Life in the slow lane: molecular mechanisms of metabolic rate depression.

Kenneth B. Storey

Institute of Biochemistry, Carleton University, Ottawa, Canada K1S 5B6
kenneth_storey@carleton.ca

Estivation is a state of aerobic hypometabolism typically used by organisms to endure seasonally arid conditions, often associated with desert environments. Frequently, estivating species are active only a few weeks of the year when conditions are right for high-intensity feeding and breeding and then they retreat to estivate in sheltered sites, often underground. In general, estivation includes a strong reduction in metabolic rate, a primary reliance on lipids to fuel metabolism, and methods of water retention, either physical (e.g. cocoons) or metabolic (e.g. urea accumulation). Two aspects of metabolic regulation during estivation are the focus of recent studies in my lab: (1) signal transduction mechanisms that mediate transitions to and from the hypometabolic state, and (2) the role of gene expression in supporting hypometabolism. Our model animals are the spadefoot toad, Scaphiopus couchii, from the Arizona desert and the land snail, Otala lactea, a native of the Mediterranean region. Recent studies indicate prominent roles of protein kinases A and C, tyrosine kinases and protein phosphatases 1 and 2A, revealing a general suppression of signal transducing systems in organs that appears to support the hypometabolic state. Changes in the maximal activities of selected enzymes of intermediary metabolism and up-regulation of specific genes (e.g. riboflavin binding protein in toad liver) also contribute to metabolic reorganization in estivation The mechanisms of metabolic depression in estivators are similar to those seen in hibernation and anaerobiosis and allow us to propose a unified set of biochemical principles for the control of metabolic arrest in nature.

Metabolic rate depression in xeric insects: a beautiful fact ruined by several nasty little theories?

S.L. Chown

Department of Zoology & Entomology, University of Pretoria, Pretoria 0002, South Africa

Metabolic rate depression (here equivalent to reduced whole organism oxygen uptake rates) is commonly held to be an organismal response to arid environments. This is reputedly true also of insects. More recently, laboratory selection experiments have suggested that metabolic rate depression might not always be a response to desiccating conditions. Likewise, flow-through gas analysis techniques have raised the argument that respiratory transpiration constitutes such a small proportion of total water loss in both mesic and xeric species that modification of this loss by alterations to metabolic rate is unlikely to represent any significant advantage to species from arid environments. Moreover, it has also been suggested that species from cool areas should have elevated metabolic rates compared to those from more tropical regions (metabolic cold adaptation), and that flightless species should have reduced metabolic rates compared to those with wings. Together with environmen! tal covariation of temperature and water availability, these ideas suggest that the metabolic rate depression hypothesis requires more careful scrutiny. There are several ways in which this might be done, with laboratory selection appearing to be most appealing. However, this approach might not always provide insight into the changes that species undergo in the field. Large-scale comparisons of the interspecific relationship between water loss and metabolic rate in xeric and mesic species provide another approach. They suggest that metabolic rate depression is a plausible means to reduce water loss, but do little to address the confounding issues raised by smaller-scale, experimental work.

Key factors for survival of the alder leaf beetle, Agelastica alni (Coleoptera, Chrysomelidae), during anoxia induced by submergence

Gregor Kölsch

Zoological Institute, University of Kiel, Olshausenstr. 40, 24098 Kiel, Germany; gkoelsch@zoologie.uni-kiel.de

Agelastica alni is a univoltine species feeding on trees of the genus Alnus which typically grow in wet or humid places. As the beetles overwinter close to the host trees in the upper layers of the soil, they are likely to be submerged after heavy rainfall.
The resistance to submergence was determined on the basis of the survival rate and the time required for recovery after submergence. During diapause, the beetles survive submergence in water lasting several days, although they cannot use the oxygen dissolved in the water by plastron respiration (anoxia). In autumn and spring, the resistance to submergence is less pronounced. The beetles are able to reduce their metabolic rate (heat flow rate in microcalorimetry) by almost 95% under anoxia (N2 atmosphere). Selected biochemical parameters were measured in beetles that had been deep frozen after submergence: contents of glucose, glycogen, lactate, AMP, ADP, ATP, inorganic phosphate and adenylate energy charge (AEC). The different experimental groups of beetles (characterized by season, temperature, and duration of the experiment) were clustered together on the basis of similar duration of the recovery period. The resulting clusters were then submitted to a discriminant analysis using the biochemical parameters to reveal the factors leading to long or short periods of recovery, respectively: High glycogen content rendered possible long submergence, and a relatively high AMP-content and AEC-value after submergence facilitated recovery. Submergence critical for survival was correlated with low AMP, glucose and glycogen contents. Apart from these proximate factors, a potential role of oxidative stress during recovery is discussed.

Water balance in desert insects: lessons from non-charismatic microfauna

Allen G. Gibbs

Center for Insect Science, University of Arizona

Water stress is a particularly important problem for insects and other small organisms in arid environments. Cactophilic fruitflies in the genus Drosophila have invaded deserts on numerous occasions, including multiple independent invasions of the Sonoran Desert in North America. Because the evolutionary history of this genus is so well studied, we can investigate the mechanisms of adaptation in a rigorous phylogenetic context. As expected, desert fruitflies lose water less rapidly than their mesic congeners. They are also able to tolerate the loss of a greater percentage of body water, but this difference is due mainly to phylogenetic history, and does not represent an adaptation specifically to desert habitats.
A laboratory analog of desert Drosophila is provided by populations of D. melanogaster that have been subjected to selection for desiccation resistance. Selected populations resemble desert species in that they lose water slowly, relative to control populations, and are not more tolerant of dehydration stress. They differ, however, in having much higher water contents and different behavioral responses to desiccating conditions. Our comparisons of laboratory and natural populations reveal that not all possible adaptive mechanisms evolve in stressful environments. Different physiological and behavioral strategies may evolve depending upon the particular options available in the environment.

Carbohydrate sparing mechanisms during recovery from exercise in animals adapted to arid environments

Paul A. Fournier

Animal Locomotion Laboratory, Department of Human Movement and Exercise Science, The University of Western Australia, Perth, Western Australia, Australia, 6907
(email: fournier@cyllene.uwa.edu.au)

It is often overlooked that there are over 50 species of native rodents in Australia, many of which are well adapted to the arid and semi-arid environments typical of more than two thirds of the Australian land mass. Since food is not always available in these environments, this poses the problem of whether in the absence of food intake these animals can replenish their stores of muscle glycogen when recovering from high intensity physical activity, an important question given the importance of glycogen in 'flight or fight' responses. Using the Western chestnut mouse (Pseudomys nanus ferculinus) to answer this question, we have shown that following high intensity exercise these animals have the impressive capacity to replenish rapidly and completely their stores of muscle glycogen, even in the absence of food intake. The most likely carbon source for glycogen resynthesis is the lactate produced during exercise, and our results obtained both in vivo and in vitro suggest that the intramuscular pathway of lactate glyconeogenesis participates in this process. Finally, we have provided evidence that the high rates of glycogen synthesis involve (1) dephosphorylation-mediated activation of glycogen synthase, (2) inhibition of glycogen phosphorylase, and (3) stimulation of glucose transport via recruitment of the glucose transporter GLUT 4 to the plasma membrane. How specific are these mechanisms to fasting in semi-arid/arid environments is a question yet to be answered.

A slow-fast metabolic continuum in mammals

Barry G. Lovegrove

School of Botany and Zoology, University of Natal, P/Bag X01 Scottsville, South Africa
Tel: 27-33-26-5113, Fax: 27-33-260515, email: lovegrove@nu.ac.za

The basal metabolic rate (BMR) of mammals is influenced by zoogeography; Holarctic species have higher BMRs than Afrotropical, Australasian and Indomalayan species. Although it has been suggested that rainfall variability may generate these broad-scale geographical gradients (Lovegrove 2000), supportive empirical analyses of global climate variables are lacking. Using conventional analyses that ignore the influence of inherited traits, this study significantly correlated the residual BMR of more than 200 small mammals (< 1kg) from six zoogeographical zones with ambient temperature and rainfall variability after removing body size effects. Normothermic body temperatures ranging from 31 - 39°C were also positively correlated with residual BMR. These data identify a metabolic continuum in small mammals in which species in hot and/or unpredictable environments have the lowest BMRs whereas those in cold and/or predictable environments have the highest basal rates. Maintenance metabolism thus evolves in response to climate and climate variability refuting the early hypotheses of Scholander et al. (1950) that argued that mammalian BMR and body temperature are not determined by climate.

References
Lovegrove, B. G. 2000. The zoogeography of mammalian basal metabolic rate. The American Naturalist 156:201-219.
Scholander, P. F., R. Hock, V. Walters, and L. Irving 1950. Adaptation to cold in arctic and tropical mammals and birds in relation to body temperature, insulation, and basal metabolic rate. Biological Bulletin 99:259-271.

The effect of temperature on alveolar type II cell adrenergic receptors in the fat-tailed dunnart, Sminthopsis crassicaudata and the bearded dragon, Pogona vitticeps.

Carol Ormond, Sandra Orgeig and Christopher B. Daniels

Department of Environmental Biology, University of Adelaide, Australia

Pulmonary surfactant is crucial for maintaining lung function. Pulmonary surfactant is synthesised in alveolar type II cells and secreted into the lining of the lung in response to ventilation, temperature changes, autonomic neurotransmitters and other biochemical factors. Despite the reduction in cellular metabolic rate, the secretory response of type II cells to neurotransmitters appears to be maintained at both warm (37°C) and cold (18°C) incubation temperatures in both dunnarts and bearded dragons. Type II cells were isolated from warm (Tb=33.6 °C + 0.34) and cold (Tb=13.17 °C + 0.21) fat-tailed dunnarts (Sminthopsis crassicaudata) and 35°C- and 15°C-acclimated bearded dragons (Pogona vitticeps). Receptor number and binding affinity (K_d) were measured using a radioreceptor binding assay at both 15 and 35°C. In the dunnart, neither Tb, nor assay temperature affected binding affinity (Torpid; 15°C: Kd = 0.29 + 0.03 nmol l^-1; 35°C: Kd = 0.22 + 0.09; Active; 15°C: Kd = 0.22 + 0.045; 35°C: Kd = 0.27 + 0.056; p > 0.05). However, significantly higher receptor numbers were observed in cells isolated from cold dunnarts measured at 15°C (42237 + 10190 receptors/cell) c.f. cells isolated from warm dunnarts measured at 15°C (30172 + 4080 receptors/cell, p = 0.04). Similarly, cells isolated from warm animals measured at 35°C had a greater number of receptors (69310 + 13160 receptors/cell) than cells isolated from cold dunnarts measured at 35°C (38681 + 4356.9 receptors/cell, p = 0.04). Therefore, receptors from warm and cold animals appear to be higher in number when measured at 35°C and 15°C, respectively. We suggest that the observed changes in receptor number are due to changes in fluidity of the plasma membranes at different assay temperatures. Fluidity changes may lead to the masking of receptor binding sites on the plasma membranes when temperature changes during the assay period. Thermal compensation of the plasma membranes in cold animals, allows changes in the lipid composition of membranes, that enable the receptor sites to remain open, ready for adrenergic stimulation.

Low metabolic rate in scorpions: Implications for high biomass, cannibalism, and future research

John Lighton

University of Nevada, Las Vegas, Department of Biological Sciences, NV, 89154, USA

Scorpions are abundant in arid areas, where their population biomass may exceed that of vertebrates. Since scorpions are predators of small arthropods and feed infrequently across multi-year lifespans, a parsimonious explanation for theor observed, anomalously high biomass may be a depressed metabolic rate (MR). We tested the hypothesis that scorpion MR is significantly depressed compared to other arthropods, and also measured the temperature dependence of scorpion MR to quantify the interaction of large seasonal variations of desert temperatures with MR and thus with long term metabolic expenditure. Scorpion MR increased markedly with temperature (mean Q10= 2.97) with considerable inter-individual variation. The MR's at 25 °C of scorpions from two New World genera were less than 24% of typical terrestrial arthropods (spiders, mites, solphugids, insects) of the same mass. Literature measurements of four Old World scorpion genera from hygri! c to xeric environments support this finding. It is thus likely that low scorpion MR contributes to high scorpion biomass. In arid (resource limited) areas, the combination of high biomass and high production efficiency associated with low MR may also favor a "transgenerational energy storage" strategy, whereby juveniles are harvested by cannibalistic adults which may be closely related to their juvenile prey. Prospects for continuing research to test this hypothesis will be considered.