Warm-up rates during arousal from torpor in heterothermic mammals: physiological correlates and a comparison with heterothermic insects

Summary This study examines the relationship between warm-up rate, body mass, metabolic rate, thermal conductance and normothermic body temperature in heterothermic mammals during arousal from torpor. Predictions based on the assumption that the energetic cost of arousal has been minimised are tested using data for 35 species. The observation that across-species warm-up rate correlates negatively with body mass is confirmed using a comparative technique which removes confounding effects due to the non-independence of species data due to shared common ancestry. Mean warm-up rate during arousal correlates negatively with basal metabolic rate and positively with the temperature difference through which the animal warms, having controlled for other factors. These results suggest that selection has operated to minimise the overall energetic, cost of warm-up. In contrast, peak warm-up rate during arousal correlates positively with peak metabolic rate during arousal, and negatively with thermal conductance, when body mass has been taken into account. These results suggest that peak warm-up rate is more sensitive to the fundamental processes of heat generation and loss. Although heterothermic marsupials have lower normothermic body temperatures and basal metabolic rates, marsupials and heterothermic eutherian mammals do not differ systematically in warm-up rate. Pre-flight warm-up rates in one group of endothermic insects, the bees, are significantly higher than predictions based on rates of arousal of a mammal of the same body mass.Abbreviations BMR basal metabolic rate - ICM independent comparisons method - MWR mean warm-up rate - PMR peak metabolic rate - PWR peak·warm-up rate - Tb_activity body temperature during activity - Tb_torpor body temperature during torpor - T _arousal increase in body temperature during arousal     

Thermal constraints for stingless bee foragers: the importance of body size and coloration

In the dry tropics, foraging bees face significant thermal constraints as a result of high ambient temperatures and direct insolation. In order to determine the potential importance of body size and body coloration in heat gain and heat loss, passive warm-up and cooling rates were measured for freshly killed workers of 24 stingless bee species. Results accorded with biophysical principles. Small bees reached lower temperature excesses (T_exc) and warmed up and lost heat much more rapidly than larger bees. In addition to body size, body coloration had a clear effect on thermal parameters. Light-coloured bees warmed up less rapidly and had lower T_exc than dark bees. An intraspecific comparison of Melipona costaricensis and Cephalotrigona capitata colour morphs confirmed that body coloration influences thermal characteristics. This study is the first to indicate that abdominal coloration in stingless bees might be involved in the regulation of body temperature in extreme thermal conditions. However, body temperatures of foraging bees of colour morphs were not very different. This is probably due to behavioural adaptations (e.g. foraging strategies) or differences in convective and evaporative heat loss or the production of metabolic heat during flight, that all mask the effect of body colour. Notwithstanding such effects and potential thermoregulatory capabilities, stingless bees show niche differentiation and biogeographic distributions that correlate with body coloration and body size. This also suggests that, in general, light bees have an advantage over black bees in hot open lowland habitats, whereas black bees might have an advantage in wet habitats and mountains. The origin, occurrence and function of flavinism (yellow integument colouring) are discussed.     

What does determine gonad weight in the wild kissing bug Mepraia spinolai

Female fecundity increases with body size in a variety of insects, but it is unknown if this generalization applies for kissing bugs. In this study, we evaluate whether gonad weight in the bloodsucking insect Mepraia spinolai correlates with body size, or determined by nutrition or developmental time. We found that the investment on reproductive tissue correlates positively and significantly with body size and with the amount of ingested blood by female insects along their lifespan. Total molting time did not significantly affect gonad weight. We suggest that under optimal feeding conditions M. spinolai females could express their maximum reproductive potential.     

Per-stage growth rates of head and body sizes in scarab larvae (Coleoptera: Scarabaeidae) decrease across ontogeny following a species-specific pattern

It has been widely assumed that the stepwise increase in the exoskeleton size of larval insects approximately follows a geometric progression from instar to instar, known as Dyar's Rule. However, it is not clear whether the per-instar increase in body size follows this rule. In insects, Dyar's Rule has been identified either by regressing the log-scaled size on the instar number (log-linear regression analysis) or by comparing the postmolt/premolt size ratio between instars (growth rate analysis). A previous study on the body mass of caterpillars showed the methodological pitfall that Dyar's Rule was statistically supported by log-linear regression analysis, but not at all by growth rates analysis. I considered this concern here by examining the per-stage growth rates of head and body sizes for larvae of the beetle Trypoxylus dichotomus using both methods and compared the resulting growth rates for body size within and between taxonomic orders. Dyar's Rule was statistically supported by the log-linear regression analysis but not by growth rate analysis for both the head and body sizes in T. dichotomus. The body size growth rate in T. dichotomus decreased as the instar progressed. This developmental pattern was also found in reported data for the other six scarabs, but not in data for Lepidoptera or Hymenoptera. These findings confirm that the per-stage growth rate of body size does not follow Dyar's Rule in a wide range of insects, and suggest that developmental change in the body size growth rate varies among insect groups.     

Convective and evaporative cooling in sawfly larvae

Responses to radiant and convective heat input were analysed in the gregarious larvae of Perga dorsalis (0·5-2·5 g body weight). Aggregating diminishes convective heat loss from each individual and augments the body temperature of larvae in the sun. Voluntary raising of the abdomen, occurring at body temperatures above about 30·4°C, increases convective heat loss. At body temperatures above about 37°C, a filtrate from the semiliquid midgut contents is excreted from the anus and spread over the body. This increases evaporative heat loss and maintains the body temperature below the critical thermal maximum (42°C) even when ambient temperature rises to 48°C. Based on the tolerance to water loss (17 per cent of the body weight) and the rates of evaporation, it is evident that evaporative cooling may be employed successfully throughout the hottest hours of the day.     

Thermal conditions for successful breeding in Great Tits (Parus major L.)

Summary The development of temperature regulation in relation to the growth and age of the nestlings is described in a way permitting use of the data in a model designed to predict the range of temperature tolerance of broods of Great Tits in the nestling stage. Such a model is described in a second paper. The physiological part of that model is made up mainly of six equations (nos. 6, 10, 11, 12, 14 and 15), which are all presented and discussed here. It is shown in this paper that the development of temperature regulation is a function of body weight rather than of age. The level of the basal metabolic rate of nestling Great Tits is lower than that of adult passerines of comparable size. The basal metabolic rate of a newly hatched Great Tit is only about one fourthe of the metabolic rate expected from Lasiewski and Dawson's equation for adult passerine birds. This discrepancy diminishes gradually during the nestling period and disapears shortly before fledging.Basal and maximum metabolic rates, as well as the body temperatures coinciding with these rates, are described in allometric equations as functions of nestling body weight. The evaporative heat loss of the nestlings is described as a function of body weight and body temperature, and an estimate of the maximum amount of water available to them for evaporative heat loss is given. A distinction is made between a long-term risk of hyperthermia, which results in mortality through dehydration of the nestling body, and an immediate risk of hyperthermia, which occurs when the maximum rate at which nestlings can evaporate water is insufficient to cope with the required heat loss by water evaporation. It is concluded that this immediate risk of hyperthermia is the most important of the factors affecting the upper limit of the range of temperature tolerance.     

Adaptation of the Thermal Responses of Insects

SYNOPSIS. Some insects adjust heat production and heat loss,while others depend upon adjustments in location and postureto regulate body temperature. Many activities oE insects aretuned to internal temperature. These two features predict thatthe nature and form of temperature control in insects interactstrongly in adaptation to climate, energy demand, niche specialization,and population size of insects.     

Energetic inequivalence in eusocial insect colonies

The energetic equivalence rule states that population-level metabolic rate is independent of average body size. This rule has been both supported and refuted by allometric studies of abundance and individual metabolic rate, but no study, to my knowledge, has tested the rule with direct measurements of whole-population metabolic rate. Here, I find a positive scaling of whole-colony metabolic rate with body size for eusocial insects. Individual metabolic rates in these colonies scaled with body size more steeply than expected from laboratory studies on insects, while population size was independent of body size. Using consumer-resource models, I suggest that the colony-level metabolic rate scaling observed here may arise from a change in the scaling of individual metabolic rate resulting from a change in the body size dependence of mortality rates.     

A review of the energetics of pollination biology

Pollination biology is often associated with mutualistic interactions between plants and their animal pollen vectors, with energy rewards as the foundation for co-evolution. Energy is supplied as food (often nectar from flowers) or as heat (in sun-tracking or thermogenic plants). The requirements of pollinators for these resources depend on many factors, including the costs of living, locomotion, thermoregulation and behaviour, all of which are influenced by body size. These requirements are modified by the availability of energy offered by plants and environmental conditions. Endothermic insects, birds and bats are very effective, because they move faster and are more independent of environmental temperatures, than are ectothermic insects, but they are energetically costly for the plant. The body size of endothermic pollinators appears to be influenced by opposing requirements of the animals and plants. Large body size is advantageous for endotherms to retain heat. However, plants select for small body size of endotherms, as energy costs of larger size are not matched by increases in flight speed. If high energy costs of endothermy cannot be met, birds and mammals employ daily torpor, and large insects reduce the frequency of facultative endothermy. Energy uptake can be limited by the time required to absorb the energy or eliminate the excess water that comes with it. It can also be influenced by variations in climate that determine temperature and flowering season.     

Prothoracicotropic hormone regulates developmental timing and body size in Drosophila

In insects, control of body size is intimately linked to nutritional quality as well as environmental and genetic cues that regulate the timing of developmental transitions. Prothoracicotropic hormone (PTTH) has been proposed to play an essential role in regulating the production and/or release of ecdysone, a steroid hormone that stimulates molting and metamorphosis. In this report, we examine the consequences on Drosophila development of ablating the PTTH-producing neurons. Surprisingly, PTTH production is not essential for molting or metamorphosis. Instead, loss of PTTH results in delayed larval development and eclosion of larger flies with more cells. Prolonged feeding, without changing the rate of growth, causes the overgrowth and is a consequence of low ecdysteroid titers. These results indicate that final body size in insects is determined by a balance between growth-rate regulators such as insulin and developmental timing cues such as PTTH that set the duration of the feeding interval.     

Scaling of insulation in seals and whales

We describe scaling of morphological variables that influence total insulation in eight species of marine mammals ranging in average size from 35 to 30000 kg. We also calculate total heat loss and the partitioning of heat loss through the body surface and appendages. For the eight species investigated, heat loss in 0°C water is appreciably higher than the predicted basal metabolic rates for small species such as the ringed seal. Rorquals, on the other hand, will probably not need to raise their metabolic rates to keep warm. At rest, 10–30% of the heat production of a resting animal is lost through flippers, fins and flukes. This amount can increase to 70–80% during moderate exercise. Whole-body conductance scales with body size in the same way in marine as in terrestrial mammals, although conductance is higher for a given body size in a marine mammal.     

Front Cover

Courtship displays are typically comprised of the same behavioral pattern, or patterns, repeated several times by males. Both the quantity and quality of the displays produced by a given male bird are not, however, constant. The number and/or quality of displays can decrease over time, indicating fatigue, or males can increase the number and/or quality as they display more, indicating a warm-up period. Although there is evidence for fatigue or warm-up periods for many types of courtship displays, data on motor components of avian courtship are scant, despite how commonly they are used. Here, we test whether drumming, a non-vocal motor display, in male ruffed grouse (Bonasa umbellus) changes in relation to the number of displays executed. Using a large number of recordings, our linear mixed models yielded a significant effect of cumulative number of drumming displays on the number of wingbeats per second, referred to as pulse rate. Across males, pulse rate is slowest when males begin drumming each day and increases until approximately 50 drumming displays have been produced. The rate of increase is also modulated by the nighttime low temperature such that cooler conditions are associated with lower pulse rates and a slower increase in pulse rate relative to the cumulative number of displays. Further, the maximum pulse rate recorded and average pulse rate after 50 displays is inversely correlated with body mass such that larger males are slower than smaller males. We suggest that the daily changes in pulse rate likely reflect a warm-up period based upon the effects of cumulative drumming count and temperature on pulse rate. Whether these dynamic changes in the production of a motor display are informative to female grouse is unknown. However, we propose that daily changes in how motor displays are performed may be a common feature of avian courtship that has gone relatively unnoticed, despite the potential for motor performance to be a trait that is important for female mate choice.     

Why mammalian lineages respond differently to sexual selection: metabolic rate constrains the evolution of sperm size

The hypothesis that sperm competition should favour increases in sperm size, because it results in faster swimming speeds, has received support from studies on many taxa, but remains contentious for mammals. We suggest that this may be because mammalian lineages respond differently to sexual selection, owing to major differences in body size, which are associated with differences in mass-specific metabolic rate. Recent evidence suggests that cellular metabolic rate also scales with body size, so that small mammals have cells that process energy and resources from the environment at a faster rate. We develop the 'metabolic rate constraint hypothesis' which proposes that low mass-specific metabolic rate among large mammals may limit their ability to respond to sexual selection by increasing sperm size, while this constraint does not exist among small mammals. Here we show that among rodents, which have high mass-specific metabolic rates, sperm size increases under sperm competition, reaching the longest sperm sizes found in eutherian mammals. By contrast, mammalian lineages with large body sizes have small sperm, and while metabolic rate (corrected for body size) influences sperm size, sperm competition levels do not. When all eutherian mammals are analysed jointly, our results suggest that as mass-specific metabolic rate increases, so does maximum sperm size. In addition, species with low mass-specific metabolic rates produce uniformly small sperm, while species with high mass-specific metabolic rates produce a wide range of sperm sizes. These findings support the hypothesis that mass-specific metabolic rates determine the budget available for sperm production: at high levels, sperm size increases in response to sexual selection, while low levels constrain the ability to respond to sexual selection by increasing sperm size. Thus, adaptive and costly traits, such as sperm size, may only evolve under sexual selection when metabolic rate does not constrain cellular budgets.     

Genetic variation in spontaneous ovulation rate and LH receptor induction in mice

Selection for litter size (Line S1) and for post-weaning body weight gain (Line G) increased spontaneous ovulation rate in mature females by 69 and 73%, respectively, over that of randomly bred control mice (Line C). Inbreeding from S1 mice with selection for litter size produced highly inbred lines with elevated ovulation rates. Inbreeding from Line C mice produced a 21% divergence among lines, but did not depress the mean ovulation rate. Crosses of these lines revealed little heterosis in ovulation rate. LH receptors were induced by treating females from 22 days of age with diethylstilboestrol for 4 days and FSH for 2 days. The in-vitro binding of 125I-labelled hCG per microgram DNA decreased 56% in response to selection for litter size and increased 57% in response to selection for body weight gain, indicating high susceptibility of this trait to genetic change. Inbreeding from Line C mice produced a 135% divergence amongst lines, but did not depress the mean LH receptor induction. Body weight had significant effects on ovulation rate and LH receptor induction. These results show that selection for litter size and for rapid post-weaning body weight gain increases ovulation rate, but we suggest that different mechanisms are involved in these responses.     

The constraints of body size on aerodynamics and energetics in flying fruit flies: an integrative view

Reynolds number and thus body size may potentially limit aerodynamic force production in flying insects due to relative changes of viscous forces on the beating wings. By comparing four different species of fruit flies similar in shape but with different body mass, we have investigated how small insects cope with changes in fluid mechanical constraints on power requirements for flight and the efficiency with which chemical energy is turned into aerodynamic flight forces. The animals were flown in a flight arena in which stroke kinematics, aerodynamic force production, and carbon dioxide release were measured within the entire working range of the flight motor. The data suggest that during hovering performance mean lift coefficient for flight is higher in smaller animals than in their larger relatives. This result runs counter to predictions based on conventional aerodynamic theory and suggests subtle differences in stroke kinematics between the animals. Estimates in profile power requirements based on high drag coefficient suggest that among all tested species of fruit flies elastic energy storage might not be required to minimize energetic expenditures during flight. Moreover, muscle efficiency significantly increases with increasing body size whereas aerodynamic efficiency tends to decrease with increasing size or Reynolds number. As a consequence of these two opposite trends, total flight efficiency tends to increase only slightly within the 6-fold range of body sizes. Surprisingly, total flight efficiency in fruit flies is broadly independent of different profile power estimates and typically yields mean values between 2–4%.     

Desiccation resistance and water balance in southern African keratin beetles (Coleoptera, Trogidae): the influence of body size and habitat

Desiccation resistance and water balance were examined in the adults of seven trogid species, which differed both in body size and in the habitats from which they were collected. Body water contents (51–58% fresh mass) and desiccation rates at 27 °C (0.00026–0.00093 g h⁻¹) in these species were very similar to those of unrelated, similar-sized beetles from arid habitats. The keratin beetles differed markedly from many other adult Coleoptera by virtue of their very high haemolymph osmolality and inability to regulate haemolymph osmolality, and to catabolise lipids for water production, during desiccation. Like most other insects, the xeric trogid species had lower rates of water loss and longer survival times than trogids from mesic areas. This was due both to lower rates of water loss and to the larger body size of species from the more arid areas. Because absolute body water content was higher in large beetles than in small ones, larger body size conferred higher desiccation resistance on the very large Kalahari desert species. This suggests that there may be strong selection for large body size in such insects from arid areas. Most ecological and ecophysiological investigations of geographical variation in body size, and the species-body size distribution, have focused on temperature and metabolic rate as explanatory variables. This study suggests that attention should also be given to desiccation resistance. Accepted: 29 September 1997     

Macroecology of local insect communities

The inter-relationships between animal body weight, range size, species richness and abundance are currently the basis of macroecology. Using 41 099 insects sampled from 31 Acacia tree canopies in north-east Tanzania, we first documented the basic macroecological patterns. The relationship between body weight and both species richness and abundance was polygonal with the highest insect species richness and abundance occurring at intermediate body weights. Across individual tree communities, the most statistically robust relationships were found between range size, abundance and species richness and they were all linear. In a second part, we focused on the positive abundance-range size relationship and we could test predictions of six of the eight proposed hypotheses to explain this widely documented pattern of community structure. The relationship is most likely explained by the metapopulation hypothesis stating that with more patches being occupied, local abundance in a given patch increases due to a higher rate of immigration from nearby patches. In addition, we found high slopes for the species-area relationship, typical of island systems and thus it seems reasonable to characterise Acacia trees in the savannah as habitat islands for insects.     

Allometry of post-flight cooling rates in moths: a comparison with vertebrate homeotherms.

1. The rates of post-flight cooling in 25 saturniid moths of 8 genera ranging in weight from 81 to 2650 mg were measured and compared with cooling rates in sphingids, birds and mammals. 2. The initial and terminal cooling rates of the saturniids did not differ significantly. 3. Large saturniids have relatively smaller thoraxes than small ones. 4. In saturniids the rate of post-flight cooling is inversely related both to thoracic volume and total weight. 5. Cooling rate is less dependent on thoracic volume in saturniids than in sphingids. 6. Weight-specific conductance calculated on the basis of total weight, shows that moths are not as well insulated as birds or mammals. However, when considered on the basis of thoracic weight, the weight-specific conductance of saturniids and sphingids closely approximates that predicted by the regression of weight-specific conductance on total body weight in birds and mammals. 7. Since the insulation of saturniids and sphingids is no more effective for animals of their size than is that of birds and mammals, their high body temperatures during activity appear to depend primarily on high levels of heat production.     

Responses to desiccation in four Coleopterans from sub-Antarctic South Georgia

RATES OF WATER LOSS WERE DETERMINED FOR FOUR COLEOPTERA SPECIES: the herbivores Hydromedion sparsutum, Perimylops antarcticus (Family Perimylopidae) and the carnivores Trechisibus antarcticus, Oopterus soledadinus (Family Carabidae) collected during summer from a range of terrestrial habitats at South Georgia. A recording microbalance enabled measurement of individual weight loss with time in <5% r.h. at 10, 20, 30 and 35 degrees C. Adults of T. antarcticus had significantly higher rates of water loss than any other species over all temperatures. Individuals of both herbivores exhibited the slowest water loss rates under the experimental conditions. Within species, rates at 10 or 20 degrees C were slower than at the higher temperatures. Adult P. antarcticus had significantly greater amounts of body water than adult H. sparsutum for each of the four temperatures. Within species and life-stages of both herbivores, body water contents after drying at 10 degrees C were significantly lower than individuals dried at 30-35 degrees C, but no such differences were observed for the carnivores. At each temperature, rates of water loss were negatively correlated with initial live weight in all four species, but this was not the case within species or between adults and larvae. Maximum survival times during desiccation declined as temperature increased, but did not differ between species at 10 degrees C. Over 30-35 degrees C, survival times of both herbivores were significantly longer than either of the carnivores. Smaller insects (e.g. the carabids) had faster rates of water loss than the larger perimylopids under the same environmental conditions. The latter had greater resistance to desiccation than the former. It is suggested that the larger body water content of P. antarcticus enables it to resist desiccation more than the other three species, which correlates with its ecological distribution. Differences in water contents after drying individuals at low and high temperatures may be caused either by the water binding properties of cells and tissues or by reduction in energy stores in order to maintain metabolism at lower environmental temperatures causing a body weight loss. Whilst both herbivores show some physiological adaptations to drying conditions, it is suggested that the two carnivorous beetles may have adapted behaviourally to the South Georgia environment.     

Effect of Intermittent Cold Exposure on Brown Fat Activation,Obesity, and Energy Homeostasis in Mice

Homeotherms have specific mechanisms to maintain a constant core body temperature despite changes in thermal environment, food supply, and metabolic demand. Brown adipose tissue, the principal thermogenic organ, quickly and efficiently increases heat production by dissipating the mitochondrial proton motive force. It has been suggested that activation of brown fat, via either environmental (i.e. cold exposure) or pharmacologic means, could be used to increase metabolic rate and thus reduce body weight. Here we assess the effects of intermittent cold exposure (4°C for one to eight hours three times a week) on C57BL/6J mice fed a high fat diet. Cold exposure increased metabolic rate approximately two-fold during the challenge and activated brown fat. In response, food intake increased to compensate fully for the increased energy expenditure; thus, the mice showed no reduction in body weight or adiposity. Despite the unchanged adiposity, the cold-treated mice showed transient improvements in glucose homeostasis. Administration of the cannabinoid receptor-1 inverse agonist AM251 caused weight loss and improvements in glucose homeostasis, but showed no further improvements when combined with cold exposure. These data suggest that intermittent cold exposure causes transient, meaningful improvements in glucose homeostasis, but without synergy when combined with AM251. Since energy expenditure is significantly increased during cold exposure, a drug that dissociates food intake from metabolic demand during cold exposure may achieve weight loss and further metabolic improvements.