues are frequently used to reconstruct the diet of animals. This usually requires killing the subjects. While there is an extensive medical literature on measuring the ¹³C/¹²C ratio of exhaled CO₂ to determine substrate digestion and oxidation, we found little evidence that animal physiologists or physiological ecologists have applied ¹³C/¹²C breath analysis in their studies. The analysis breath ¹³C/¹²C ratios has the advantage of being non-invasive and non-destructive and can be repeatedly used on the same individual. Herein we briefly discuss the medical literature. We then discuss research which shows that, not only can the breath¹³C/¹²C ratio indicate what an animal is currently eating, but also the animal's diet in the past, and any changes in diet have occurred over time. We show that naturally occurring ¹³C/¹²C ratios in exhaled CO₂ provides quantitative measure of the relative contribution of carbohydrates and lipids to flight metabolism. This technique is ripe for application to field research, and we encourage physiological ecologists to add this technique to their toolbox.

Laboratory and field studies have demonstrated that the immune system is sensitive to environmental contaminants. Testing protocols have been developed to screen for immunotoxic effects and elucidate mechanisms of toxicity in laboratory rodents. Similar methods have been applied to wildlife species in captivity and the wild. Several epizootics in wildlife have been associated with elevated exposure to contaminants. This paper discusses immunotoxicological techniques used in studies of avian wildlife. Measurements of immunological structure include peripheral white blood cell counts and the mass and cellularity of immune organs such as the thymus, spleen, and bursa of Fabricius. While contaminants can alter these measures of immunological structure, such measures do not directly assess how the immune system functions, i.e., responds to specific challenges. The two most commonly used in vivo immune function tests in birds are the phytohemagglutinin (PHA) skin response for T cell-mediated immunity and the sheep red blood cell (SRBC) hemagglutination assay for antibody-mediated immunity. In vitro tests of immune function in avian wildlife include proliferation of lymphocytes in response to various mitogens and phagocytosis of fluorescent particles by monocytes. While optimization of in vitro techniques for wildlife species is often time-consuming, these assays usually require only a single blood sample and can elucidate mechanisms of toxicity. In immunological studies of wildlife, investigators should consider factors that may influence immune responses, including age, body condition, date, developmental stage of the immune system, and time required for the progression of immune responses.

I used three innovative, nondestructive field methods (gas dilution, doubly labeled water and radiography) to measure individual energy and water budgets of wild, female desert tortoises (Gopherus agassizii). With these budgets, I evaluated whether body reserves help females produce eggs independent of rainfall and food availability. Female desert tortoises used large seasonal and annual changes in metabolism and body water, protein and energy reserves to survive and produce eggs. Although lipid reserves are important to female desert tortoises, nitrogen or crude protein appears to be the primary limiting resource for producing eggs. By reducing metabolic rates 90%, females conserved enough body reserves to produce eggs during extreme drought conditions; this is an effective bet-hedging reproductive pattern in an extreme and unpredictable environment.

The flexible phenotypes of birds and mammals often appear to represent adjustments to alleviate some energetic bottleneck or another. By increasing the size of the organs involved in digestion and assimilation of nutrients (gut and liver), an individual bird can increase its ability to process nutrients, for example to quickly store fuel for onward flight. Similarly, an increase in the exercise organs (pectoral muscles and heart) enables a bird to increase its metabolic power for sustained flight or for thermoregulation. Reflecting the stationary cost of organ maintenance, changes in the size of any part of the “metabolic machinery” will be reflected in Basal Metabolic Rate (BMR) unless changes in metabolic intensity also occur. Energetic bottlenecks appear to be set by the marginal value of organ size increases relative to particular peak requirements (including safety factors). These points are elaborated using the studies on long-distance migrating shorebirds, especially red knots Calidris canutus. Red knots encounter energy expenditure levels similar to experimentally determined ceiling levels of ca. 5 times BMR in other birds and mammals, both during the breeding season on High Arctic tundra (probably mainly a function of costs of thermoregulation) and during winter in temperate coastal wetlands (a function of the high costs of processing mollusks, prey poor in nutrients but rich in shell material and salt water). During migration, red knots phenotypically alternate between a “fueling [life-cycle] stage” and a “flight stage.” Fueling red knots in tropical areas may encounter heat load problems whilst still on the ground, but high flight altitudes during migratory flights seem to take care of overheating and unacceptably high rates of evaporative water loss. The allocation principles for the flexible phenotypes of red knots and other birds, the costs of their organ flexibility and the ways in which they “organize” all the fast phenotypic changes, are yet to be discovered.

The adaptive significance of mechanisms of energy and water conservation among species of desert rodents, which avoid temperature extremes by remaining within a burrow during the day, is well established. Conventional wisdom holds that arid-zone birds, diurnal organisms that endure the brunt of their environment, occupy these desert climates because of the possession of physiological design features common to all within the class Aves. We review studies that show that desert birds may have evolved specific features to deal with hot desert conditions including: a reduced basal metabolic rate (BMR) and field metabolic rate (FMR), and lower total evaporative water loss (TEWL) and water turnover (WTO).

Previous work on the comparative physiology of desert birds relied primarily on information gathered on species from the deserts of the southwestern U.S., which are semi-arid habitats of recent geologic origin. We include data on species from Old World deserts, which are geologically older than those in the New World, and place physiological responses along an aridity axis that includes mesic, semi-arid, arid, and hyperarid environments.

The physiological differences between desert and mesic birds that we have identified using the comparative method could arise as a result of acclimation to different environments, of genetic change mediated by selection, or both. We present data on the flexibility of BMR and TEWL in Hoopoe Larks that suggest that phenotypic adjustments in these variables can be substantial. Finally, we suggest that linkages between the physiology of individual organism and its life-history are fundamental to the understanding of life-history evolution.

Animals must make “decisions” (e.g., when or whether to breed, the effort to put into a breeding episode) by integrating physiological, environmental and social inputs. This integration can be studied only in a field context. In Adélie penguins (Pygoscelis adeliae) reproduction is constrained by foraging ecology, mode of transport, and the extreme latitude at which they live. The decision whether to breed in a given year is influenced by body conditions. Adélie penguins must fast for several weeks during the early reproductive stages and use stored fat for metabolic energy. Females that return to the colony, but do not breed, are 10–12% lighter than females that do breed. Birds that are relatively low in body mass tend to have lower reproductive success than heavier birds, and an individual's reproductive success is positively correlated with the body fat stores it had on arrival. After eggs are laid, parents alternate in attending the nest. Nest failure occurs if one parent does not make a timely return and its fasting partner must eventually leave. During normal-length fasts plasma corticosterone and glucose levels do not change. Blood β-hydroxybutyrate levels gradually increase during the fast while uric acid levels remain low, but in birds with the longest fasts (>∼50 days), ketone levels may fall and uric acid levels increase, indicative of a switch from using fat to using body proteins for metabolism. In incubating males, hematocrit and hemoglobin concentrations also increase, suggesting dehydration can accompany energy stress during the breeding fast.

The morphological designs of animals represent a balance between stability for efficient locomotion and instability associated with maneuverability. Morphologies that deviate from designs associated with stability are highly maneuverable. Major features affecting maneuverability are positions of control surfaces and flexibility of the body. Within odontocete cetaceans (i.e., toothed whales), variation in body design affects stability and turning performance. Position of control surfaces (i.e., flippers, fin, flukes, peduncle) provides a generally stable design with respect to an arrow model. Destabilizing forces generated during swimming are balanced by dynamic stabilization due to the phase relationships of various body components. Cetaceans with flexible bodies and mobile flippers are able to turn tightly at low turning rates, whereas fast-swimming cetaceans with less flexibility and relatively immobile flippers sacrifice small turn radii for higher turning rates. In cetaceans, body and control surface mobility and placement appear to be associated with prey type and habitat. Flexibility and slow, precise maneuvering are found in cetaceans that inhabit more complex habitats, whereas high-speed maneuvers are used by cetaceans in the pelagic environment.

Perturbations vary in period and amplitude, and responses to unavoidable perturbations depend on response time and scale. Disturbances due to unavoidable perturbations occur in three translational planes and three rotational axes during forwards and backwards swimming. Stability depends on hydrodynamic damping and correcting forces, which may be generated by propulsors (powered) or by control surfaces moving with the body (trimming). Hydrostatic forces affecting body orientation (posture) result in negative metacentric heights amplifying rolling disturbances. The ability to counteract perturbations and correct disturbances is greater for fishes with more slender bodies, which appears to affect habitat choices. Postural control problems are greatest at low speeds, and are avoided by some fishes by sitting on the bottom. In currents, body form and behavior affect lift, drag, weight, and friction and hence speeds to which posture can be controlled. Self-correcting and regulated damping and trimming mechanisms are most important in stabilizing swimming trajectories. Body resistance, fin trajectory, multiple propulsors, and long-based fins damp self-generated locomotor disturbances. Powered control using the tail evolved early in chordates, and is retained by most groups, although fishes, especially acanthopterygians, make greater use of appendages. As with most areas of stability, little is known of control costs. Costs and benefits of low-density inclusions and hydrodynamic mechanisms for depth control vary with habits and habitats. Control may make substantial contributions to energy budgets.

The understanding of fish maneuvering and its application to underwater rigid bodies are considered. The goal is to gain insight into stealth. The recent progress made in NUWC is reviewed. Fish morphology suggests that control fins for maneuverability have unique scalar relationships irrespective of their speed type. Maneuvering experiments are carried out with fish that are fast yet maneuverable. The gap in maneuverability between fish and small underwater vehicles is quantified. The hydrodynamics of a dorsal fin based brisk maneuvering device and a dual flapping foil device, as applied to rigid cylindrical bodies, are described. The role of pectoral wings in maneuvering and station keeping near surface waves is discussed. A pendulum model of dolphin swimming is presented to show that body length and tail flapping frequency are related. For nearly neutrally buoyant bodies, Froude number and maneuverability are related. Analysis of measurements indicates that the Strouhal number of dolphins is a constant. The mechanism of discrete and deterministic vortex shedding from oscillating control surfaces has the property of large amplitude unsteady forcing and an exquisite phase dependence, which makes it inherently amenable to active control for precision maneuvering. Theoretical control studies are carried out to demonstrate the feasibility of maneuverability of biologically inspired bodies under surface waves. The application of fish hydrodynamics to the silencing of propulsors is considered. Two strategies for the reduction of radiated noise are developed. The effects of a reduction of rotational rate are modeled. The active cambering of blades made of digitally programmable artificial muscles, and their thrust enhancement, are demonstrated. Next, wake momentum filling is carried out by artificial muscles at the trailing edge of a stator blade of an upstream stator propulsor, and articulating them like a fish tail. A reduction of radiated noise, called blade tonals, is demonstrated theoretically.

The Draper Laboratory Vorticity Control Unmanned Undersea Vehicle (VCUUV) is the first mission-scale, autonomous underwater vehicle that uses vorticity control propulsion and maneuvering. Built as a research platform with which to study the energetics and maneuvering performance of fish-swimming propulsion, the VCUUV is a self-contained free swimming research vehicle which follows the morphology and kinematics of a yellowfin tuna. The forward half of the vehicle is comprised of a rigid hull which houses batteries, electronics, ballast and hydraulic power unit. The aft section is a freely flooded articulated robot tail which is terminated with a lunate caudal fin. Utilizing experimentally optimized body and tail kinematics from the MIT RoboTuna, the VCUUV has demonstrated stable steady swimming speeds up to 1.2 m/sec and aggressive maneuvering trajectories with turning rates up to 75 degrees per second. This paper summarizes the vehicle maneuvering and stability performance observed in field trials and compares the results to predicted performance using theoretical and empirical techniques.

The dictionary definition of stability as “Firmly established, not easily to be changed” immediately indicates the conflict between stability and maneuverability in aquatic locomotion. The present paper addresses several issues resulting from these opposing requirements. Classical stability theory for bodies moving in fluids is based on developments in submarine and airship motions. These have lateral symmetry, in common with most animals. This enables the separation of the equations of motion into two sets of 3 each. The vertical (longitudinal) set, which includes motions in the axial (surge), normal (heave) and pitching directions, can thus be separated from the lateral-horizontal plane which includes yaw, roll and sideslip motions. This has been found useful in the past for longitudinal stability studies based on coasting configurations but is not applicable to the analysis of turning, fast starts and vigorous swimming, where the lateral symmetry of the fish body is broken by bending motions. The present paper will also examine some of the aspects of the stability vs. maneuverability tradeoff for these asymmetric motions. An analysis of the conditions under which the separation of equations of motions into vertical and horizontal planes is justified, and a definition of the equations to be used in cases where this separation is not accurate enough is presented.

Accelerations and directional changes of flying animals derive from interactions between aerodynamic force production and the inertial resistance of the body to translation and rotation. Anatomical and allometric features of body design thus mediate the rapidity of aerial maneuvers. Both translational and rotational responsiveness of the body to applied force decrease with increased total mass. For flying vertebrates, contributions of the relatively heavy wings to whole-body rotational inertia are substantial, whereas the relatively light wings of many insect taxa suggest that rotational inertia is dominated by the contributions of body segments. In some circumstances, inertial features of wing design may be as significant as are their aerodynamic properties in influencing the rapidity of body rotations. Stability in flight requires force and moment balances that are usually attained via bilateral symmetry in wingbeat kinematics, whereas body roll and yaw derive from bilaterally asymmetric movements of both axial and appendicular structures. In many flying vertebrates, use of the tail facilitates the generation of aerodynamic torques and substantially enhances quickness of body rotation. Geometrical constraints on wingbeat kinematics may limit total force production and thus accelerational capacity in certain behavioral circumstances. Unitary limits to animal flight performance and maneuverability are unlikely, however, given varied and context-specific interactions among anatomical, biomechanical, and energetic features of design.

While useful in describing the efficiency of maneuvering flight, steady-state (i.e., fixed wing) models of maneuvering performance cannot provide insight to the efficacy of maneuvering, particularly during low-speed flapping flight. Contrasted with airplane-analogous gliding/high speed maneuvering, the aerodynamic and biomechanical mechanisms employed by birds at low flight speeds are violent, with rapidly alternating forces routinely being developed. The saltatory nature of this type of flight results in extreme linear and angular displacements of the bird's body; however, birds isolate their heads from these accelerations with cervical reflexes. Experiments with pigeons suggest this ability to isolate the visual and vestibular systems is critical to controlled flapping flight: birds wearing collars that prohibited the neck from isolating the head from the angular accelerations of induced rolls frequently exhibited (50% of flights) a loss of vestibular and/or visual horizon and were unable to maintain controlled flight.

Animals can swerve, dodge, dive, climb, turn and stop abruptly. Their stability and maneuverability are remarkable, but a challenge to quantify. Formal stability analysis can allow for quantitative comparisons within and among species. Stability analysis used in concert with a template (a simple, general model that serves as a guide for control) can lead to testable hypotheses of function. Neural control models postulated without knowledge of the animal's mechanical (musculo-skeletal) system can be counterproductive and even destabilizing. Perturbations actively corrected by reflex feedback in one direction can result in perturbations in other directions because the system is coupled dynamically. The passive rate of recovery from a perturbation in one direction differs from rates in other directions. We hypothesize that animals might exert less neural control in directions that rapidly recover via passive dynamics (e.g., in body orientation and rotation). By contrast, animals are likely to exert more neural control in directions that recover slowly or not at all via passive dynamics (e.g., forward velocity and heading). Neural control best enhances stability when it works with the natural, passive dynamics of the mechanical system. Measuring maneuverability is more challenging and new, general metrics are needed. Templates reveal that simple analyses of summed forces and quantification of the center of pressure can lead to valuable hypotheses, whereas kinematic descriptions may be inadequate. The study of stability and maneuverability has direct relevance to the behavior and ecology of animals, but is also critical if animal design is to be understood. Animals appear to be grossly over-built for steady-state, straight-ahead locomotion, as they appear to possess too many neurons, muscles, joints and even too many appendages. The next step in animal locomotion is to subject animals to perturbations and reveal the function of all their parts.

For a standing animal to be statically stable, a vertical line through its centre of mass must pass through the polygon of support defined by its feet. Statically stable gaits are possible for quadrupeds but do not seem to be used. Physical and mathematical models have shown that bipedal gaits can be dynamically stable. Accelerations and decelerations of animals may be limited by muscle strength, by the coefficient of friction with the ground or by considerations of stability. Cornering ability similarly may be limited by strength or by the coefficient of friction. It may be faster to use a longer route involving corners of larger radius than a shorter one with sharper corners.

In the experiments stick insects walk on an inclined substrate such that the legs of one side of the body point uphill and the legs of the other side point downhill. In this situation the vertical axis of the body is rotated against the inclination of the substrate as if to compensate for the effect of substrate inclination. A very small effect has been found when the experiment was performed with animals standing on a tilted platform which shows that the effect depends on the behavioral context. When, however, animals first walked along the inclined surface and then, before measurement, stopped walking spontaneously, a rotation of the body has been observed similar to that in walking animals. In a second experiment it was tested whether the observed body rotation is caused by the change of direction of gravity vector or by the fact that on an inclined surface gravity necessarily has a component pulling the body sideways. Experiments with animals standing on horizontal ground and additional weights applied pulling the body to the side showed similar body rotations supporting the latter idea. In a simulation study it could be shown that the combined activity of proportional feedback controllers in the leg joints is sufficient to explain the observed behavior. This is however only possible if the gain factors of coxa-trochanter joint controller and of femur-tibia joint controller show a ratio in the order of 1 : 0.05 to 1 : 1.8. In order to describe the behavior of animals standing on a tilted platform, a ratio of 1 : 1.7 is necessary. In walking animals, this body rotation requires to change the trajectories of stance and swing movements. The latter have been studied in more detail. During swing, the femur-tibia joint is more extended in the uphill legs. Conversely, the coxa-trochanter joint appears to be more elevated in the downhill legs which compensates the smaller lift in the femur-tibia joint. The results are discussed in the context of different hypotheses.

For both historical and technological reasons, most robots, including those meant to mimic animals or operate in natural environments,³ use actuators and control systems that have high (stiff) mechanical impedance. By contrast, most animals exhibit low (soft) impedance. While a robot's stiff joints may be programmed to closely imitate the recorded motion of an animal's soft joints, any unexpected position disturbances will generate reactive forces and torques much higher for the robot than for the animal. The dual of this is also true: while an animal will react to a force disturbance by significantly yielding position, a typical robot will greatly resist.

These differences cause three deleterious effects for high impedance robots. First, the higher forces may cause damage to the robot or to its environment (which is particularly important if that environment includes people). Second, the robot must acquire very precise information about its position relative to the environment so as to minimize its velocity upon impact. Third, many of the self-stabilizing effects of natural dynamics are “shorted out”⁴ by the robot's high impedance, so that stabilization requires more effort from the control system.

Over the past 5 yr, our laboratory has designed a series of walking robots based on “Series-Elastic Actuators” and “Virtual Model Control.” Using these two techniques, we have been able to build low-impedance walking robots that are both safe and robust, that operate blindly without any model of upcoming terrain, and that add minimal control effort in parallel to their self-stabilizing passive dynamics. We have discovered that it is possible to achieve surprisingly effective ambulation from rather simple mechanisms and control systems. After describing the historical and technological motivations for our approach, this paper gives an overview of our methods and shows some of the results we have obtained.