R. M. McDevitt

Central Limits to Sustainable Metabolic Rate Have No Role in Cold Acclimation of the Short-tailed Field Vole (Microtus agrestis)

We investigated the extent to which the changes in basal metabolic rate (BMR), gut morphology, and food intake (FI) that typically occur during cold acclimation in small mammals can be explained by the concept of alimentary-mediated limits to sustainable metabolic energy expenditure. Adult short-tailed field voles (Microtus agrestis) were cold stressed by continuous exposure to 5° C. Exposure for 10, 20, 50, and 100 d (n = 6 in all cases) produced significant changes in oxygen consumption (V̇o2), mass, FI, and the dry weight of a variety of morphological parameters when compared with voles that were not cold exposed (n = 8). At 10°, 20°, and 25° C, V̇o2 (mL · min⁻¹) increased significantly with the duration of cold exposure. After 100 d cold exposure, V̇o2 had increased by more than 50% at each test temperature. Food intake (g · d⁻¹) increased significantly by 106% after 10 d cold exposure but did not increase further with increased exposure time. The ratio of FI (J · h⁻¹) to BMR (J · h⁻¹) was 1.2 in controls and increased to 2.7 after 10 d cold exposure. Thereafter the ratio decreased, and after 100 d cold exposure FI:BMR was not significantly different from control levels. The mass of cold-exposed voles increased significantly with duration of exposure. Masses of the following morphological parameters increased with increasing duration of cold exposure; whole body mass, carcass, skeleton, pelage, subcutaneous fat, liver, kidney, lung, and interscapular brown fat (BAT). There was no significant relationship between duration of cold exposure and the masses of muscle, large intestine, heart, and brain. Using stepwise multiple regression analysis we showed that variation in BMR was linked mostly to changes in skeletal mass. However, when skeletal mass was removed as an independent variable from the analysis, BAT, muscle, and gut mass entered as significant predictors, together explaining 55.5% of the variation in BMR. Although FI increased during cold exposure, the increase (106%) was apparently insufficient to precipitate a hypertrophic response in the gut. Nevertheless BMR did increase as duration of cold exposure increased, probably linked to an increase in BAT mass and thus thermogenic capacity. We cannot support the hypothesis that the changes that typically occur in BMR, food intake, and gut morphology during cold acclimation are a consequence of alimentary-mediated limits to sustainable metabolic rate.

Metabolic and Organ Mass Responses to Selection for High Growth Rates in the Domestic Chicken (Gallus domesticus)

Evolutionary hypotheses suggest that higher rates of postembryonic development in birds should either lower the resting metabolic rate (RMR) in a trade‐off between the costs of growth and maintenance or increase RMR because of a buildup of metabolic machinery. Furthermore, some suggest that higher rates of postembryonic development in birds should reduce peak metabolic rate (PMR) through delayed tissue maturation and/or an increased energy allocation to organ growth. We studied this by comparing metabolic rates and organ sizes of fast‐growing meat‐type chickens (broilers) with those of birds from a laying strain, which grow much slower. During the first week of life, despite growing six times faster, the RMR of the broiler chickens was lower than that of birds of the laying strain. The difference between strains in RMR disappeared thereafter, even though broilers continued to grow twice as fast as layers. The differences between strains in growth rate during the first week after hatching were not reflected in similar differences in the relative masses of the heart, liver, and small intestine. However, broilers had heavier intestines once they reached a body mass of 80 g. In contrast, broilers had relatively smaller brains than did layers. There was a positive correlation, over both strains, between RMR and the masses of leg muscles, intestine, and liver. Furthermore, despite delayed maturation of muscle tissue, broilers exhibited significantly higher PMR. We hypothesize that a balance between the larger relative muscle mass but lower muscle maturation level explains this high PMR. Another correlation, between leg muscle mass and PMR, partly explained the positive correlation between RMR and PMR.

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.

Limits to Sustainable Metabolic Rate during Transient Exposure to Low Temperatures in Short­ tailed Field Voles (Microtus agrestis)

We exposed short-tailed field voles, Microtus agrestis, to transient decreases in ambient temperature to evaluate the limits of their sustainable metabolic rates. We predicted that voles exposed to transient low temperatures would elevate their food intake until they reached some alimentary limit and thereafter they would withdraw reserves. During short-term (24-h) exposure to temperatures below the lower critical temperature (25° C) daily food intake actually decreased significantly to a minimum of 1.51 ± 0.41 g at 10° C but was greater at 5° and -5° C. Weight loss (g) increased significantly with decreasing temperature; however, at 5° C vole mass increased. During more prolonged exposure for 4 d, food intake increased significantly with the duration of cold exposure (5° and 15° C) to a maximum on days 3 and 4. In a separate experiment voles were randomly exposed for 3-d intervals to a range of temperatures from 20° to 5° C and were returned to 25° C for 3 d between exposures. Both food intake and weight loss increased significantly with decreasing temperature; voles gained mass at 20° and 25° C. There was 40% mortality in voles exposed to -5° C for 24 h (n = 10). When voles were exposed to 5° C for 6 d before they were exposed to -5° C, there was zero mortality at -5° C for 12 d (n = 6). The basal metabolism (BMR) of voles before transient cold exposure, 1.71 ± 0.41 mL · min⁻¹, was not significantly different from that of the same voles after transient cold exposure (2.17 ± 0.71 mL min⁻¹). Maximum food intake at 5°C (5.67 ± 1.45 g · d⁻¹) represented 1.7 times BMR, which is considerably lower than the limit on alimentary uptake of seven times BMR previously suggested. Our results suggest that the voles were using a strategy of energy minimization during transient cold exposure that combined increased energy intake with body reserve utilization. However, the duration of cold exposure had a profound effect on this strategy. The mortality data in this species at low temperatures combined with levels of food intake relative to BMR suggest that sustainable metabolic rate is not limited by constraints imposed centrally by the alimentary system but rather by constraints at the sites of energy utilization.

Seasonal variation in the metabolic rate of the Pygmy shrew, Sorex minutus: Can resting metabolic rate be measured in post-absorptive shrews?

Abstract 1. 1. VO 2 (ml min −1 ) in winter-, summer- and spring-acclimatized Pygmy shrews, Sorex minutus , varied significantly with season, gender and ambient temperature. Body mass varied significantly with season and was lightest in winter-acclimatized shrews. 2. 2. Resting metabolic rate (RMR) was lowest in winter shrews (0.619 ± 0.131 ml min −1 ). In spring-acclimatized shrews RMR was significantly higher in females (0.750 ± 0.120 ml min −1 ) compared to the males (0.723 ± 0.09 ml min −1 ). 3. 3. VO 2 in summer shrews decreased at ambient temperatures above the TNZ (22–30°C) by 55% suggesting that some form of reversible metabolic down-regulation at high T a was occurring. 4. 4. There was no significant reduction of VO 2 in post-absorptive shrews compared to fed shrews from any season. We believe that S. minutus responded to food deprivation by increasing activity, presumably foraging activity, with a resultant increase in VO 2 .

Long photophase is not a sufficient stimulus to reduce thermogenic capacity in winter-acclimatized short-tailed field voles (Microtus agrestis) during long-term cold acclimation

The thermogenic capacity of brown adipose tissue in winter- and summer-acclimatized short-tailed field voles (Microtus agrestis) was investigated by examining changes in mass of brown adipose tissue, the ratio of white adipose tissue to brown adipose tissue, the concentration of the uncoupling protein (thermogenin) in whole depots (μg) and in mitochondrial mass (μg·mg-1) and the activity of cytochrome c oxidase in the depots (mmol·min-1). The concentration of thermogenin in winter-acclimatized voles (n=8), per brown adipose tissue depot and per mitochondrial mass, was significantly higher than in summer-acclimatized voles (n=6). There was no significant difference in the level of cytochrome c oxidase activity between these two groups. Four groups of winter-acclimatized voles (n=6 in each group) were exposed to 5°C for 10, 20, 50 and 100 days in a 14L:10D photoperiod. Body mass, brown adipose tissue mass, white adipose tissue mass and basal metabolic rate were significantly positively related to the length of time cold exposed up to 100 days. There was a significant inverse relationship between the ratio of white to brown adipose tissue mass and the duration of cold exposure. There was no significant relationship between thermogenin concentration, either per depot or in mitochondrial mass of brown adipose tissue, with the length of time cold exposed. The level of cytochrome c oxidase activity increased significantly from control levels to a maximum after 10 days in the cold but decreased from 10 days onwards. In winter-acclimatized M. agrestis, a 14L:10D photoperiod is not a sufficient stimulus to reduce thermogenic capacity during cold acclimation. Indeed, some changes in the indirect parameters reflecting thermogenesis, notably the increase in basal metabolic rate and the decrease in the ratio of white to brown adipose tissue mass, indicated that despite the long photophase the thermogenic capacity was slightly further enhanced during the cold acclimation.

Seasonal variation in brown adipose tissue mass and lipid droplet size of Sorex minutus, the pygmy shrew; The relationship between morphology and metabolic rate

Abstract 1. 1. Metabolic rate, brown adipose tissue (BAT) mass and BAT lipid droplet size, were measured in winter-, summer- and spring-acclimatized Pygmy shrews, Sorex minutus . 2. 2. BAT mass changed significantly with season both in relative and absolute terms. Winter-acclimatized shrews had the smallest (135 ± 10 mg) and spring-acclimatized shrews had the heaviest BAT depots (310 ± 28 mg). Relative BAT mass varied between 2–7% depending on season. Median BAT lipid droplet size (μm 2 ) was smallest in winter-acclimatized (106 μm 2 ) and largest in spring-acclimatized shrews (326 μm 2 ). 3. 3. Resting metabolic rate and thermoregulatory thermogenesis were significantly positively related to BAT mass. There was a significant inverse relationship between mass independent metabolic rate and lipid droplet size in all seasonally acclimatized shrews. 4. 4. Winter-acclimatization of BAT in S. minutus is characterised by a decrease in BAT mass signifying a marked utilisation of lipid stores and by a reduction in BAT lipid droplet size, signifying an increase in thermogenic activity.

The importance of nest utilization as a behavioural thermoregulatory strategy in Sorex minutus the pygmy shrew

Abstract 1. 1|We examined the importance of the behavioural thermoregulatory mechanism of nest utilization in one of the smallest temperate endotherms, Sorex minutus , the pygmy shrew and in particular, if there were any seasonal variations in the effect of nest use on metabolic rate. 2. 2|VO 2 was highly significantly related to ambient temperature, nest presence and season in S. minutus (ANOVA). Shrews that had the opportunity to utilize nests showed a reduction in VO 2 of up to 20%, depending on season and ambient temperature. 3. 3|VO 2 in winter acclimatized shrews was significantly reduced when nests were provided at temperatures below thermoneutrality. Nest utilization did not affect VO 2 at any temperature in summer acclimatized shrews. In adult spring shrews of both sexes, VO 2 was only significantly reduced at low temperatures (10°C) when nests were used. 4. 4|Nest utilization is an important behavioural thermoregulatory strategy in S. minutus which should be taken into account in estimations of daily energy expenditure.