Flying fast improves aerodynamic economy of heavier birds.

A paradox of avian long-distance migrations is that birds must greatly increase their body mass prior to departure, yet this is presumed to substantially increase their energy cost of flight. However, here we show that when homing pigeons flying in a flock are loaded with ventrally located weight, both their heart rate and estimated energy expenditure rise by a remarkably small amount. The net effect is that costs per unit time increase only slightly and per unit mass they decrease. We suggest that this is because these homing flights are relatively fast, and consequently flight costs associated with increases in body parasite drag dominate over those of weight support, leading to an improvement in mass-specific flight economy. We propose that the relatively small absolute aerodynamic penalty for carrying enlarged fuel stores and flight muscles during fast flight has helped to select for the evolution of long-distance migration.

Low resting metabolic rate and increased hunger due to ß-MSH and ß-endorphin deletion in a canine model.

Mutations that perturb leptin-melanocortin signaling are known to cause hyperphagia and obesity, but energy expenditure has not been well studied outside rodents. We report on a common canine mutation in pro-opiomelanocortin (POMC), which prevents production of ß-melanocyte-stimulating hormone (ß-MSH) and ß-endorphin but not α-MSH; humans, similar to dogs, produce α-MSH and ß-MSH from the POMC propeptide, but rodents produce only α-MSH. We show that energy expenditure is markedly lower in affected dogs, which also have increased motivational salience in response to a food cue, indicating increased wanting or hunger. There was no difference in satiety at a modified ad libitum meal or in their hedonic response to food, nor disruption of adrenocorticotropic hormone (ACTH) or thyroid axes. In vitro, we show that ß-MSH signals comparably to α-MSH at melanocortin receptors. These data implicate ß-MSH and ß-endorphin as important in determining hunger and moderating energy expenditure and suggest that this role is independent of the presence of α-MSH.

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 variability: does variation in morphological and physiological traits differ between men and women?

Many researchers presume greater variability between female participants than between males due to the menstrual cycle. This view has encouraged a sex bias in health and medical research, resulting in considerable knowledge gaps with important clinical implications. Yet in another field-evolutionary biology-the received wisdom is the reverse: that men are more variable, possibly due to male heterogamety. To test these competing hypotheses, we compared variance between the sexes for 50 morphological and physiological traits, analysing data from the NHANES database. Nearly half the traits did not exhibit sexual dimorphism in variation, while 18 exhibited greater female variation (GFV), indicating GFV does not dominate human characteristics. Only eight traits exhibited greater male variation (GMV), indicating GMV also does not dominate, and in turn offering scant support for the heterogamety hypothesis. When our analysis was filtered to include only women with regular menstrual cycles (and men of equivalent age), the number of traits with GFV and GMV were low and not statistically different, suggesting that the menstrual cycle does not typically explain GFV when it occurs. In practical terms, health and medical researchers should no longer simply assume that female participants will induce additional variation in the traits of interest.

Does eating less or exercising more to reduce energy availability produce distinct metabolic responses?

When less energy is available to consume, people often lose weight, which reduces their overall metabolic rate. Their cellular metabolic rate may also decrease (metabolic adaptation), possibly reflected in physiological and/or endocrinological changes. Reduced energy availability can result from calorie restriction or increased activity energy expenditure, raising the following question that our review explores: do the body's metabolic and physiological responses to this reduction differ or not depending on whether they are induced by dietary restriction or increased activity? First, human studies offer indirect, contentious evidence that the body metabolically adapts to reduced energy availability, both in response to either a calorie intake deficit or increased activity (exercise; without a concomitant increase in food intake). Considering individual aspects of the body's physiology as constituents of whole-body metabolic rate, similar responses to reduced energy availability are observed in terms of reproductive capacity, somatic maintenance and hormone levels. By contrast, tissue phenotypic responses differ, most evidently for skeletal tissue, which is preserved in response to exercise but not calorie restriction. Thus, while in many ways 'a calorie deficit is a calorie deficit', certain tissues respond differently depending on the energy deficit intervention. This article is part of a discussion meeting issue 'Causes of obesity: theories, conjectures and evidence (Part I)'.

Allometric scaling of metabolic rate and cardiorespiratory variables in aquatic and terrestrial mammals.

While basal metabolic rate (BMR) scales proportionally with body mass (Mb ), it remains unclear whether the relationship differs between mammals from aquatic and terrestrial habitats. We hypothesized that differences in BMR allometry would be reflected in similar differences in scaling of O2 delivery pathways through the cardiorespiratory system. We performed a comparative analysis of BMR across 63 mammalian species (20 aquatic, 43 terrestrial) with a Mb range from 10 kg to 5318 kg. Our results revealed elevated BMRs in small (>10 kg and <100 kg) aquatic mammals compared to small terrestrial mammals. The results demonstrated that minute ventilation, that is, tidal volume (VT )·breathing frequency (fR ), as well as cardiac output, that is, stroke volume·heart rate, do not differ between the two habitats. We found that the "aquatic breathing strategy", characterized by higher VT and lower fR resulting in a more effective gas exchange, and by elevated blood hemoglobin concentrations resulting in a higher volume of O2 for the same volume of blood, supported elevated metabolic requirements in aquatic mammals. The results from this study provide a possible explanation of how differences in gas exchange may serve energy demands in aquatic versus terrestrial mammals.

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.

Does aerobic scope influence geographical distribution of teleost fishes?

Many abiotic and biotic factors are known to shape species' distributions, but we lack understanding of how innate physiological traits, such as aerobic scope (AS), may influence the latitudinal range of species. Based on theoretical assumptions, a positive link between AS and distribution range has been proposed, but there has been no broad comparative study across species to test this hypothesis. We collected metabolic rate data from the literature and performed a phylogenetically informed analysis to investigate the influence of AS on the current geographical distributions of 111 teleost fish species. Contrary to expectations, we found a negative relationship between absolute latitude range and thermal peak AS in temperate fishes. We found no evidence for an association between thermal range of AS and the range of latitudes occupied for 32 species. Our main results therefore contradict the prevailing theory of a positive link between AS and distribution range in fish.

Total daily energy expenditure has declined over the past three decades due to declining basal expenditure, not reduced activity expenditure.

Obesity is caused by a prolonged positive energy balance1,2. Whether reduced energy expenditure stemming from reduced activity levels contributes is debated3,4. Here we show that in both sexes, total energy expenditure (TEE) adjusted for body composition and age declined since the late 1980s, while adjusted activity energy expenditure increased over time. We use the International Atomic Energy Agency Doubly Labelled Water database on energy expenditure of adults in the United States and Europe (n = 4,799) to explore patterns in total (TEE: n = 4,799), basal (BEE: n = 1,432) and physical activity energy expenditure (n = 1,432) over time. In males, adjusted BEE decreased significantly, but in females this did not reach significance. A larger dataset of basal metabolic rate (equivalent to BEE) measurements of 9,912 adults across 163 studies spanning 100 years replicates the decline in BEE in both sexes. We conclude that increasing obesity in the United States/Europe has probably not been fuelled by reduced physical activity leading to lowered TEE. We identify here a decline in adjusted BEE as a previously unrecognized factor.

Variation in human water turnover associated with environmental and lifestyle factors.

Water is essential for survival, but one in three individuals worldwide (2.2 billion people) lacks access to safe drinking water. Water intake requirements largely reflect water turnover (WT), the water used by the body each day. We investigated the determinants of human WT in 5604 people from the ages of 8 days to 96 years from 23 countries using isotope-tracking (2H) methods. Age, body size, and composition were significantly associated with WT, as were physical activity, athletic status, pregnancy, socioeconomic status, and environmental characteristics (latitude, altitude, air temperature, and humidity). People who lived in countries with a low human development index (HDI) had higher WT than people in high-HDI countries. On the basis of this extensive dataset, we provide equations to predict human WT in relation to anthropometric, economic, and environmental factors.

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.

The Mystery of Energy Compensation.

AbstractThe received wisdom on how activity affects energy expenditure is that the more activity is undertaken, the more calories will have been burned by the end of the day. Yet traditional hunter-gatherers, who lead physically hard lives, burn no more calories each day than Western populations living in labor-saving environments. Indeed, there is now a wealth of data, both for humans and other animals, demonstrating that long-term lifestyle changes involving increases in exercise or other physical activities do not result in commensurate increases in daily energy expenditure (DEE). This is because humans and other animals exhibit a degree of energy compensation at the organismal level, ameliorating some of the increases in DEE that would occur from the increased activity by decreasing the energy expended on other biological processes. And energy compensation can be sizable, reaching many hundreds of calories in humans. But the processes that are downregulated in the long-term to achieve energy compensation are far from clear, particularly in humans-we do not know how energy compensation is achieved. My review here of the literature on relevant exercise intervention studies, for both humans and other species, indicates conflict regarding the role, if any, of basal metabolic rate (BMR) or low-level activity such as fidgeting play, particularly once changes in body composition are factored out. In situations where BMR and low-level activity are not major components of energy compensation, what then drives it? I discuss how changes in mitochondrial efficiency and changes in circadian fluctuations in BMR may contribute to our understanding of energy management. Currently unexplored, these mechanisms and others may provide important insights into the mystery of how energy compensation is achieved.

The cardio-respiratory effects of passive heating and the human thermoneutral zone.

The thermoneutral zone (TNZ) defines the range of ambient temperatures at which resting metabolic rate (MR) is at a minimum. While the TNZ lower limit has been characterized, it is still unclear whether there is an upper limit, that is, beyond which MR during rest increases, and if so, what physiological upregulations explain this. We take the first step to fill this knowledge gap by measuring MR and multiple physiological variables in participants exposed to ambient heat stress while resting. Thirteen participants were exposed for an hour to 28℃-50% relative humidity (RH) air, and both 40 and 50℃ each in 25% RH and humid (50% RH) conditions. Core and skin temperatures, blood pressure, sweat-, heart-, and breathing-rate, minute ventilation, and movement levels were recorded throughout each condition. MR increased 35% (p = .015) during exposure to 40℃-25% RH compared to baseline and a further 13% (p = .000) at in 50℃-50%RH. This was not explained by increased fidgeting (p = .26), suggesting physiological upregulation. However, while greater heat stress invoked increases in heart rate (64%, p = .000), minute ventilation (78%, p = .000), and sweat rate (74%. p = .000) when comparing 50℃-50% RH with baseline, the exact size of their relative energy cost is unclear and, therefore, so is their contribution to this increase in MR. Our study shows clear evidence that resting MR increases in humans at high temperature-there is a metabolic upper critical temperature, at least as low as 40℃. Further studies should pinpoint this value and fully explain this increased MR.

Energy compensation and adiposity in humans.

Understanding the impacts of activity on energy balance is crucial. Increasing levels of activity may bring diminishing returns in energy expenditure because of compensatory responses in non-activity energy expenditures.1-3 This suggestion has profound implications for both the evolution of metabolism and human health. It implies that a long-term increase in activity does not directly translate into an increase in total energy expenditure (TEE) because other components of TEE may decrease in response-energy compensation. We used the largest dataset compiled on adult TEE and basal energy expenditure (BEE) (n = 1,754) of people living normal lives to find that energy compensation by a typical human averages 28% due to reduced BEE; this suggests that only 72% of the extra calories we burn from additional activity translates into extra calories burned that day. Moreover, the degree of energy compensation varied considerably between people of different body compositions. This association between compensation and adiposity could be due to among-individual differences in compensation: people who compensate more may be more likely to accumulate body fat. Alternatively, the process might occur within individuals: as we get fatter, our body might compensate more strongly for the calories burned during activity, making losing fat progressively more difficult. Determining the causality of the relationship between energy compensation and adiposity will be key to improving public health strategies regarding obesity.

Fish heating tolerance scales similarly across individual physiology and populations.

Extrapolating patterns from individuals to populations informs climate vulnerability models, yet biological responses to warming are uncertain at both levels. Here we contrast data on the heating tolerances of fishes from laboratory experiments with abundance patterns of wild populations. We find that heating tolerances in terms of individual physiologies in the lab and abundance in the wild decline with increasing temperature at the same rate. However, at a given acclimation temperature or optimum temperature, tropical individuals and populations have broader heating tolerances than temperate ones. These congruent relationships implicate a tight coupling between physiological and demographic processes underpinning macroecological patterns, and identify vulnerability in both temperate and tropical species.

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.

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.

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.

Powering Ocean Giants: The Energetics of Shark and Ray Megafauna.

Shark and ray megafauna have crucial roles as top predators in many marine ecosystems, but are currently among the most threatened vertebrates and, based on historical extinctions, may be highly susceptible to future environmental perturbations. However, our understanding of their energetics lags behind that of other taxa. Such knowledge is required to answer important ecological questions and predict their responses to ocean warming, which may be limited by expanding ocean deoxygenation and declining prey availability. To develop bioenergetics models for shark and ray megafauna, incremental improvements in respirometry systems are useful but unlikely to accommodate the largest species. Advances in biologging tools and modelling could help answer the most pressing ecological questions about these iconic species.

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.