The Time Allometry of Mammalian Chewing Movements: Chewing Frequency Scales with Body Mass in Mammals

For a sample of 26 extant mammalian species, a significant relationship between body mass and chewing frequency was found, in which chewing frequency is proportional to body mass to the -0·128 power. This relationship is similar to previously published data relating stride frequency and body mass in quadrupedal mammals. It was also found that jaw length is proportional to body mass to the 0·312 power, which is consistent with geometric scaling of jaw length. The period of the chewing cycle was found to be proportional to jaw length to the 0·383 power. These results demonstrate that chewing frequency does not scale as metabolic rate, and support the suggestion that the natural frequency of the chewing rhythm may be derived from masses and lengths of the components of the masticatory apparatus alone.     

Seasonal variation in thermal energetics of the Australian owlet-nightjar (Aegotheles cristatus)

Many birds living in regions with seasonal fluctuations in ambient temperatures (T_a) typically respond to cold by increasing insulation and adjusting metabolic rate. Seasonal variation in thermal physiology has not been studied for the Caprimulgiformes, an order of birds that generally have basal metabolic rates (BMR) lower than predicted for their body mass. We measured the metabolic rate and thermal conductance of Australian owlet-nightjars (Aegotheles cristatus) during summer and winter using open-flow respirometry. Within the thermoneutral zone (TNZ; 31.3 to 34.8 °C), there was no seasonal difference in BMR or thermal conductance (C), but body temperature was higher in summer- (38.2 ± 0.3 °C) than winter-acclimatized (37.1 ± 0.5 °C) birds. Below the TNZ, resting metabolic rate (RMR) increased linearly with decreasing T_a, and RMR and C were higher for summer- than winter-acclimatized birds. The mean mass-specific BMR of owlet-nightjars (1.27 mL O₂ g^− 1 h^− 1) was close to the allometrically predicted value for a 45 g Caprimulgiformes, but well below that predicted for birds overall. These results suggest that owlet-nightjars increase plumage insulation to cope with low winter T_a, which is reflected in the seasonal difference in RMR and C below the TNZ, rather than adjusting BMR.     

Effects of metabolic level on the body size scaling of metabolic rate in birds and mammals

Metabolic rate is traditionally assumed to scale with body mass to the 3/4-power, but significant deviations from the '3/4-power law' have been observed for several different taxa of animals and plants, and for different physiological states. The recently proposed 'metabolic-level boundaries hypothesis' represents one of the attempts to explain this variation. It predicts that the power (log-log slope) of metabolic scaling relationships should vary between 2/3 and 1, in a systematic way with metabolic level. Here, this hypothesis is tested using data from birds and mammals. As predicted, in both of these independently evolved endothermic taxa, the scaling slope approaches 1 at the lowest and highest metabolic levels (as observed during torpor and strenuous exercise, respectively), whereas it is near 2/3 at intermediate resting and cold-induced metabolic levels. Remarkably, both taxa show similar, approximately U-shaped relationships between the scaling slope and the metabolic (activity) level. These predictable patterns strongly support the view that variation of the scaling slope is not merely noise obscuring the signal of a universal scaling law, but rather is the result of multiple physical constraints whose relative influence depends on the metabolic state of the organisms being analysed.     

Power and metabolic scope of bird flight: a phylogenetic analysis of biomechanical predictions

For flying animals aerodynamic theory predicts that mechanical power required to fly scales as P proportional, variant m (7/6) in a series of isometric birds, and that the flight metabolic scope (P/BMR; BMR is basal metabolic rate) scales as P (scope) proportional, variant m (5/12). I tested these predictions by using phylogenetic independent contrasts from a set of 20 bird species, where flight metabolic rate was measured during laboratory conditions (mainly in wind tunnels). The body mass scaling exponent for P was 0.90, significantly lower than the predicted 7/6. This is partially due to the fact that real birds show an allometric scaling of wing span, which reduces flight cost. P (scope) was estimated using direct measurements of BMR in combination with allometric equations. The body mass scaling of P (scope) ranged between 0.31 and 0.51 for three data sets, respectively, and none differed significantly from the prediction of 5/12. Body mass scaling exponents of P (scope) differed significantly from 0 in all cases, and so P (scope) showed a positive body mass scaling in birds in accordance with the prediction.     

Shape shifting predicts ontogenetic changes in metabolic scaling in diverse aquatic invertebrates

Metabolism fuels all biological activities, and thus understanding its variation is fundamentally important. Much of this variation is related to body size, which is commonly believed to follow a 3/4-power scaling law. However, during ontogeny, many kinds of animals and plants show marked shifts in metabolic scaling that deviate from 3/4-power scaling predicted by general models. Here, we show that in diverse aquatic invertebrates, ontogenetic shifts in the scaling of routine metabolic rate from near isometry (b_R = scaling exponent approx. 1) to negative allometry (b_R < 1), or the reverse, are associated with significant changes in body shape (indexed by b_L = the scaling exponent of the relationship between body mass and body length). The observed inverse correlations between b_R and b_L are predicted by metabolic scaling theory that emphasizes resource/waste fluxes across external body surfaces, but contradict theory that emphasizes resource transport through internal networks. Geometric estimates of the scaling of surface area (SA) with body mass (b_A) further show that ontogenetic shifts in b_R and b_A are positively correlated. These results support new metabolic scaling theory based on SA influences that may be applied to ontogenetic shifts in b_R shown by many kinds of animals and plants.     

Interrelationships between egg mass and adult body mass and metabolism among passerine birds

Summary The regression of egg mass of Passeriformes against female body mass (n=1244) and basal metabolic rate of Passeriformes against body mass (n=159) have similar slopes, indicating that for this group egg mass is directly proportional to basal metabolic rate and that the relative egg mass (% of body mass) is directly proportional to the weight-specific metabolism. This relationship and the average caloric density of passerine eggs (n=38) provides an estimate of the cost of egg production, which for single eggs is 41 % of the basal metabolic rate.

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Beziehungen zwischen Eigewicht, Körpergewicht und Stoffwechsel bei Sperlingsvögeln

Zusammenfassung Die Regressionsgeraden von Eigewichten der Passeriformes und weiblicher Körpergewichte (N=1244) einerseits sowie von Ruheumsatz und Körpergewichten (N=159) andererseits haben vergleichbare Steigungen. Das bedeutet, (1) daß für diese Vogelordnung das Eigewicht proportional zum Ruheumsatz und (2) daß das relative Eigewicht (% des Körpergewichtes) proportional zum gewichtspezifischen Stoffwechsel ist. Dieses Verhältnis und der durchschnittliche kalorische Wert der Eier (N=38) erlauben die Kosten der Eiproduktion zu schätzen: sie betragen für das einzelne Ei 41 % des Ruheumsatzes.

     

The link between metabolic rate and body temperature in galliform birds in thermoneutral and heat exposure conditions: The classical and phylogenetically corrected approach

Three galliform species (grey partridges, ring-necked pheasants, and king quail) were involved in body temperature and resting metabolic rate measurements over a broad range of ambient temperatures (20–45 °C). At thermoneutrality, inter-species differences in colonic temperature, as well as in metabolic rate, were observed. During heat exposure, all species reacted by elevating their body temperatures above 44 °C, thereby inducing temporary hyperthermia. Heat-stressing birds resulted in a slightly increased metabolic rate in king quail, but not in partridges and pheasants. Based on data of body temperature and weight specific (per body mass unit) basal metabolic rate among ten species of Galliformes order, classical and phylogenetically corrected analyses of covariation between these two physiological traits were performed. The scaling of body temperature to body mass, revealed a significant exponent of: −0.0062 and −0.0080 for conventional and phylogenetical methods, respectively. In the analyzed species, a strong positive relationship between residuals of body mass values between body temperature and metabolic rate were found. The results obtained may show a plausible evolutionary link between these traits in galliform birds.     

Size-dependent variations in plant growth rates and the “¾-power rule”

Size-dependent variations in morphological and physiological variables adduced to influence growth rate (e.g., cell surface area and volume, chlorophyll a concentration per cell) were determined by reevaluating published data from unicellular and multicellular plants and animals. With respect to cell volume, reduced major axis regression of the available data indicated that cell surface area decreases roughly as the 0.69-power, the concentration of Chl a decreased roughly as the 0.80-power, and cell mass decreased as the 0.77-power. Computer simulations indicated that the scaling exponent for cell surface area was the consequence of size-dependent variations in cell geometry and aspect ratio (i.e., cell length/width) rather than the result of geometric similitude among cells differing in size. The anisometric relation between cell mass and volume indicated that bulk cell density declines with increasing cell volume. Reanalyses of published data showed that growth rate and weight-specific growth rate scale as the ¾- and negative ¼-power, respectively, with respect to the body mass of unicellular and multicellular plants and animals. It is speculated that the anisometric relation between the growth rate and mass of unicellular plants is attributable to a “dilution” of metabolically active cellular constituents with increasing cell size in combination with the scaling of surface area with respect to volume (and therefore cell mass). It is further speculated that similar biological scalings may account for the ¾-power rule obtained for taxonomically and ecologically diverse multicellular plants and animals.     

Ontogenetic body-mass scaling of resting metabolic rate covaries with species-specific metabolic level and body size in spiders and snakes

According to common belief, metabolic rate usually scales with body mass to the 3/4-power, which is considered by some to be a universal law of nature. However, substantial variation in the metabolic scaling exponent (b) exists, much of which can be related to the overall metabolic level (L) of various taxonomic groups of organisms, as predicted by the recently proposed metabolic-level boundaries (MLB) hypothesis. Here the MLB hypothesis was tested using data for intraspecific (ontogenetic) body-mass scaling of resting metabolic rate in spiders and boid snakes. As predicted, in both animal groups b varies mostly between 2/3 and 1, and is significantly negatively related to L. L is, in turn, negatively related to species-specific body mass (M_m: estimated as the mass at the midpoint of a scaling relationship), and as a result, larger species tend to have steeper metabolic scaling slopes (b) than smaller species. After adjusting for the effects of M_m, b and L are still negatively related, though significantly only in the spiders, which exhibit a much wider range of L than the snakes. Therefore, in spiders and snakes the intraspecific scaling of metabolic rate with body mass itself scales with interspecific variation in both metabolic level and body mass.     

Beyond the '3/4-power law': variation in the intra- and interspecific scaling of metabolic rate in animals

In this review I show that the '3/4-power scaling law' of metabolic rate is not universal, either within or among animal species. Significant variation in the scaling of metabolic rate with body mass is described mainly for animals, but also for unicells and plants. Much of this variation, which can be related to taxonomic, physiological, and/or environmental differences, is not adequately explained by existing theoretical models, which are also reviewed. As a result, synthetic explanatory schemes based on multiple boundary constraints and on the scaling of multiple energy-using processes are advocated. It is also stressed that a complete understanding of metabolic scaling will require the identification of both proximate (functional) and ultimate (evolutionary) causes. Four major types of intraspecific metabolic scaling with body mass are recognized [based on the power function R=aMb, where R is respiration (metabolic) rate, a is a constant, M is body mass, and b is the scaling exponent]: Type I: linear, negatively allometric (b<1); Type II: linear, isometric (b=1); Type III: nonlinear, ontogenetic shift from isometric (b=1), or nearly isometric, to negatively allometric (b<1); and Type IV: nonlinear, ontogenetic shift from positively allometric (b>1) to one or two later phases of negative allometry (b<1). Ontogenetic changes in the metabolic intensity of four component processes (i.e. growth, reproduction, locomotion, and heat production) appear to be important in these different patterns of metabolic scaling. These changes may, in turn, be shaped by age (size)-specific patterns of mortality. In addition, major differences in interspecific metabolic scaling are described, especially with respect to mode of temperature regulation, body-size range, and activity level. A 'metabolic-level boundaries hypothesis' focusing on two major constraints (surface-area limits on resource/waste exchange processes and mass/volume limits on power production) can explain much, but not all of this variation. My analysis indicates that further empirical and theoretical work is needed to understand fully the physiological and ecological bases for the considerable variation in metabolic scaling that is observed both within and among species. Recommended approaches for doing this are discussed. I conclude that the scaling of metabolism is not the simple result of a physical law, but rather appears to be the more complex result of diverse adaptations evolved in the context of both physico-chemical and ecological constraints.     

Basal metabolic rate of endotherms can be modeled using heat-transfer principles and physiological concepts: reply to "can the basal metabolic rate of endotherms be explained by biophysical modeling?"

Our recent article (Roberts et al. 2010 ) proposes a mechanistic model for the relation between basal metabolic rate (BMR) and body mass (M) in mammals. The model is based on heat-transfer principles in the form of an equation for distributed heat generation within the body. The model can also be written in the form of the allometric equation BMR = aM(b), in which a is the coefficient of the mass term and b is the allometric exponent. The model generates two interesting results: it predicts that b takes the value 2/3, indicating that BMR is proportional to surface area in endotherms. It also provides an explanation of the physiological components that make up a, that is, respiratory heat loss, core-skin thermal conductance, and core-skin thermal gradient. Some of the ideas in our article have been questioned (Seymour and White 2011 ), and this is our response to those questions. We specifically address the following points: whether a heat-transfer model can explain the level of BMR in mammals, whether our test of the model is inadequate because it uses the same literature data that generated the values of the physiological variables, and whether geometry and empirical values combine to make a "coincidence" that makes the model only appear to conform to real processes.     

Metabolic rate, maximum metabolism, and advantages of torpor in the fat mouse Steatomys pratensis natalensis Roberts, 1921 (Dendeomurinae)

1. The fat mouse Steatomys pratensis natalensis (mean body mass 37.4±0.43 (se)) has a low euthermic body temperature T_b=30.1–33.8 °C and a low basal metabolic rate (BMR)=0.50 ml O₂ g⁻¹ h⁻¹.

2. Below an ambient temperature (T_a)=15 °C, the mice were hypothermic.

3. The lowest survivable T_a=10 °C.

4. Torpor is efficient in conserving energy between T_a=15–30 °C, below T_a=15 °C, the mice arouse.

5. Euthermic and torpid mice were hyperthermic at T_a=35 °C.

6. Thermal conductance was 0.159 ml O₂ g⁻¹ h⁻¹ °C⁻¹, 98.8% of the expected value.

7. Non-shivering thermogenesis (NST) was 2.196 ml O² g⁻¹ h⁻¹ (3.69×BMR).

8. Maximal oxygen consumption, however, was 3.83 ml O₂ g⁻¹ h⁻¹ (6.44×BMR), indicating that other methods of heat production are additive.

9. Because fat mice conserve energy by torpor only between T_a=15–30 °C, we suggest that torpor may be a more important mechanism for surviving food shortages than for surviving cold weather.

Effects of body lipid content on the resting metabolic rate and postprandial metabolic response in the southern catfish Silurus meridionalis

We assessed the effects of body lipid content on the resting metabolic rate and specific dynamic action (SDA) of the southern catfish Silurus meridionalis. Obese and lean fish were obtained by feeding the fish with two different feeds at 27.5 °C for 4 weeks prior to the experiment. The fish were fed with experimental diets with a meal size of 4% by body mass. A continuous-flow respirometer was used to determine the oxygen consumption rate at 2-h intervals until the postprandial oxygen consumption rate had returned to the preprandial level. The body lipid content of the obese fish was significantly greater than that of the lean fish. The metabolic parameters evaluated (resting metabolic rate, peak metabolic rate (R_peak), factorial ratio, time to peak, duration, energy expended on SDA (SDA_E), or SDA coefficient) were not significantly affected by body fat content in terms of the whole-body or mass-specific values. Increased body fat content did not decrease the resting metabolic rate in the southern catfish, which might be due to the higher levels of highly unsaturated fatty acids in these fish. The results also suggest that the body composition does not appear to affect the SDA response.     

Oscillatory pattern in oxygen consumption of Hummingbirds

Mammals and birds offer the most conspicuous example of homeothermic endothermy, a metabolic feature that implies maintenance of a constant body temperature along broad ranges of ambient temperature. The concept of homeothermic endothermy has been developed in close association with the terms thermoneutral zone and basal metabolic rate. These two metabolic parameters, however, are not easily estimated in micro-endotherms, a difficulty that might emerge from intrinsic aspects of endothermy in minute animals. To address this issue, we used empirical work derived from theoretical considerations. Our theoretical analysis is based on a model of body temperature control by shifts in metabolic rate, and assumes that micro-endotherms lose heat very quickly due to body size, and exhibit a remarkable capacity to rapidly increase metabolic output. We found that these two metabolic traits can lead to non-equilibrium metabolic rate and body temperature. We then measured metabolic rate and body temperature during euthermia in two species of hummingbirds, and analyzed data using the χ² periodogram statistic and a power spectral analysis. We found long-range correlation in both oxygen consumption and body temperature during euthermia, a finding that suggests non-random 1/f oscillations. A similar pattern was not found in the rat, a much larger endotherm. Hummingbirds, then, do not appear to maintain steady-state metabolic conditions during euthermia. If, as we suggest, this pattern applies to micro-endotherms in general, the traditional concepts of thermoneutral zone and basal rate of metabolism might not apply to these animals.     

The theoretical possibility of reverse translation of proteins into genes

It is shown on a theoretical basis that the existence of a “power law” relationship between body mass M and total metabolic heat generation rate Q of the form Q = kM^α does not uniquely determine the dependence of metabolic rate on body temperature. However, it is shown that a particular assumption for this temperature dependence, successful in other problems, does predict a “power law” similar to the empirical one. At the same time it also accounts satisfactorily for the linear dependence of metabolic rate on ambient temperature.     

The scaling and temperature dependence of vertebrate metabolism

Body size and temperature are primary determinants of metabolic rate, and the standard metabolic rate (SMR) of animals ranging in size from unicells to mammals has been thought to be proportional to body mass (M) raised to the power of three-quarters for over 40 years. However, recent evidence from rigorously selected datasets suggests that this is not the case for birds and mammals. To determine whether the influence of body mass on the metabolic rate of vertebrates is indeed universal, we compiled SMR measurements for 938 species spanning six orders of magnitude variation in mass. When normalized to a common temperature of 38 degrees C, the SMR scaling exponents of fish, amphibians, reptiles, birds and mammals are significantly heterogeneous. This suggests both that there is no universal metabolic allometry and that models that attempt to explain only quarter-power scaling of metabolic rate are unlikely to succeed.     

Ontogeny of integumental calcium in relation to surface area and skin water content in the perinatal rat.

Calcium is an important regulator of epidermal differentiation and skin biomechanics in many vertebrate species. In this study, we measured total epidermal calcium in the perinatal Sprague-Dawley rat. Values ranged from 12 to 15 mg per 100 g of tissue. These levels were elevated compared with dermis and other soft (nonbone) organs, including brain, kidney, heart, and liver. Administration of radioactive calcium to the pregnant rat resulted in high rates of 45Ca2+ localization in the fetal epidermis 24 h later. From gestational day 20 to postnatal day 3, the epidermis showed progressive dehydration with water content decreasing from 79 to 73%. Dermal hydration over the same period decreased from 91 to 81%. In the neonatal rat (age 0-3 days), linear regression analysis of surface area vs. body weight on a log-log plot yielded a slope of 1.04. This finding contrasts with an expected slope of 0.67 based on simple surface area-to-volume relationships and differs from the empirical 0.75-power law observed in adult bioenergetics. In summary, these results show the perinatal rat is encapsulated by a continuous differentially hydrated calcium-rich epidermal envelope that increases in surface area over the early postnatal period directly as the first power of body mass.     

Summer acclimatization in the short-tailed field vole,Microtus agrestis

We investigated the changes that occurred in basal and noradrenaline-induced metabolic rate, body temperature and body mass in short-tailed field voles,Microtus agrestis, during exposure to naturally increasing photoperiod and ambient temperature. These parameters were first measured in winter-acclimatized voles (n=8) and then in the same voles which had been allowed to seasonally acclimatize to photoperiod and ambient temperature (6 months later). Noradrenaline induced metabolic rate, basal metabolic rate and nonshivering thermogenesis were significantly higher in winter-acclimatized compared to summer-acclimatized voles. There was a significant positive relationship between basal metabolic rate and noradrenaline-induced metabolic rate. Body mass was significantly higher in summer-acclimatized compared to winter-acclimatized voles. There was a significant positive relationship between body mass and noradrenaline-induced metabolic rate in both winter-acclimalized and summer-acclimatized voles; however, there was no relationship between basal metabolic rate and body mass in either seasonal group of voles. Body temperature after measurements of basal metabolic rate was not significantly different in the seasonal cohorts of voles. However, body temperature was significantly higher in winter-acclimatized compared to summer-acclimatized voles after injection of noradrenaline. Previously we have found that a long photoperiod was not a sufficient stimulus to reduce thermogenic capacity in winter-acclimatized voles during cold exposure, since basal metabolic rate increased to compensate for a reduction in regulatory nonshivering thermogenesis. Here we found that a combination of increased ambient temperature and photoperiod did significantly reduce thermogenic capacity in winter-acclimatized voles. This provided evidence that the two aspects of non-shivering thermogenesis, obligatory and regulatory, are stimulated by different exogenous cues. Summer acclimatization in the shorttailed field vole is manifest as a significant decrease in both basal and noradrenaline-induced metabolic rate, combined with a significant increase in body mass.Abbreviations ANCOV A analysis of covariance - BAT brown adipose tissue - BM body mass - BMR basal metabolic rate - NST non-shivering thermogenesis - NA noradrenaline - V the maximum V recorded following mass specific injection of noradrenaline - V the maximum V recorded following mass specific injection of saline - T _a ambient temperature - T _b rectal body temperature - T _1c lower critical temperature - UCP uncoupling protein - V oxygen consumption     

A unifying explanation for diverse metabolic scaling in animals and plants

The scaling of metabolic rate with body mass has long been a controversial topic. Some workers have claimed that the slope of log-log metabolic scaling relationships typically obeys a universal 3/4-power law resulting from the geometry of resource-transport networks. Others have attempted to explain the broad diversity of metabolic scaling relationships. Although several potentially useful models have been proposed, at present none successfully predicts the entire range of scaling relationships seen among both physiological states and taxonomic groups of animals and plants. Here I argue that our understanding may be aided by three shifts in focus: from explaining average tendencies to explaining variation between extreme boundary limits, from explaining the slope and elevation (metabolic level) of scaling relationships separately to showing how and why they are interrelated, and from focusing primarily on internal factors (e.g. body design) to a more balanced consideration of both internal and external (ecological) factors. By incorporating all of these shifts in focus, the recently proposed metabolic-level boundaries hypothesis appears to provide a useful way of explaining both taxonomic and physiological variation in metabolic scaling relationships. This hypothesis correctly predicts that the scaling slope should vary mostly between 2/3 and 1 and that it should be related to metabolic (activity) level according to an approximately U-shaped function. It also implies that the scaling of other energy-dependent biological processes should be related to the metabolic level of the organisms being examined. Some data are presented that support this implication, but further research is needed.