Solving the conundrum of intra-specific variation in metabolic rate: A multidisciplinary conceptual and methodological toolkit: New technical developments are opening the door to an understanding of why metabolic rate varies among individual animals of a species: New technical developments are opening the door to an understanding of why metabolic rate varies among individual animals of a species.

Researchers from diverse disciplines, including organismal and cellular physiology, sports science, human nutrition, evolution and ecology, have sought to understand the causes and consequences of the surprising variation in metabolic rate found among and within individual animals of the same species. Research in this area has been hampered by differences in approach, terminology and methodology, and the context in which measurements are made. Recent advances provide important opportunities to identify and address the key questions in the field. By bringing together researchers from different areas of biology and biomedicine, we describe and evaluate these developments and the insights they could yield, highlighting the need for more standardisation across disciplines. We conclude with a list of important questions that can now be addressed by developing a common conceptual and methodological toolkit for studies on metabolic variation in animals.

Greater male variability in daily energy expenditure develops through puberty.

There is considerably greater variation in metabolic rates between men than between women, in terms of basal, activity and total (daily) energy expenditure (EE). One possible explanation is that EE is associated with male sexual characteristics (which are known to vary more than other traits) such as musculature and athletic capacity. Such traits might be predicted to be most prominent during periods of adolescence and young adulthood, when sexual behaviour develops and peaks. We tested this hypothesis on a large dataset by comparing the amount of male variation and female variation in total EE, activity EE and basal EE, at different life stages, along with several morphological traits: height, fat free mass and fat mass. Total EE, and to some degree also activity EE, exhibit considerable greater male variation (GMV) in young adults, and then a decreasing GMV in progressively older individuals. Arguably, basal EE, and also morphometrics, do not exhibit this pattern. These findings suggest that single male sexual characteristics may not exhibit peak GMV in young adulthood, however total and perhaps also activity EE, associated with many morphological and physiological traits combined, do exhibit GMV most prominently during the reproductive life stages.

Variability in energy expenditure is much greater in males than females.

In mammals, trait variation is often reported to be greater among males than females. However, to date, mainly only morphological traits have been studied. Energy expenditure represents the metabolic costs of multiple physical, physiological, and behavioral traits. Energy expenditure could exhibit particularly high greater male variation through a cumulative effect if those traits mostly exhibit greater male variation, or a lack of greater male variation if many of them do not. Sex differences in energy expenditure variation have been little explored. We analyzed a large database on energy expenditure in adult humans (1494 males and 3108 females) to investigate whether humans have evolved sex differences in the degree of interindividual variation in energy expenditure. We found that, even when statistically comparing males and females of the same age, height, and body composition, there is much more variation in total, activity, and basal energy expenditure among males. However, with aging, variation in total energy expenditure decreases, and because this happens more rapidly in males, the magnitude of greater male variation, though still large, is attenuated in older age groups. Considerably greater male variation in both total and activity energy expenditure could be explained by greater male variation in levels of daily activity. The considerably greater male variation in basal energy expenditure is remarkable and may be explained, at least in part, by greater male variation in the size of energy-demanding organs. If energy expenditure is a trait that is of indirect interest to females when choosing a sexual partner, this would suggest that energy expenditure is under sexual selection. However, we present a novel energetics model demonstrating that it is also possible that females have been under stabilizing selection pressure for an intermediate basal energy expenditure to maximize energy available for reproduction.

Are humans evolved specialists for running in the heat? Man vs. horse races provide empirical insights.

NEW FINDINGS: What is the central question of this study? Do available comparative data provide empirical evidence that humans are adapted to endurance running at high ambient temperatures? What is the main finding and its importance? Comparing the results of races that pit man against horse, we find that ambient temperature on race day has less deleterious effects on running speed in humans than it does on their quadrupedal adversary. This is evidence that humans are adapted for endurance running at high ambient temperatures. We debate whether this supports the hypothesis that early man was evolutionarily adapted for persistence hunting. ABSTRACT: Many mammals run faster and for longer than humans and have superior cardiovascular physiologies. Yet humans are considered by some scholars to be excellent endurance runners at high ambient temperatures, and in our past to have been persistence hunters capable of running down fleeter quarry over extended periods during the heat of the day. This suggests that human endurance running is less affected by high ambient temperatures than is that of other cursorial ungulates. However, there are no investigations of this hypothesis. We took advantage of longitudinal race results available for three annual events that pit human athletes directly against a hyper-adapted ungulate racer, the thoroughbred horse. Regressing running speed against ambient temperature shows race speed deteriorating with hotter temperatures more slowly in humans than in horses. This is the first direct evidence that human running is less inhibited by high ambient temperatures than that of another endurance species, supporting the argument that we are indeed adapted for high temperature endurance running. Nonetheless, it is far from clear that this capacity is explained by an endurance hunting past because in absolute terms humans are slower than horses and indeed many other ungulate species. While some human populations have persistence hunted (and on occasion still do), the success of this unlikely foraging strategy may be best explained by the application of another adaption - high cognitive capacity. With dedication, experience and discipline, capitalising on their small endurance advantage in high temperatures, humans have a chance of running a more athletic prey to exhaustion.

The energetics of 'airtime': estimating swim power from breaching behaviour in fishes and cetaceans.

Displays of maximum swimming speeds are rare in the laboratory and the wild, limiting our understanding of the top-end athletic capacities of aquatic vertebrates. However, jumps out of the water - exhibited by a diversity of fish and cetaceans - might sometimes represent a behaviour comprising maximum burst effort. We collected data on such breaching behaviour for 14 fish and cetacean species primarily from online videos, to calculate breaching speed. From newly derived formulae based on the drag coefficient and hydrodynamic efficiency, we also calculated the associated power. The fastest breaching speeds were exhibited by species 2 m in length, peaking at nearly 11 m s-1; as species size decreases below this, the fastest breaches become slower, while species larger than 2 m do not show a systematic pattern. The power associated with the fastest breaches was consistently ∼50 W kg-1 (equivalent to 200 W kg-1 muscle) in species from 20 cm to 2 m in length, suggesting that this value may represent a universal (conservative) upper boundary. And it is similar to the maximum recorded power output per muscle mass recorded in any species of similar size, suggesting that some breaches could indeed be representative of maximum capability.

Energetic limits: Defining the bounds and trade-offs of successful energy management in a capital breeder.

Judicious management of energy can be invaluable for animal survival and reproductive success. Capital breeding mammals typically transfer energy to their young at extremely high rates while undergoing prolonged fasting, making lactation a tremendously energy demanding period. Effective management of the competing demands of the mother's energy needs and those of her offspring is presumably fundamental to maximizing lifetime reproductive success. How does the mother maximize her chances of successfully rearing her pup, by ensuring that both her pup and herself have sufficient energy during this 'energetic fast'? While energy management models were first discussed in the 1990s, application of this analytical technique is still very much in its infancy. Recent work suggests that a broad range of species exhibits 'energy compensation'; during periods when they expend more energy on activity, their bodies partially compensate by reducing background (basal) metabolic rate as an adaptation to limit overall energy expenditure. However, the value of energy management models in understanding animal ecology is presently unclear. We investigate whether energy management models provide insights into the breeding strategy of phocid seals. Not only do we expect lactating seals to display energy compensation because of their breeding strategy of high energy transfer while fasting, but we anticipate that mothers exhibiting a lack of energy compensation are less likely to rear offspring successfully. On the Isle of May in Scotland, we collected heart rate data as a proxy for energy expenditure in 52 known individual grey seal (Halichoerus grypus) mothers, repeatedly across 3 years of breeding. We provide evidence that grey seal mothers typically exhibit energy compensation during lactation by downregulating their background metabolic rate to limit daily energy expenditure during periods when other energy costs are relatively high. However, individuals that fail to energy compensate during the lactation period are more likely to end lactation earlier than expected. Our study is the first to demonstrate the importance of energy compensation to an animal's reproductive expenditure. Moreover, our multi-seasonal data indicate that environmental stressors may reduce the capacity of some individuals to follow the energy compensation strategy.

100 years since Scott reached the pole: a century of learning about the physiological demands of Antarctica.

The 1910-1913 Terra Nova Expedition to the Antarctic, led by Captain Robert Falcon Scott, was a venture of science and discovery. It is also a well-known story of heroism and tragedy since his quest to reach the South Pole and conduct research en route, while successful was also fateful. Although Scott and his four companions hauled their sledges to the Pole, they died on their return journey either directly or indirectly from the extreme physiological stresses they experienced. One hundred years on, our understanding of such stresses caused by Antarctic extremes and how the body reacts to severe exercise, malnutrition, hypothermia, high altitude, and sleep deprivation has greatly advanced. On the centenary of Scott's expedition to the bottom of the Earth, there is still controversy surrounding whether the deaths of those five men could have, or should have, been avoided. This paper reviews present-day knowledge related to the physiology of sustained man-hauling in Antarctica and contrasts this with the comparative ignorance about these issues around the turn of the 20th century. It closes by considering whether, with modern understanding about the effects of such a scenario on the human condition, Scott could have prepared and managed his team differently and so survived the epic 1,600-mile journey. The conclusion is that by carrying rations with a different composition of macromolecules, enabling greater calorific intake at similar overall weight, Scott might have secured the lives of some of the party, and it is also possible that enhanced levels of vitamin C in his rations, albeit difficult to achieve in 1911, could have significantly improved their survival chances. Nevertheless, even with today's knowledge, a repeat attempt at his expedition would by no means be bound to succeed.

Regression dilution in energy management patterns.

Analysis of some experimental biology data involves linear regression and interpretation of the resulting slope value. Usually, the x-axis measurements include noise. Noise in the x-variable can create regression dilution, and many biologists are not aware of the implications: regression dilution results in an underestimation of the true slope value. This is particularly problematic when the slope value is diagnostic. For example, energy management strategies of animals can be determined from the regression slope estimate of mean energy expenditure against resting energy expenditure. Typically, energy expenditure is represented by a proxy such as heart rate, which adds substantive measurement error. With simulations and analysis of empirical data, we explore the possible effect of regression dilution on interpretations of energy management strategies. We conclude that unless the coefficient of determination r2 is very high, there is a good possibility that regression dilution will affect qualitative interpretation. We recommend some ways to contend with regression dilution, including the application of alternative available regression approaches under certain circumstances.

The reign of the p-value is over: what alternative analyses could we employ to fill the power vacuum?

The p-value has long been the figurehead of statistical analysis in biology, but its position is under threat. p is now widely recognized as providing quite limited information about our data, and as being easily misinterpreted. Many biologists are aware of p's frailties, but less clear about how they might change the way they analyse their data in response. This article highlights and summarizes four broad statistical approaches that augment or replace the p-value, and that are relatively straightforward to apply. First, you can augment your p-value with information about how confident you are in it, how likely it is that you will get a similar p-value in a replicate study, or the probability that a statistically significant finding is in fact a false positive. Second, you can enhance the information provided by frequentist statistics with a focus on effect sizes and a quantified confidence that those effect sizes are accurate. Third, you can augment or substitute p-values with the Bayes factor to inform on the relative levels of evidence for the null and alternative hypotheses; this approach is particularly appropriate for studies where you wish to keep collecting data until clear evidence for or against your hypothesis has accrued. Finally, specifically where you are using multiple variables to predict an outcome through model building, Akaike information criteria can take the place of the p-value, providing quantified information on what model is best. Hopefully, this quick-and-easy guide to some simple yet powerful statistical options will support biologists in adopting new approaches where they feel that the p-value alone is not doing their data justice.

Combining abundance and performance data reveals how temperature regulates coastal occurrences and activity of a roaming apex predator.

The redistribution of species has emerged as one of the most pervasive impacts of anthropogenic climate warming, and presents many societal challenges. Understanding how temperature regulates species distributions is particularly important for mobile marine fauna such as sharks given their seemingly rapid responses to warming, and the socio-political implications of human encounters with some dangerous species. The predictability of species distributions can potentially be improved by accounting for temperature's influence on performance, an elusive relationship for most large animals. We combined multi-decadal catch data and bio-logging to show that coastal abundance and swimming performance of tiger sharks Galeocerdo cuvier are both highest at ~22°C, suggesting thermal constraints on performance may regulate this species' distribution. Tiger sharks are responsible for a large proportion of shark bites on humans, and a focus of controversial control measures in several countries. The combination of distribution and performance data moves towards a mechanistic understanding of tiger shark's thermal niche, and delivers a simple yet powerful indicator for predicting the location and timing of their occurrences throughout coastlines. For example, tiger sharks are mostly caught at Australia's popular New South Wales beaches (i.e. near Sydney) in the warmest months, but our data suggest similar abundances will occur in winter and summer if annual sea surface temperatures increase by a further 1-2°C.

Latent power of basking sharks revealed by exceptional breaching events.

The fast swimming and associated breaching behaviour of endothermic mackerel sharks is well suited to the capture of agile prey. In contrast, the observed but rarely documented breaching capability of basking sharks is incongruous to their famously languid lifestyle as filter-feeding planktivores. Indeed, by analysing video footage and an animal-instrumented data logger, we found that basking sharks exhibit the same vertical velocity (approx. 5 m s-1) during breach events as the famously powerful predatory great white shark. We estimate that an 8-m, 2700-kg basking shark, recorded breaching at 5 m s-1 and accelerating at 0.4 m s-2, expended mechanical energy at a rate of 5.5 W kg-1; a mass-specific energetic cost comparable to that of the great white shark. The energy cost of such a breach is equivalent to around 1/17th of the daily standard metabolic cost for a basking shark, while the ratio is about half this for a great white shark. While breaches by basking sharks must serve a different function to white shark breaches, their similar breaching speeds questions our perception of the physiology of large filter-feeding fish.

How does school size affect tail beat frequency in turbulent water?

The energy savings experienced by fish swimming in a school have so far been investigated in an near-idealised experimental context including a relatively laminar water flow. The effects of explicitly turbulent flows and different group sizes are yet to be considered. Our repeated-measures study is a first step in addressing both of these issues: whether schooling is more energetically economical for fish when swimming in a quantified non-laminar flow and how this might be moderated by group size. We measured tail beat frequency (tbf) in sea bass swimming in a group of 3 or 6, or singly. Video data enabled us to approximately track the movements of the fish during the experiments and in turn ascertain the water flow rates and turbulence levels experienced for each target individual. Although the fish exhibited reductions in tbf during group swimming, which may indicate some energy savings, these savings appear to be attenuated, presumably due to the water turbulence and the movement of the fish relative to each other. Surprisingly, tbf was unrelated to flow rate when the fish were swimming singly or in a group of three, and decreased with increasing flow rates when swimming in a group of six. However, the fish increased tbf in greater turbulence at all group sizes. Our study demonstrates that under the challenging and complex conditions of turbulent flow and short-term changes in school structure, group size can moderate the influences of water flow on a fish's swimming kinematics, and in turn perhaps their energy costs. SUMMARY STATEMENT: The energy savings that sea bass experience from schooling are affected by flow speed or turbulence, moderated by group size.

Effects of Body Mass Index on Bone Loading Due to Physical Activity.

The aim of the current study was to compare bone loading due to physical activity between lean, and overweight and obese individuals. Fifteen participants (lower BMI group: BMI < 25 kg/m2, n = 7; higher BMI group: 25 kg/m2 < BMI < 36.35 kg/m2, n = 8) wore a tri-axial accelerometer on 1 day to collect data for the calculation of bone loading. The International Physical Activity Questionnaire (short form) was used to measure time spent at different physical activity levels. Daily step counts were measured using a pedometer. Differences between groups were compared using independent t-tests. Accelerometer data revealed greater loading dose at the hip in lower BMI participants at a frequency band of 0.1-2 Hz (P = .039, Cohen's d = 1.27) and 2-4 Hz (P = .044, d = 1.24). Lower BMI participants also had a significantly greater step count (P = .023, d = 1.55). This corroborated with loading intensity (d ≥ 0.93) and questionnaire (d = 0.79) effect sizes to indicate higher BMI participants tended to spend more time in very light activity, and less time in light and moderate activity. Overall, participants with a lower BMI exhibited greater bone loading due to physical activity; participants with a higher BMI may benefit from more light and moderate level activity to maintain bone health.

Practice makes perfect: Performance optimisation in 'arboreal' parkour athletes illuminates the evolutionary ecology of great ape anatomy.

An animal's size is central to its ecology, yet remarkably little is known about the selective pressures that drive this trait. A particularly compelling example is how ancestral apes evolved large body mass in such a physically and energetically challenging environment as the forest canopy, where weight-bearing branches and lianas are flexible, irregular and discontinuous, and the majority of preferred foods are situated on the most flexible branches at the periphery of tree crowns. To date the issue has been intractable due to a lack of relevant fossil material, the limited capacity of the fossil record to reconstruct an animal's behavioural ecology and the inability to measure energy consumption in freely moving apes. We studied the oxygen consumption of parkour athletes while they traversed an arboreal-like course as an elite model ape, to test the ecomorphological and behavioural mechanisms by which a large-bodied ape could optimize its energetic performance during tree-based locomotion. Our results show that familiarity with the arboreal-like course allowed the athletes to substantially reduce their energy expenditure. Furthermore, athletes with larger arm spans and shorter legs were particularly adept at finding energetic savings. Our results flesh out the scanty fossil record to offer evidence that long, strong arms, broad chests and a strong axial system, combined with the frequent use of uniform branch-to-branch arboreal pathways, were critical to off-setting the mechanical and energetic demands of large mass in ancestral apes.

A different angle: comparative analyses of whole-animal transport costs when running uphill.

Comparative work on the cost of terrestrial locomotion in animals has focused on the underpinning physiology and biomechanics. Often, much of an animal's energy budget is spent on moving around; thus, there is also value in interpreting such data from an ecological perspective. When animals move through their environment, they encounter topographical variation, and this is a key factor that can dramatically affect their energy expenditure. We collated published data on the costs for birds and mammals to locomote terrestrially on inclines, and investigated the scaling relationships using a phylogenetically informed approach. We show that smaller animals have a greater mass-specific cost of transport on inclines across the body mass range analysed. We also demonstrate that the increase in cost for smaller animals to run up a slope as opposed to along a flat surface is comparatively low. Heavier animals show larger absolute and relative increases in energy cost to travel uphill. Consideration of all aspects of the cost of incline locomotion - absolute, relative and mass specific - provides a fuller understanding of the interactions between transport costs, body mass, incline gradient and phylogeny, and enables us to consider their ecological implications, which we couch within the context of the 'energy landscape'.

Considering aspects of the 3Rs principles within experimental animal biology.

The 3Rs - Replacement, Reduction and Refinement - are embedded into the legislation and guidelines governing the ethics of animal use in experiments. Here, we consider the advantages of adopting key aspects of the 3Rs into experimental biology, represented mainly by the fields of animal behaviour, neurobiology, physiology, toxicology and biomechanics. Replacing protected animals with less sentient forms or species, cells, tissues or computer modelling approaches has been broadly successful. However, many studies investigate specific models that exhibit a particular adaptation, or a species that is a target for conservation, such that their replacement is inappropriate. Regardless of the species used, refining procedures to ensure the health and well-being of animals prior to and during experiments is crucial for the integrity of the results and legitimacy of the science. Although the concepts of health and welfare are developed for model organisms, relatively little is known regarding non-traditional species that may be more ecologically relevant. Studies should reduce the number of experimental animals by employing the minimum suitable sample size. This is often calculated using power analyses, which is associated with making statistical inferences based on the P-value, yet P-values often leave scientists on shaky ground. We endorse focusing on effect sizes accompanied by confidence intervals as a more appropriate means of interpreting data; in turn, sample size could be calculated based on effect size precision. Ultimately, the appropriate employment of the 3Rs principles in experimental biology empowers scientists in justifying their research, and results in higher-quality science.

Ecological Influences and Morphological Correlates of Resting and Maximal Metabolic Rates across Teleost Fish Species.

Rates of aerobic metabolism vary considerably across evolutionary lineages, but little is known about the proximate and ultimate factors that generate and maintain this variability. Using data for 131 teleost fish species, we performed a large-scale phylogenetic comparative analysis of how interspecific variation in resting metabolic rates (RMRs) and maximum metabolic rates (MMRs) is related to several ecological and morphological variables. Mass- and temperature-adjusted RMR and MMR are highly correlated along a continuum spanning a 30- to 40-fold range. Phylogenetic generalized least squares models suggest that RMR and MMR are higher in pelagic species and that species with higher trophic levels exhibit elevated MMR. This variation is mirrored at various levels of structural organization: gill surface area, muscle protein content, and caudal fin aspect ratio (a proxy for activity) are positively related with aerobic capacity. Muscle protein content and caudal fin aspect ratio are also positively correlated with RMR. Hypoxia-tolerant lineages fall at the lower end of the metabolic continuum. Different ecological lifestyles are associated with contrasting levels of aerobic capacity, possibly reflecting the interplay between selection for increased locomotor performance on one hand and tolerance to low resource availability, particularly oxygen, on the other. These results support the aerobic capacity model of the evolution of endothermy, suggesting elevated body temperatures evolved as correlated responses to selection for high activity levels.

Terrestrial movement energetics: current knowledge and its application to the optimising animal.

The energetic cost of locomotion can be a substantial proportion of an animal's daily energy budget and thus key to its ecology. Studies on myriad species have added to our knowledge about the general cost of animal movement, including the effects of variations in the environment such as terrain angle. However, further such studies might provide diminishing returns on the development of a deeper understanding of how animals trade-off the cost of movement with other energy costs, and other ecological currencies such as time. Here, I propose the 'individual energy landscape' as an approach to conceptualising the choices facing the optimising animal. In this Commentary, first I outline previous broad findings about animal walking and running locomotion, focusing in particular on the use of net cost of transport as a metric of comparison between species, and then considering the effects of environmental perturbations and other extrinsic factors on movement costs. I then introduce and explore the idea that these factors combine with the behaviour of the animal in seeking short-term optimality to create that animal's individual energy landscape - the result of the geographical landscape and environmental factors combined with the animal's selected trade-offs. Considering an animal's locomotion energy expenditure within this context enables hard-won empirical data on transport costs to be applied to questions about how an animal can and does move through its environment to maximise its fitness, and the relative importance, or otherwise, of locomotion energy economy.

Do animals exercise to keep fit?

We humans know we are not physically fit unless we do extra, voluntary exercise. Yet we have never asked whether the same is true for animals. If it is, then given that energy will be spent keeping fit this raises important issues about new energetic trade-offs, which have never been considered.

Is there a trade-off between peak performance and performance breadth across temperatures for aerobic scope in teleost fishes?

The physiology and behaviour of ectotherms are strongly influenced by environmental temperature. A general hypothesis is that for performance traits, such as those related to growth, metabolism or locomotion, species face a trade-off between being a thermal specialist or a thermal generalist, implying a negative correlation between peak performance and performance breadth across a range of temperatures. Focusing on teleost fishes, we performed a phylogenetically informed comparative analysis of the relationship between performance peak and breadth for aerobic scope (AS), which represents whole-animal capacity available to carry out simultaneous oxygen-demanding processes (e.g. growth, locomotion, reproduction) above maintenance. Literature data for 28 species indicate that peak aerobic capacity is not linked to thermal performance breadth and that other physiological factors affecting thermal tolerance may prevent such a trade-off from emerging. The results therefore suggest that functional links between peak and thermal breadth for AS may not constrain evolutionary responses to environmental changes such as climate warming.