An experimental test of the thermoregulatory hypothesis for the evolution of endothermy

The thermoregulatory hypothesis proposes that endothermy in mammals and birds evolved as a thermoregulatory mechanism per se and that natural selection operated directly to increase body temperature and thermal stability through increments in resting metabolic rate. We experimentally tested this hypothesis by measuring the thermoregulatory consequences of increased metabolic rate in resting lizards (Varanus exanthematicus). A large metabolic increment was induced by feeding the animals and consequent changes in metabolic rate and body temperature were monitored. Although metabolic rate tripled at 32 degrees C and quadrupled at 35 degrees C, body temperature rose only about 0.5 degrees C. The rate of decline of body temperature in a colder environment did not decrease as metabolic rate increased. Thus, increasing the visceral metabolic rate of this ectothermic lizard established neither consequential endothermy nor homeothermy. These results are inconsistent with a thermoregulatory explanation for the evolution of endothermy.     

Growth estimates from otolith increment widths of juvenile chinook salmon (Oncorhynchus tshawytscha) reared in changing environments

For otolith increments to provide useful estimates of fish growth, otolith growth must covary closely with somatic growth. We reared groups of juvenile chinook salmon ( Oncorhynchus tshawytscha Walbaum) for 70 days, changing ration or temperature during a 20-day treatment period. Restricted rations halted somatic growth, however increment widths decreased gradually; somatic growth was overestimated from increment width. Otolith growth followed changes in water temperature more closely than changes in ration, supporting a hypothesized effect of metabolic rate on otolith growth. Increment growth was only loosely coupled to fish growth rate, and may also be affected by past growth histories. For juvenile fish, increment widths may not be sensitive indicators of short-term changes in growing conditions.     

Correlation among dominance status, metabolic rate and otolith size in masu salmon

In spatial competition between individuals, neither fish sex nor body mass affected dominance status in masu salmon Oncorhynchus masou . In contrast, resting metabolic rate ( M _R) was significantly correlated with dominance status, indicating that a high metabolic rate can increase the dominance rank of juvenile salmon. Whole animal growth rate was significantly correlated with M _R, but not with initial body weight. This suggests that the body size of masu salmon is not a cause, but rather a consequence, of dominance status which is closely related to M _R. The increment width between otolith daily rings was also significantly correlated with M _R. Thus, the size of the Otolith may indicate the degree of M _R.     

The influence of metabolic rate on otolith increment width in Atlantic salmon parr, Salmo salar L.

The influence of metabolic rate on otolith accretion in Atlantic salmon parr was investigated by comparing oxygen consumption rate and increment width in fast and slow growing individuals. Increment width was found to be positively correlated to mean daily oxygen consumption in both fast growing (S1) and slow growing (S2) parr. The results support previous suggestions that a process related to metabolic rate, rather than somatic growth, governs the rate of otolith accretion.     

The effect of feeding on the metabolic rate in harbour seals (Phoca vitulina)

The heat increment of feeding was estimated in harbour seals (Phoca vitulina). Seals were given different amounts of herring, ranging from 0.8 to 2.65 kg. The caloric content of the herring ranged from 6575 to 12560 kJ·kg^-1 depending on time of year. Metabolic rate increased within 30 min after feeding, and the magnitude and duration of heat increment of feeding depended on the size of the meal and the caloric content of the herring. Measured heat increment of feeding was up to 14.9% of gross energy intake and metabolic rate increased as much as 46% above resting, postabsorptive metabolic rate for 15 h duration in a harbour seal with a body weight of approximately 40 kg.     

Effects of temperature,starvation and photoperiod on otolith increments in larval Chinese sucker, <Emphasis Type="Italic">Myxocyprinus asiaticus</Emphasis>

Effects of water temperature, starvation and photoperiod on otolith increment formation in larval Chinese sucker, Myxocyprinus asiaticus, were examined in this study. The results demonstrated that otolith increments of larvae reared under diel temperature fluctuations were very clear and appeared with a high contrast, while those of larvae raised under constant water temperatures were vague or hard to identify. The increment deposition rates were less than 1.0/day in later stage of starvation period. Also, increment deposition was affected by cyclic regimes of water temperature fluctuations, the number of increments corresponded to the cycle times rather than the exact days larvae experienced. However, varying of feeding frequency and photoperiod did not result in any alterations of daily increment formation. Increment width increased obviously with higher rearing temperatures till several days after yolk absorption. However, the width presented an ontogenetic decline during period of endogenous nutrition and the first several days of exogenous nutrition stage. Starvation decoupled the relationship between somatic growth and otolith growth; otolith kept growing, and increment width of starved larvae was similar to those in fed individuals before 9–20 days old; the divergence of increment width from the fed larvae occurred in later stage of starvation period. It can be concluded that temperature regimes and food levels are the major factors affecting increment formation in terms of clarity, deposition rate and width, while photoperiod and feeding frequency have less influence on it.     

Seasonal change in xylem growth of <Emphasis Type="Italic">Pinus densiflora</Emphasis> in central Japan

This study investigated the seasonal change in xylem growth of Japanese red pine (Pinus densiflora). Wood cores were sampled at 2-week intervals from April to November in 2012 using the microcoring method. Daily increment rates of tracheid number and tree-ring width were compared with seasonal changes in daily mean temperature and photoperiod. Xylem growth started in early to late May and stopped in late October to early November. The maximum daily increment rates of tracheid number and tree-ring width were in early July. The 95 % confidence intervals of the timing of the maximum daily increment rates included the summer solstice (23 June) with the longest photoperiod, but not the warmest day (30 July). The maximum daily increment rate of xylem growth is thought to be controlled by the photoperiod rather than by temperature. The daily mean temperature exceeded 20 °C after the summer solstice, indicating that temperature is not a limiting factor for xylem growth. This study suggests that the timing of maximum daily increment rates of xylem growth of P. densiflora is controlled by the photoperiod.     

Is the marginal otolith increment width a reliable recent growth index for larval and juvenile herring?

Marginal otolith increment width analysis was performed on field‐collected larval and juvenile spring‐spawned herring Clupea harengus that experienced variable feeding conditions and high temperatures that were above the optimum for growth. Although drastic zooplankton biomass reduction had a significant effect on increment width, a delay of a few days in the otolith response was observed. More importantly, a very clear, positive temperature effect on marginal increment width was demonstrated in fish characterized by temperature independent somatic growth. These results indicate that under natural conditions it may be impossible to distinguish increment width changes related to variation in feeding conditions from changes caused by temperature fluctuations. Therefore, it was concluded that marginal otolith increment width analysis could not be used as a recent growth index ( I _G) for herring larvae and juveniles exposed to drastic temperature fluctuations. The implication of these results is significant not only for the use of marginal increments as a recent growth index, but also if growth rate backcalculation is to be used as a research method.     

The relationship between specific dynamic action and otolith growth in pike

The hypothesis was tested that the daily increment width (IW) of the otolith comprises two components, one that correlates with basal metabolic rate (as has been demonstrated previously) and the other that correlates with apparent specific dynamic action ( R _sda)(the post‐prandial elevation in metabolism). Simultaneous measurements of IW and metabolic rate before and after a meal were collected from individual pike Esox lucius . After feeding, IW and metabolic rate increased above basal levels for 5–6 days. There was no correlation between daily IW and R _sda, reflecting within‐individual difference in the shapes of the post‐prandial responses of the two variables. There was a significant relationship between the total changes of IW and metabolic rate integrated following meals. The magnitude of the post‐prandial response as a proportion of the basal level was larger for metabolic rate than IW, mirroring the previously reported responses of these variables to acute temperature change. This study suggests that analysis of IW has the potential to provide a historic record of energy intake but only when integrated over a period equivalent to the digestion time. Consideration of energy budget theory indicates that IW is unlikely to provide a robust record of short‐term somatic growth if activity metabolism is significant and variable.     

The influence of temperature,sexual condition,and season on the metabolic rate of the lizardPsammodromus hispanicus

Summary Male and femalePsammodromus hispanicus from southern Europe were acclimated to four seasonal conditions of photoperiod and night time temperature. During the dark period, the lizards' body temperatures fell to ambient air temperature but during the light period the lizards were allowed to thermoregulate behaviourally and at such times the lizards' mean body temperature varied from 29.0°C to 32.6°C. The resting metabolic rate of these lizards was measured in 5°C steps from 5°C to 30°C or 35°C. Sexual condition had little effect on resting metabolic rate, but at low temperatures lizards acclimated to winter or spring seasonal conditions had lower resting metabolic rates than those acclimated to summer or autumn conditions. At temperatures above 20°C seasonal acclimation had no effect on resting metabolic rate. It is considered that the reduction in low temperature metabolic rate in spring and winter is induced by low night time temperatures and serves to conserve energy during those seasons when lizards must spend long periods at low temperature without being able to feed.     

广东罗坑自然保护区鳄蜥的体温调节及静止代谢率的热依赖性

探讨鳄蜥（Shinisaurus crocodilurus）的体温调节和静止代谢率及其热依赖性特征,测定了在自然和实验室条件下的环境温度、鳄蜥体温以及静止代谢率（RMR）等热生物学指标。结果显示：在自然条件下,鳄蜥的野外活动体温（Th）稍高于基质温度（Tc）和空气温度（Td）并与后二者呈正相关关系（Tb=11．65＋0．47Tc,r^2=0．34,F1.75=39．11,P〈0．0001;Tb=11．61＋0．46Td,r^2=0．56,F1.75=96．56,P〈0．0001）。鳄蜥在野外的活动体温存在明显的月份间差异,但无性别及年龄上的差异。环境温度为15℃-30℃的实验条件下,鳄蜥的静止体温（Tb）与环境温度（Ta）呈正相关关系：Tb=12．450＋0．5641Ta（F1.110=11．34,r^2=0．997,P〈0．001）;在缺乏温度梯度的环境中,尽管鳄蜥的体温、空气温度和基质温度都有显著的昼夜差异,但体温、空气温度和基质温度的日平均温度之间无显著差异。鳄蜥的RMR不存在雌雄个体间的差异,并与环境温度呈正相关关系。分析显示鳄蜥的体温既有行为调节也有生理调节,其体温调节及RMR符合变温动物的热生物学特征,但是相对于其他活动较多的蜥蜴而言,鳄蜥的生理调节能力较强,这可能与其活动时间分配中静栖占绝大部分的行为特点是相适应的[动物学报54（6）：964-971,2008]。     

Effects of short-term acclimation on thermoregulatory responses of the rock kestrel, Falco rupicolus

The effects of a short-term acclimation period on basal metabolic rate (BMR) and resting metabolic rate (RMR) were measured in captive-bred Rock Kestrels (Falco rupicolus). Birds were exposed to winter conditions (pre-acclimation) in a semi-natural environment before they were acclimated for a period of 3 weeks at a constant temperature of 25 °C and a constant light:dark cycle (12:12 h) (post-acclimation). After acclimation the kestrels showed changes in RMR, BMR and the width of the thermoneutral zone. There was inter- and intra-individual phenotypic plasticity in BMR and RMR both pre- and post-acclimation. However, more inter-individual variation was seen after acclimation. This study concurs with recent suggestions that phenotypic plasticity in BMR is prevalent in avian physiology, and thus a single-species-specific BMR value may not be representative. Furthermore, comparative avian studies of BMR need to account for phenotypic plasticity.     

The effect of fasting on activity and resting metabolism in the sand cricket, Gryllus firmus: a multivariate approach

Heat increment of feeding (HIF) is a ubiquitous feature of animals, and corresponds to a conspicuous rise in metabolism after a meal, induced by the release of energy due to digestion and absorption of foodstuffs. However, there exists great variation both in the duration and magnitude of HIF. In insects, HIF is well known, and it appears to be dramatic, especially in immature stages. However, little is known about the effect of HIF on different aspects of metabolism. We determined metabolic rate as CO2 production in fasted and non-fasted nymphs of the sand cricket (Gryllus firmus). A number of metabolic variables were computed from the simultaneous activity record: activity, resting, minimum, maximum and average metabolic rate. Our results suggest that there is a general effect of fasting in metabolic rate but with a graded response: the larger the influence of activity on the metabolic variable, the less is the effect of fasting that was detected.     

冷驯化对中缅树鼩产热能力的影响

在 ( 5± 1)℃条件下对中缅树 (Tupaiabelangeri)进行低温胁迫处理 ( 0～ 2 8d) ,测定其冷驯化过程中的静止代谢率 (RMR)、非颤抖性产热 (NSTmax)、冷诱导最大产热 (CIRMR)、体重、体温等生理指标 ,探讨低温对中缅树产热能力的影响。结果表明 :①冷驯化期间中缅树体重增加 ,体温降低 ,产热能力显著增强 ;②在冷驯化过程中 ,增加RMR和CIRMR是中缅树抵抗低温胁迫的主要产热模式。     

Energetic costs and thermoregulation in northern fur seal (Callorhinus ursinus) pups: the importance of behavioral strategies for thermal balance in furred marine mammals

Behavioral thermoregulation represents an important strategy for reducing energetic costs in thermally challenging environments, particularly among terrestrial vertebrates. Because of the cryptic lifestyle of aquatic species, the energetic benefits of such behaviors in marine endotherms have been much more difficult to demonstrate. In this study, I examined the importance of behavioral thermoregulation in the northern fur seal (Callorhinus ursinus) pup, a small-bodied endotherm that spends prolonged periods at sea. The thermal neutral zones of three weaned male northern fur seal pups (body mass range = 11.8-12.8 kg) were determined by measuring resting metabolic rate using open-flow respirometry at water temperatures ranging from 2.5° to 25.0°C. Metabolic rate averaged 10.03 ± 2.26 mL O?kg?1 min?1 for pups resting within their thermal neutral zone; lower critical temperature was 8.3° ± 2.5°C , approximately 8°C higher than the coldest sea surface temperatures encountered in northern Pacific waters. To determine whether behavioral strategies could mitigate this potential thermal limitation, I measured metabolic rate during grooming activities and the unique jughandling behavior of fur seals. Both sedentary grooming and active grooming resulted in significant increases in metabolic rate relative to rest (P = 0.001), and percent time spent grooming increased significantly at colder water temperatures (P < 0.001). Jughandling metabolic rate (12.71 ± 2.73 mL O?kg?1 min ?1) was significantly greater than resting rates at water temperatures within the thermal neutral zone (P < 0.05) but less than resting metabolism at colder water temperatures. These data indicate that behavioral strategies may help to mitigate thermal challenges faced by northern fur seal pups while resting at sea.     

Resting metabolism and heat increment of feeding in mandarin fish (Siniperca chuatsi) and Chinese snakehead (Channa argus)

Resting metabolism was measured in immature mandarin fish Siniperca chuatsi weighing 42.1-510.2 g and Chinese snakehead Channa argus weighing 41.5-510.3 g at 10, 15, 20, 25, 30 and 35 degrees C. Heat increment of feeding was measured in mandarin fish weighing 202.0 (+/-14.0) g and snakehead weighing 200.8 (+/-19.3) g fed swamp loach Misgurnus anguillicaudatus at 1% body weight per day at 28 degrees C. In both species, weight exponent in the power relationship between resting metabolism and body weight was not affected by temperature. The relationship between resting metabolism and temperature could be described by a power function. The temperature exponent was 1.39 in mandarin fish and 2.10 in snakehead (P<0.05), indicating that resting metabolism in snakehead increased with temperature at a faster rate than in mandarin fish. Multiple regression models were used to describe the effects of body weight (W, g) and temperature (T, degrees C) on the resting metabolism (R(s), mg O(2)/h): lnR(s)=-5.343+0.772 lnW+1.387 lnT for the mandarin fish and lnR(s)=-7.863+0.801 lnW+2.104 lnT for the Chinese snakehead. The proportion of food energy channelled to heat increment was 8.7% in mandarin fish and 6.8% in snakehead.     

Metabolic effects of low-energy diet on steller sea lions, Eumetopias jubatus

Diets of six Steller sea lions (Eumetopias jubatus) were switched between a high (herring) and a low (squid) energy density food for 14 d to determine the effects on ingested prey mass, body mass, resting metabolic rate, and the heat increment of feeding. Body mass was measured daily, and resting metabolism was measured weekly by gas respirometry. Ingested food mass did not differ significantly between the squid diet and the control or the recovery herring diet periods. As a result of differences in energy density, gross energy intake was significantly lower during the squid diet phase than during either the control or recovery periods. As a result, sea lions lost an average of 1.1 kg/d, totaling 12.2% of their initial body mass by the end of the experimental period. The heat increment of feeding for a 4-kg squid meal was significantly lower than for a similarly sized meal of herring. Decreases in both absolute (24.0 to 18.0 MJ/d, -24%) and mass-corrected (903 to 697 kJ/d/kg0.67, -20%) metabolism were observed by the end of the squid feedings. This study suggests that sea lions can depress their resting metabolism in response to decreases in energy intake or body mass, regardless of satiation level.     

Metabolic depression in animals: physiological perspectives and biochemical generalizations

Depression of metabolic rate has been recorded for virtually all major animal phyla in response to environmental stress. The extent of depression is usually measured as the ratio of the depressed metabolic rate to the normal resting metabolic rate. Metabolic rate is sometimes only depressed to approx. 80% of the resting value (i.e. a depression of approx. 20% of resting); it is more commonly 5-40 % of resting (i.e. a depression of approx. 60-95% of resting); extreme depression is to 1% or less of resting, or even to an unmeasurably low metabolic rate (i.e. a depression of approx. 99-100% of resting). We have examined the resting and depressed metabolic rate of animals as a function of their body mass, corrected to a common temperature. This allometric approach allows ready comparison of the absolute level of both resting and depressed metabolic rate for various animals, and suggests three general patterns of metabolic depression. Firstly, metabolic depression to approx. 0.05-0.4 of rest is a common and remarkably consistent pattern for various non-cryptobiotic animals (e.g. molluscs, earthworms, crustaceans, fishes, amphibians, reptiles). This extent of metabolic depression is typical for dormant animals with ‘intrinsic’ depression, i.e. reduction of metabolic rate in anticipation of adverse environmental conditions but without substantial changes to their ionic or osmotic status, or state of body water. Some of these types of animal are able to survive anoxia for limited periods, and their anaerobic metabolic depression is also to approx. 0.05-0.4 of resting. Metabolic depression to much less than 0.2 of resting is apparent for some ‘resting’, ‘over-wintering’ or diapaused eggs of these animals, but this can be due to early developmental arrest so that the egg has a low ‘metabolic mass’ of developed tissue (compared to the overall mass of the egg) with no metabolic depression, rather than having metabolic depression of the entire cell mass. A profound decrease in metabolic rate occurs in hibernating (or aestivating) mammals and birds during torpor, e.g. to less than 0.01 of pre-torpor metabolic rate, but there is often no intrinsic metabolic depression in addition to that reduction in metabolic rate due to readjustment of thermoregulatory control and a decrease in body temperature with a concommitant Q₁₀ effect. There may be a modest intrinsic metabolic depression for some species in shallow torpor (to approx. 0.86) and a more substantial metabolic depression for deep torpor (approx. 0.6), but any energy saving accruing from this intrinsic depression is small compared to the substantial savings accrued from the readjustment of thermoregulation and the Q₁₀ effect. Secondly, a more extreme pattern of metabolic depression (to < 0.05 of rest) is evident for cryptobiotic animals. For these animals there is a profound change in their internal environment-for anoxybiotic animals there is an absence of oxygen and for osmobiotic, anhydrobiotic or cryobiotic animals there is an alteration of the ionic/osmotic balance or state of body water. Some normally aerobic animals can tolerate anoxia for considerable periods, and their duration of tolerance is inversely related to their magnitude of metabolic depression; anaerobic metabolic rate can be less than 0.005 of resting. The metabolic rate of anhydrobiotic animals is often so low as to be unmeasurable, if not zero. Thus, anhydrobiosis is the ultimate strategy for eggs or other stages of the life cycle to survive extended periods of environmental stress. Thirdly, a pattern of absence of metabolism when normally hydrated (as opposed to anhydrobiotic or cryobiotic) is apparently unique to diapaused eggs of the brine-shrimp (Artemia spp., an anostracan crustacean) during anoxia. The apparent complete metabolic depression of anoxic yet hydrated cysts (and extreme metabolic depression of normoxic, hypoxic, or osmobiotic, yet hydrated cysts), is an obvious exception to the above patterns. In searching for biochemical mechanisms for metabolic depression, it is clear that there are five general characteristics at the molecular level of cells which have a depressed metabolism; a decrease in pH, the presence of latent mRNA, a change in protein phosphorylation state, the maintenance of one particular energy-utilizing process (ion pumping), and the down-regulation of another (protein synthesis). Oxygen sensing is now the focus of intense investigation and obviously plays an important role in many aspects of cell biology. Recent studies show that oxygen sensing is involved in metabolic depression and research is now being directed towards characterising the proteins and mechanisms that comprise this response. As more data accumulate, oxygen sensing as a mechanism will probably become the sixth general characteristic of depressed cells. The majority of studies on these general characteristics of metabolically depressed cells come from members of the most common group of animals that depress metabolism, those non-cryptobiotic animals that remain hydrated and depress to 0.05-0.4 of rest. These biochemical investigations are becoming more molecular and sophisticated, and directed towards defined processes, but as yet no complete mechanism has been delineated. The consistency of the molecular data within this group of animals suggests similar metabolic strategies and mechanisms associated with metabolic depression. The biochemical ‘adaptations’ of anhydrobiotic organisms would seem to be related more to surviving the dramatic reduction in cell water content and its physico-chemical state, than to molecular mechanisms for lowering metabolic rate. Metabolic depression would seem to be an almost inevitable consequence of their altered hydration state. The unique case of profound metabolic depression of hydrated Artemia spp. cysts under a variety of conditions could reflect unique mechanisms at the molecular level. However, the available data are not consistent with this possibility (with the exception of a uniquely large decrease in ATP concentration of depressed, hydrated Artemia spp. cysts) and the question remains: how do cells of anoxic and hydrated Artemia spp. differ from anoxic goldfish or turtle cells, enabling them so much more completely to depress their metabolism?     

Comparative non-shivering thermogenesis in adjacent populations of the common spiny mouse (Acomys cahirinus) from opposite slopes: the effects of increasing salinity

We compared non-shivering thermogenesis between two adjacent populations of the common spiny mouse Acomys cahirinus from different habitats, in relation to increasing salinity. Individuals were captured from the north- and south-facing slopes of the same valley, that represent "Mediterranean" and "desert" habitats, respectively. We hypothesized that the two populations of mice would differ in their thermoregulatory capacities, reflecting their need to cope with the environmental stress in each habitat. We measured resting metabolic rate by recording oxygen consumption, body temperature and response to an injection of exogenous noradrenaline. Mice were maintained on diets with increasing levels of salt intake to examine their abilities to cope with increasing osmotic stress. Mice from north-facing slopes generally had a higher resting metabolic rate and a higher increase in oxygen consumption in response to noradrenaline than mice from south-facing slopes. Increasing salinity decreased resting metabolic rate values, body temperature, and oxygen consumption in response to noradrenaline in both populations, and diminished slope-dependant differences. We suggest that these differences could be a result of an ongoing adaptive process to different climatic conditions, typical of the Mediterranean region, that are a demonstrable example of evolution in action.     

Energetically costly behaviour and the evolution of resting metabolic rate in insects

1. A general hypothesis is presented to explain interspecific differences in size-independent resting metabolic rate. This hypothesis is based on a presumed trade-off between a low resting metabolism and adaptations of metabolism during activity.
2. With such a trade-off, selection to reduce resting metabolism is less intense in active species than in species where resting metabolism constitutes a large proportion of the daily metabolic costs. Those animals that spend more energy on activity should therefore have a higher resting metabolic rate than animals that spend less energy on activity.
3. A literature review reveals that flying insects have higher resting metabolic rates than species that use energetically less demanding types of locomotion.
4. Insects producing acoustic advertisement signals can be shown to have higher mass-independent resting metabolic rates than closely related species without this energetically demanding behaviour.
5. Literature data on vertebrate resting metabolic rates are also consistent with the presented hypothesis: the more energy animals spend on activity, the higher the mass-independent resting metabolic rate.