Virtual Issue: Locomotion unplugged: how movement in animals is influenced by the environment

Duncan J Irschick and Tim Higham

Locomotion is a vital activity for organisms to escape predators, reproduce, and feed, among other activities. In short, ecology and locomotion are intimately intertwined. For much of the past century, locomotion has been primarily studied under controlled laboratory conditions, with an emphasis on mechanistic studies of muscle anatomy and biomechanics. Over the past 20 years, however, the rise of novel field-portable technologies such as accelerometers, high-speed video cameras, satellite tags and movement sensors, has enabled researchers to literally take the “laboratory” into the “field”. While laboratory studies of locomotion continue to play a vital role in the realm of biomechanics and functional morphology, a new and exciting paradigm for studying locomotion has arisen that complements this existing paradigm. This new perspective focuses on studying locomotion in natural settings, and aims to understand both locomotor performance (e.g., speed, acceleration) and general movement patterns in relation to both micro- and macro ecological factors. This contextualization of locomotion will facilitate a broader understanding of what underlies phenotypic diversity.

Movement ecology has emerged over the last decade as one of the fastest-growing areas in ecology. The growth of technologies designed to detect movement, such as satellite tags and accelerometers has enabled researchers to track animals over vast distances. This has enabled researchers to ask questions regarding which factors influence these movement patterns in increasing detail. One example comes from studies of tiger sharks (Galeocerdo cuvier), which migrate long distances in the Atlantic ocean (>1000 km), and recent satellite tracking studies reveal that despite differences in human disturbance between Florida (where baited dives are illegal) and the Bahamas (where baited dives are widely practiced), there appear to be no differences in migration patterns between sharks that emanate from the two regions (Hammerschlag et al. 2012). These remote technologies enable researchers to not just understand broad scale-movement patterns, but also gain fine-scale data on how animals move. New developments in estimating movement speeds and accelerations now enable researchers to estimate energetic expenditure, such as in recent studies of turtles (Fossettee et al. 2012). By understanding more clearly the energetic limitations and costs of these extensive migrations, researchers can begin to understand the intrinsic and extrinsic factors that may be regulating how far, and in which manner, animals move. The broad panorama of movement ecology exists not only for aquatic animals, but also for terrestrial animals. Large animals such as elephants can be ecosystem engineers because of their profound impact on habitat structure. However, until recently, researchers have not fully appreciated the amount of variation among individuals in how they move, or the factors that might explain these differences. However, recent work by Jachowski et al. (2013) show how physiological differences among individual African elephants can predict movement patterns. This suggests that a monomorphic view of these large animals may be misguided, and a greater attention to individual-based ecology may reveal how some individual animals can greatly impact habitats whereas other individuals have relatively little influence.

As highlighted above in the work by Jachowski et al. (2013), individual variation is a rich source for scientific discovery as it allows researchers to isolate the factors that drive differences in locomotion. With a focus on consistent individual differences, or personalities, Galliard et al. (2013) determined whether exploratory behavior of newborn lizards correlated with locomotor traits and metabolic rate. Surprisingly, they found no correlation between resting metabolic rate and exploratory behavior. However, there was a weak correlation between locomotor performance and exploratory behavior, which is likely related to a combined effect of developmental history and natural selection, rather than differences in motivation, physiology or morphology. In addition to exploratory behavior, individuals can vary in a number of other traits, such as the amount of exercise in which they engage. We know that exercise has a profound impact on morphology and physiology, but few attempts have been made to examine the consequences of ecologically relevant variation in exercise. Why would individuals vary in their level of exercise? As noted by Sinclair et al. (2013), a source of variation lies in the existence of behavioral phenotypes, or personalities. Ecological pressures might, in part, determine these personalities, and consequently the level of exercise. For example, living in fast flowing streams may result in increased levels of exercise in fishes relative to those living in slow moving streams. Sinclair et al. (2013) found that increased exercise in mosquitofish led to increased swimming performance, boldness, tendency to explore, and aggression. They conclude that personality is labile within individuals, such that differences in personality may stem from abiotic impacts from the environment (e.g. flow velocity in a stream). If these abiotic factors change, then personality may also change. This exciting area of research highlights the intimate link between ecology and locomotion, and suggests that ecology not only impacts locomotion, but also that locomotion impacts ecology.

Different aspects of habitat structure can impact locomotion both directly and indirectly, and how animals cope with these effects is often crucial for survival and effective reproduction. While animals of all sizes are impacted by structural features of the environment, this concept is most easily studied at a finer scale with smaller and more abundant animals that can be easily observed and manipulated. Unlike terrestrial animals, arboreal animals occur in a world which bends, weaves and bobs, yet the compliance of these substrates, and how they impact movement is beginning to be become more clearly understood. In arboreal green anoles (Anolis carolinensis), highly compliant branches impair locomotion by impacting both the angle that these lizards can jump from, and therefore the distances of their jumps (Gilman et al. 2013). These lizards therefore make choices about which substrates they choose to move, and the nature of their movement (e.g., jumping, running). As with anoles, Chameleons are known to move effectively in arboreal habitats due to their zygodactylous feet and prehensile tail, each of which is highly specialized for moving on narrow and complaint surfaces. Integrative research with chameleons reveals the complex nature by which the habitat influences locomotion in these species (Da Silva et al. 2013), and shows that these animals choose habitats which most obviously improves their ability to move in nature.

While field studies are critical for understanding the ecological context of locomotion, laboratory studies are a crucial complement for untangling the mechanistic bases of variation in locomotor ability. This statement is especially true for locomotion that is mechanically or energetically challenging. For example, flight is energetically expensive, especially for larger animals, and among flying animals, hummingbirds are renowned for their exceptional flying capacities. Anyone who has watched a hummingbird has likely wondered how they can obtain sufficient fuel to maintain flight. Can hummingbirds fuel their flight with food reserves, or can they fly “empty”, and gain sufficient nectar during foraging to stay aloft? Recent research by Chen and Welch (2013) show that hummingbirds can fuel locomotion entirely with exogenous sources, which suggests little need to build up fuel reserves prior to foraging. This shows how fuel reserves may be less important to some animals than others, but it also suggests very strong selection on efficiency during foraging in these animals.

Another form of highly challenging movement is rapid bursts of movement, such as jumping. While not energetically expensive, such movements are nonetheless mechanically challenging. Many animals, especially insects, employ special “tricks” to enhance these dynamic movements, such as through spring-like mechanisms in which elastic energy is stored slowly, and then released quickly, much like a catapult. The advantage of this method is that the energetic cost of producing the movement is minimized as the energy put into storage is expressed slowly, yet the locomotor output can have dramatic and positive fitness consequences, such as in the cast of jumping in click beetles, which is accomplished through storage of elastic elements in the wings, that are then “clicked” and released, therefore enabling rapid movements that can aid in escaping predators (Ribak et al. 2012). Locomotion is controlled in large part by variation in body form and the scaling of morphology. Whereas most scaling studies have been conducted on smaller animals, it is in the largest animals in the world, whales, in which scaling effects seem most apparent. As in any hydrodynamic system, scaling of body parts used for feeding impacts greatly how smaller whales and larger whales can consume food items, and recent research by Goldbogen et al. (2012) underscores this point. Larger whales seem to sacrifice locomotion for feeding by scaling to extremely large head sizes, which enables them to likely obtain larger food inputs (because of their proportionally large head). This ontogenetic shift makes sense, given that the amount of food needed to fuel movement in large whales is significant. In most animals, locomotion is driven by muscles and this raises the question of how animals maximize neuromuscular effort. For humans, exercise is essential for maximizing muscular performance, but for many wild animals that live naturally on a dietary tightrope, the role of exercise is less obvious. Indeed, research on some lizard’s reveals that strenuous exercise in a laboratory setting can result in either no change in aerobic capacity at all, or even in limb pathologies. However, in an interesting recent study, it was found that exercise changes behavior in fish. In a manner similar to humans, exercised fish were bolder and performed riskier behaviors. While the underlying mechanism remains poorly understood, it is possible that hormonal shifts as a result of exercise may play a role.

The assumption that morphology and performance are directly linked has persisted for a long time. In many cases morphological features enhance locomotion, such as increased leg length for increased sprint speed in terrestrial vertebrates. However, sexual selection often results in the exaggeration of morphological structures, potentially leading to trade-off with locomotor performance. A great example of this is the sword (elongated lower margin of the caudal fin) of some species of Xiphophorus fishes. The female preference for longer swords results in the elongated sword in males, but the degree of preference varies between species. Oufiero et al (in press) examined whether the presence of an enlarged sword depresses locomotor performance by using a species that naturally lacks a sword, two species with elongated swords, and one treatment with experimentally reduced sword length. Surprisingly, sword length did not impact locomotor performance, suggesting that some sexually selected locomotor traits may not be detrimental to locomotion. Ecologically relevant manipulation of morphology provides a valuable tool for examining the ecology of locomotion.

References

Chen, C. C. W., Welch, K. C., 2013.Hummingbirds can fuel expensive hovering flight completely with either exogenous glucose or fructose. Functional Ecology DOI: 10.1111/1365-2435.12202

Da Silva, J. M., Herrel, A., Measey, J. G., Vanhooydonck, B., Tolley, K. A. 2014. Linking microhabitat structure, morphology and locomotor performance traits in a recent radiation of dwarf chameleons. Functional Ecology DOI: 10.1111/1365-2435.12210

Fossette, S., Schofield, G., Lilley, K. S. M., Gleiss, A. C., Hays, G. C. 2012. Acceleration data reveal the energy management strategy of a marine ectotherm during reproduction. Functional Ecology 26:324-333.

Gilman, C., Irschick D. J. 2013. Foils of flexion: the effects of perch compliance on lizard locomotion and perch choice in the wild. Functional Ecology 27:374-381.

Goldbogen, J. A., Calambokidis, Croll, D. A., McKenna, M. F., Oleson, E., Potyin, J., Pyenson, D., Schorr, G., Shadwick, R. W., Tershy, B. 2011. Scaling of lunge-feeding performance in rorqual whales: mass-specific energy expenditure increases with body size and progressively limits diving capacity. Functional Ecology 26:216-226.

Hammerschlag, N., Gallagher, A. J., Wester, J., Luo, J., Ault, J. S. 2012. Don’t bite the hand that feeds: assessing ecological impacts of provisioning ecotourism on an apex marine predator. Functional Ecology. 26:567-576.

Jachowski, D. S., Montgomery, R. A., Slotow, R., Millspaugh, J. J. 2013. Unravelling complex associations between physiological state and movement of African elephants. Functional Ecology 27:1166-1175.

Le Galliard, J. F. Paquet, M., Cisel, M., Montes-Poloni, L. 2013. Personality and the pace-of-life syndrome: variation and selection on exploration, metabolism and locomotor performances. Functional Ecology 27:136-144.

Oufiero, C., Jugo, K., Garland T. Jr. 2014. Swimming with a sword: tail beat kinematics in relation to sword length in Xiphophorus. Functional Ecology DOI: 10.1111/1365-2435.12222

Sinclair, E. L. E., Noronha de Souza, C. R., Ward, A. J. W., Seebacher, F. 2013. Exercise changes behaviour. Functional Ecology DOI: 10.1111/1365-2435.12198

Ribak, G., Reingold, S., Weihs, D. 2011. The effect of natural substrates on jump height in click-beetles. Functional Ecology 26:493-499.

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