Bridging the gap as biomechanics, energetics and ecology unite

Focusing on some of the largest mammals in the ocean, Jeremy Goldbogen and David Cade (Stanford University, USA), review the lessons that have been learned about the novel and energy efficient feeding strategies of rorqual whales by temporarily attaching motion sensors to the animals (jeb247875). Lunge feeding allows massive blue whales (∼25 m) to engulf colossal mouthfuls of water, before extracting the entrapped prey, permitting these creatures to feed on dense patches of krill. In contrast, smaller, more agile rorquals, such as minke whales (∼7 m) are capable of targeting and outmanoeuvring individual fish. Intermediate sized rorquals, including humpback whales and Bryde's whales, have evolved alternative strategies that involve corralling fish in bubble nets and side-rolling on the sea floor to capture fish. The authors discuss how integrating information from high-resolution movement and video sensors attached to whales with knowledge about prey from fisheries sonar, coupled with lab-based studies of prey behaviours and biomechanical models of the energetic consequences of lunge filter feeding, are allowing us to understand better the delicate ecological balance between the behemoths of the ocean and their miniscule prey.

Changing scale to focus on the manoeuvres of fish, James Liao (University of Florida, USA) advocates for a shift in laboratory experiments to adopt a more ecologically relevant approach. Over the past 30 years, lab-based studies of fishes swimming in smoothly flowing water have revealed the fundamental fluid mechanics that underpins all fish locomotion. However, Liao and colleagues have recently begun to recreate the natural water flows that fish experience in the wild by positioning objects, including cylinders, in flowing water to simulate the impact of rocks, vegetation, and corals in rivers, lakes and oceans (jeb248011). He and his colleagues have also adapted large outdoor tanks supplied with fresh seawater to assess the natural swimming behaviour of wild fish, including during pursuit of prey. Recent advances in tracking – where globally distributed acoustic receivers pick up acoustic tags carried by fish – have also revealed details of their migration patterns. Liao hopes that this shift to learn more about the movements of animals in the wild will help biomechanists to see ‘habitat as drivers of locomotion, behaviour and migration, not just variables that affect movement mechanics’, he says.

Valentina Di Santo (Scripps Institution of Oceanography, USA) and Elsa Goerig (Harvard University, USA) expand on the theme of fish manoeuvring in their environments by reviewing the numerous energy conserving strategies used by fish naturally (jeb247918). They describe how Argentine sea bass save energy at night by listing when resting in caves and how other fish conserve energy by walking on their fins on the sea floor, allowing them to maintain stability in slow flowing water with little exertion. Fish can also take advantage of water flows created by natural structures and grey reef sharks surf incoming tides to conserve energy. In addition, remoras cling onto larger animals with a suction disk to hitch lifts, and lampreys and waterfall-climbing gobies use suckers to hold themselves in place when resting while journeying upstream. Di Santo and Goerig point out that understanding how fish interact with their environment is essential if we are to conserve environments effectively and preserve features that provide essential habitat niches for aquatic species.

Within the oceans, delicate gelatinous zooplankton form the largest group of animals, yet little is known about the movement and lifestyles of these extraordinary creatures. Brad Gemmell (University of South Florida, USA), Sean Colin (Roger Williams University, USA) and John Costello (Providence College, USA) discuss recent successes tracking these semi-transparent creatures in the wild (jeb247987). They report how researchers have used sonar to follow migrating helmet jelly fish (Periphylla periphylla), acoustic tags attached to jellyfish, and tags equipped with motion sensors and depth meters that have revealed Nomura's jellyfish (Nemopilema numurai) diving down 176 m to avoid predators. The authors review the challenges of attaching data-collecting tags to soft-bodied organisms and tag retrieval after short- and longer-term deployments. They add that researchers should also be aware of the additional risk that tagged animals may no longer behave naturally. However, they are optimistic that underwater autonomous vehicles, coupled with new tracking algorithms will ‘allow for unprecedented access to the life history patterns of some of the most abundant, yet poorly understood groups of macroscopic marine animals on our planet’.

Continuing the theme of tracking animals in their natural environments, Roxanne Beltran (University of California, Santa Cruz, USA) and colleagues explain that enormous quantities of information about the movement of animals have been generated by researchers over recent years and are now available in databases for future analysis by researchers asking different questions. They argue for the power of integrating this powerful resource with already established databases of biological traits – such as details of body shape, size, diet and life habits – to expand our understanding of the ecology of the planet (jeb247981). However, they outline the challenges that must be overcome to permit effective integration between the two domains. These include taxonomic mismatches between trait and tracking databases. In addition, trait information is recorded at the species level, in contrast to movement traces, which are recorded from individuals. There is also a significant imbalance between the different forms of data, with trait measurements covering 19,662 species, while tracking observations are available for only 362 species. Despite these and other challenges, Beltran and colleagues suggest that integrating information from tracking databases with knowledge about traits could increase our understanding of metabolism in relation to body size, longevity and sexual niche partitioning in species. ‘We argue that the expansion of publicly available animal tracking and trait databases make now an ideal time to combine the two into a rich quantitative framework’, she says.

The delicate atmosphere that envelops our planet is a far from tranquil blanket. From circulating weather systems to eddies created by mountains, trees and shrubs, the atmosphere is in perpetual turmoil and birds experience every breeze and gust. In her Commentary, Emily Shepard from Swansea University, UK, explains that small scale air turbulence, similar in size to a bird's wingspan, can have a dramatic and detrimental effect on the flight of airborne creatures, while larger scale atmospheric eddies are experienced as wind (jeb248102). Man-made structures, including cities and wind farms, also produce atmospheric disruption, with the wakes of offshore wind farms extending up to 55 km. In response to smaller scale turbulence, birds and insects adjust their wing beat patterns to counteract instability and birds have also been recorded increasing their flight power by 25–100% to overcome the increased metabolic costs of gusty conditions. While it is unclear whether birds adapt their flight paths to avoid natural air turbulence, it is apparent that larger birds, which have less available power to counteract the effects of air disturbance, actively avoid wind farms. Turbulence could be read by flying animals as a cue that finetunes their flight patterns. Shepard champions the use of laboratory and field-based studies of the impact of turbulence on flying animals to better understand the ecological impact of air currents on airborne creatures as man-made structures and climate change increasingly impact the atmosphere.

To investigate how factors such as the environment, animal behaviour and evolutionary pressures influence flight, Douglas Altshuler and colleagues from University of British Columbia, Canada, advocate integrating extensive observation of bird behaviours in natural environments with astute hypothesis development (jeb247992). In their Review, they discuss how this strategy has been used by others to understand the environmental mechanisms behind Galapagos finch beak shapes, the impact of severe winter storms on house sparrow wing shape, and how foraging in the forest has led turkey vultures to evolve longer wings for their body mass than black vultures, which forage in the open. The second approach discussed is the systematic testing of alternative hypotheses, championed by John R. Platt in 1964, by ‘devising experiments with alternative possible outcomes, each of which will exclude more of the hypotheses’. Applying this approach Altshuler and colleagues have confirmed that the range of wing motion is a strong predictor of flight style, while the decline of hummingbird manoeuvrability at altitude is caused by the lower air density, rather than lower oxygen availability. Finally, the authors discuss how statistical tests can be used to compete alternative hypotheses. They describe how they used this approach to identify hummingbird species based on their manoeuvrability with a relatively high success rate, despite the inherent experimental messiness of the initial manoeuvrability observations.

In the final Review dedicated to the biomechanics of flight, Lucy Hawkes from the University of Exeter, UK, discusses the remarkable physical adaptations that allow birds to undertake the most arduous form of locomotion powered by a unique unidirectional respiration system, while avoiding many of the diseases associated with oxygen damage, obesity (when they accumulate fat in preparation for migration) and high blood sugar levels, which afflict human populations (jeb247986). Hawkes points out the lessons that human medicine could learn from avian physiology including: understanding how diving birds – such as penguins – deal with a reduced oxygen supply to muscles; how birds minimise the amount of toxic forms of oxygen released in their bodies by metabolism, which also increase as people age, causing physical damage; the mechanisms that allow birds to acquire fat at extraordinary rates prior to migration with none of the diseases that afflict obese humans; and how birds maintain their muscles into old age, a period when humans experience dramatic muscle loss. ‘Birds have seemingly found solutions to many of society's most pressing human healthcare issues’, says Hawkes, who is optimistic that human healthcare monitoring techniques can be applied to birds, permitting researchers to learn more about their remarkable age-defying physiology.

Having discussed the opportunities provided by extending our understanding of the movements of aquatic and aerial creatures in their natural environments, we now turn to focus on the Reviews and Commentaries detailing terrestrial creatures and how they manoeuvre through their habitats.

One of the most charismatic groups of creatures on the planet has to be the geckos. They run up and down vertical surfaces, even hanging upside down, secured by their remarkably adhesive feet. ‘However, what is known about how geckos cling stems primarily from laboratory studies of static adhesion’, say Timothy Higham (University of California, Riverside, USA) and Anthony Russell (University of Calgary, Canada). They explain how these elegant reptiles secure themselves to smooth surfaces via atomic forces transmitted through millions of microscopic hair-like structures, known as setae, located on the underside of their toes (jeb247980). But the duo wanted to discover how the animals attach and detach themselves from natural surfaces in the wild. Focusing on lessons learnt from studies of geckos adhering to casts of natural materials in the lab, Higham and Russell are keen to understand how the animals coordinate their limbs, and deploy their adhesive system and claws, as they manoeuvre over surfaces like rocks and trees. However, techniques that have revealed how large creatures manoeuvre are unlikely to work for more diminutive geckos, so the authors recommend that researchers video the reptiles’ movements, in combination with recordings from motion sensors, to learn how geckos negotiate the ecosystems they inhabit.

While the environment is a key factor driving the movement of animals – to find food, water and cooler locations – the decision to move is driven by the internal physiological condition of an animal. Robyn Hetem (University of Canterbury, New Zealand) and an international team of collaborators discuss the physiological mechanisms that underpin the movements of large mammals through their environment. Reviewing how motion sensors and GPS trackers allow scientists to track the detailed movements of large mammals, Hetem and colleagues discuss how implanted body temperature and heart rate monitors can reveal hitherto underappreciated details of the physiological condition of animals: providing information about how well-nourished and hydrated an animal is, when they are pregnant and whether they are experiencing disease (jeb248112). All these factors can drive animals to seek better conditions or restrict movement when an animal is severely impaired. Focusing on body temperature measurements, the team explains that they can reveal how well an animal is coping with drought or seasonal reductions in the quality and availability of food and water. ‘The underlying physiological states can be directly quantified through biologging physiological variables’, says Hetem, adding that this strategy could ‘revolutionise conservation management’.

The mechanical way in which animals and humans move is a major governing factor in how much energy they use when manoeuvring through the environment. But in their research, Jessica Selinger and colleagues from Queen's University, Canada, frame the concept of energy use from an alternative perspective: does the drive to minimise energy use directly shape how humans walk and run (jeb248125)? Having reviewed the evidence that we maximise the efficiency of our movements, they explain how people wearing exoskeletons that alter movement adapt to find novel and efficient ways to manoeuvre in response to unusual constraints. For our bodies to do so, Selinger and colleagues argue that we must be able to sense how much energy we are using. They discuss possible neural and muscle sensors that could integrate in a multisensory network to optimise our movement. Based on these ideas, the authors discuss how this knowledge could be applied to develop new rehabilitation therapies for patients recovering from stroke, allowing them to naturally select an even stride pattern when supported to walk economically, and suggest how exoskeletons that reduce energy use could also help individuals to alter other features of their walking style, including speed or stability.

The most extreme form of animal endurance has to be the epic migrations undertaken by birds circumnavigating the planet to their breeding grounds. Anders Hedenström, Lund University, Sweden, reviews the energetics of flight, discussing the most efficient speeds at which animals can fly, the distances that they can cover during migration – based on the amount of fuel that they can carry – and the amount of power, mechanical and metabolic, that they generate when airborne (jeb248123). In practice, many migrating birds stop off along their route to refuel, adjusting the speed at which they fly depending on whether their goal is to minimize the amount of energy they consume or to arrive as quickly as possible. Migrating birds also adjust their flight speed to compensate for wind and move faster as part of a flock. Listing some of the most impressive bird migrations – including the 11,500 km odyssey completed non-stop over 8 days by bar-tailed godwits – Hedenström explains that these birds may well be close to migrating as far as possible on the reserves they carry. In contrast, other species detour from the most direct route between their breeding and overwintering grounds to avoid obstructions, such as oceans and mountain ranges, or to take advantage of beneficial wind directions. Some birds may even hedge their bets, by exploring the air at higher altitudes in the hope of finding more beneficial flight conditions, or to take advantage of thinner air to reduce the aerodynamic drag they encounter at higher elevations.

Judy Shamoun-Baranes (University of Amsterdam, The Netherlands) and Kees Camphuysen (Royal Netherlands Institute for Sea Research) focus on migration as one aspect of the annual cycle of life – including breeding and moulting – through the seasons (jeb248053). All these events must be taken into account to understand an animal's annual energy budget and to identify challenging periods during the cycle. The duo review the migrations of lesser black-backed gulls from their breeding grounds in the northern Netherlands – one group of which crosses the North Sea to overwinter in the UK, while a second group completes a longer migration south to Africa – explaining that the birds switch between costly flapping flight and inexpensive soaring, depending on the atmospheric conditions. Comparing the gulls’ energy expenditures across the year, Shamoun-Baranes and Camphuysen report that the bird's migration strategy impacts when they expend the most energy: the short-distance migrants’ energy expenditure increases 1.4-fold during the breeding season and the energy expenditure of the long-distance migrants rockets to 1.7-times average during their spring northern migration. The scientists add, ‘An annual cycle perspective is likely feasible in many species...hopefully shedding light on the ability of animals to adapt to the changing world’.

The theme of physical endurance continues in Herman Pontzer's (Duke University, USA) Review, discussing the variation of energy investment in movement by animals over different time periods (jeb247988). Explaining that muscle activity accounts for the majority of energy expenditure over short periods (seconds to minutes), Pontzer describes how small wearable, or implantable, motion sensors have revolutionized activity measurement periods over longer periods, revealing that energy consumption over that timeframe depends mainly on the amount of activity an animal undertakes. However, when researchers measure the daily energy expenditures of animals, including humans, over several months, little difference in daily energy expenditure emerges between active and inactive populations. Pontzer explains that this contradiction is the result of physiological trade-offs against other biological systems, with more active groups reducing energy expenditure in other physiological functions, such as reproduction and the immune system. Time is a key element that must be integrated into laboratory and field studies to build a better understanding of the physical and metabolic costs of movement.

In addition to feats of heroic endurance, including ultramarathons and extreme cycle races, humans have applied their ingenuity to manoeuvre through extreme environments, including snow and ice. In their Review, Federico Formenti (King's College London, UK), Graham Askew (University of Leeds, UK) and Alberto Minetti (University of Milan, Italy) discuss the energetic benefits gained by the development of ice skates and cross-country skis over 10,000 years (jeb247851). Describing the first bone ice skates, wooden skis and how skiing and skating techniques have evolved over time, they report how ice skates have increased stride length by 240%, allowing skaters to use the energy in a single stride to cover the distance traversed by a walker over six paces. In addition, the metabolic cost of cross-country skiing has fallen from 313 J m⁻¹ in 542 AD to 154 J m⁻¹ in 2004 through improvements in ski design. The trio also discuss the adaptations, biomechanical and physiological, which allow Nepalese porters to carry heavy loads more efficiently than Caucasian mountaineers – walking 60% faster thanks to a 40% increase in mechanical power – in addition to the challenges faced by medieval soldiers wearing heavy restrictive armour, which would have limited the walking speed of a 20-year-old soldier to ∼6.1 km h⁻¹.

Of course, movement across any scale would be impossible without the powerful muscles that contract with each tail flick, wing beat and pumping leg. In his Review with colleagues from the University of Queensland, Australia, Glen Lichtwark discusses the various models that relate the energetics of locomotion to the movement itself, from the amount of time a limb is in contact with the ground to the cost of the kinetic work done by limbs to move the body forward (jeb248022). But none of these approaches directly takes into account the mechanical output of the muscles that drive movement. Lichtwark and colleagues outline some of the models that predict energy output based on muscle contraction, outlining the challenges that these models must overcome, including: the structure of large animal muscles, which deform extensively during contraction; elastic components altering how muscles act; and neural control modulating force generation. However, the team point out that there have been recent successes estimating the energetic costs of movement based on muscles moving joints, with the eventual goal of applying the simple motion measurements made by smart watches to accurately predict human energy consumption.

In a bid to pull together the overarching themes in this collection of Reviews and Commentaries, Wilson and Biewener discuss the importance of integrating laboratory and field studies – as outlined in this collection – to better understand the interaction of animals with their environment through the application of novel tracking and motion sensing technologies developed by researchers and smart phone companies (jeb249585). They also highlight the need for theory to guide future experimental design, while the development of a common vocabulary – initiated by Wilson and Biewener in a Glossary and Key Word list in their Commentary – is essential for the disparate fields to integrate and facilitate progress. The duo also point out that it is essential to identify key species, often with the potential for conservation benefits, for studies that will foster integration across biological themes by building an understanding of movement efficiency, from migration to foraging strategies. They also explain that many animals operate most economically when performing in the midrange of the power they produce or the speed at which they move while going about their daily lives. Exploring these relationships in detail will help researchers to understand better the fundamental trade-offs that underpin animal decisions as they negotiate their environments. Biewener and Wilson conclude, ‘We hope that the papers in this issue stimulate novel insights and improved integration and communications among scientists working across the boundaries of biology, engineering and ecology’.