Kimberly A. Hammond

An Experimental Test for a Ceiling on Sustained Metabolic Rate in Lactating Mice

Time-averaged sustained metabolic rates (SusMRs) of humans and wild animals have been observed not to exceed about seven times basal metabolic rate (BMR), which suggests a possible ceiling on sustained metabolic scope. We tested experimentally for such a ceiling by subtracting or adding pups to vary the litter size of lactating mother mice between five and 26 pups. Mothers could regularly wean 14pups but not more (natural litter size is 8-10). Although food intake at peak lactation increased to as much as 3.4 times virgin values and increased with litter size, digestive efficiency remained constant The mass of the small intestine and of other gut compartments increased up to severalfold at peak lactation, and as a consequence so did the intestines brush-border uptake capacities for glucose and for proline. Time-averaged sustained metabolic rate at peak lactation reached 7.2 times BMR; this ratio is evidently close to a ceiling on sustained metabolic scope. Estimates of intestinal nutrient uptake capacities exceeded nutrient intakes by only a modest safety margin of reserve capacity. Intestinal hypertrophy during lactation tended to preserve those safety margins and thus to maintain digestive effciency. Conversely, postlactational intestinal atrophy and the modest size of the safety margins tended to avoid waste of biosynthetic energy.

Metabolic Ceilings under a Combination of Peak Energy Demands

Is energy expenditure limited by shared metabolic machinery for energy assimilation or by bottlenecks specific to each mode of energy expenditure? We tested this question in mice by imposing peak energy burdens of lactation and of cold stress simultaneously. We measured food intake, body and organ masses, and small intestinal brush-border hydrolase and transporter capacities in virgin female mice and in mothers nursing approximately 5, 8, or 14 pups, at either 5° C or 23° C We had already observed that mothers of 14 pups are at a limit of lactational performance at 23° C, while virgin mice at 5° C are near their limit of food intake in response to cold stress. Nevertheless, the increments in food intake due to these two energy stresses applied simultaneously proved to be additive: food intake in lactating mice at 5° C was even higher than the peak intake in lactating mice at 23° C or in virgins at 5° C. Thus, neither during peak lactation nor during peak cold stress alone was energy expenditure limited by shared machinery for energy assimilation; assimilation could be pushed even higher by adding another energy stress. Masses of the small intestine, liver, and kidney increased with food intake even more than expected from increases in body mass. These increased organ masses are adaptive and permit energy-stressed mice to process ingested nutrients at rates exceeding the capacities of unstressed mice. Safety factors (load/capacity ratios) of three intestinal brush-border hydrolases and transporters for nutrients declined toward 1 with increasing food intake. The capacity of the brush-border enzyme sucrase to produce glucose remained matched to the capacity of the brush-border glucose transporter to absorb the resulting glucose, as both varied with food intake.

The Role of Diet Quality and Energy Need in the Nutritional Ecology of a Small Herbivore, Microtus ochrogaster

The objective of this study was to determine the effect of low-quality diets and increased energy needs on nutritional aspects of the prairie vole (Microtus ochrogaster). In the laboratory, high-fiber diets were correlated with higher rates of food intake and larger hindguts, as well as a lower digestibility of dry matter, cell solubles, energy, and nitrogen, but higher fiber digestibilities than low-fiber diets. Acclimation to cold temperatures resulted in higher rates of food intake than acclimation to warm temperatures. In addition, the size of the small intestine and cecum increased in response to cold acclimation. Although increases in intake, resulting from acclimation to cold temperatures, did not result in changes in the digestibility of the diet or dietary components, they did result in decreases in the dietary turnover time. Thus, increases in transit rate through the gut do not necessarily result in declines in the amount of energy extracted per gram of food ingested. More energy per unit time, however, can be extracted from the diet, perhaps because of increases in the size of the gut allowing maintenance of digestibilities and energy need in the face of higher transit times.

Responses to lactation and cold exposure by deer mice (Peromyscus maniculatus).

Recently, much interest has been expressed in understanding how animals use phenotypic plasticity of tissue size and function to meet increased metabolic demands. We set out to learn (i) whether female deer mice (Peromyscus maniculatus) given lactation (two to seven pups per litter), cold (5°C), or cold plus lactation as energy demands display phenotypic plasticity in organ size and function; (ii) whether that plasticity is similar to laboratory mice given the same demands; and (iii) whether lactational performance in deer mice is derived from limits on central or peripheral organs. We found that deer mice responded to lactation by increasing digestible food intake and increasing the masses of the stomach, small intestine, cecum and liver, and the length of the small intestine. Heart mass was lower in lactating than in nonlactating mice. Cold exposure also caused increases in digestible food intake and increases in the masses of the small intestine, kidney, and heart. We conclude that deer mice display organ tissue plasticity in response to both lactation and cold exposure in a similar manner to laboratory mice. We also conclude that deer mice are not limited by central processing organs because they are able to increase digestive organ size continuously with increased energetic demands.

The heat increment of feeding in house wren chicks: magnitude, duration, and substitution for thermostatic costs

The heat increment of feeding (HIF), a transient postprandial increase in metabolic rate, is the energy cost of processing a meal. We measured HIF in house wren chicks (Troglodytes aedon) ranging in mass from 1.6 to 10.3 g. This mass range (age 2–10 days) spanned a transition from blind, naked, ectothermic chicks through alert, endothermic birds with nearly complete feathering. We fed chicks crickets (2.7–10% of chick body mass) and determined HIF from continuous measurements of oxygen consumption rate (O2) before and after meals. At warm ambient temperatures (Ta) of 33–36 °C, the magnitude of HIF (in ml O2 or joules) was linearly related to meal mass and was not affected by chick mass. HIF accounted for 6.3% of ingested energy, which is within the range of results for other carnivorous vertebrates. The duration of HIF was inversely related to chick mass; 10-g chicks processed a standard meal approximately twice as fast as 2-g chicks. HIF duration increased with increasing meal mass. The peak O2 during HIF, expressed as the factorial increase above resting metabolism, was independent of body mass and meal mass. In large, endothermic chicks ( > 8 g), HIF substituted for thermoregulatory heat production at low Ta.

Adaptation of the maternal intestine during lactation.

One of the most dramatic adaptations to lactation is a large increase in the size and complexity of maternal intestine. Although there are few data on changes in intestinal size, intestinal enlargement has been observed in many taxonomic groups. In this review I describe the morphological and physiological changes in the intestinal mass of lactating animals and discuss their functional significance. The observed increases maintain the digestive efficiency of the food, as well as insure adequate absorption of nutrients in the face of the increased energy demand that accompanies lactation. The extent of the increase in size is proportional to the increase in energy demand. It is clear that if the intestine did not accommodate during lactation mothers would not have the capacity to absorb the nutrients need to maintain their energy demand.

Morphological and Physiological Responses to Altitude in Deer Mice Peromyscus maniculatus

Individuals within a species, living across a wide range of habitats, often display a great deal of phenotypic plasticity for organ mass and function. We investigated the extent to which changes in organ mass are variable, corresponding to environmental demand, across an altitudinal gradient. Are there changes in the mass of oxygen delivery organs (heart and lungs) and other central processing organs (gut, liver, kidney) associated with an increased sustainable metabolic rate that results from decreased ambient temperatures and decreased oxygen availability along an altitudinal gradient? We measured food intake, resting metabolic rate (RMR), and organ mass in captive deer mice (Peromyscus maniculatus bairdii) at three sites from 1,200 to 3,800 m above sea level to determine whether energy demand was correlated with organ mass. We found that food intake, gut mass, and cardiopulmonary organ mass increased in mice living at high altitudes. RMR was not correlated with organ mass differences along the altitudinal gradient. While the conditions in this study were by no means extreme, these results show that mice living at high altitudes have higher levels of energy demand and possess larger cardiopulmonary and digestive organs than mice living at lower altitudes.

Age and aerobic performance in deer mice.

SUMMARY Age impacts the phenotype of all multicellular animals, but lifetime changes in physiological traits are poorly understood for all but a few species. Here, we describe a cross-sectional study of age effects on body composition, aerobic performance and ventilation in deer mice Peromyscus maniculatus. This species lives considerably longer in captivity (in excess of 5 years) than most laboratory rodents, and the adaptational biology of its aerobic physiology is well studied. Our deer mice grew throughout life, and, as is typical for mammals, their basal metabolic rate (BMR) and maximal oxygen consumption in exercise (V̇O2max) and thermogenesis (V̇O2sum) increased as power functions of mass. Age did not affect BMR, but we found abrupt decreases in growth rate, V̇O2max and V̇O2sum at approximately 485 days of age, and the mass-adjusted maximal aerobic performance of old mice (5 years of age) was 20% (V̇O2max) to 35% (V̇O2sum) less than that of young animals. Breathing frequency (f) and oxygen extraction (EO2) also declined with age but did not change abruptly. However, there were no consistent age-related changes in tidal volume (VT) or minute volume (V̇min) after accounting for the effects of mass and V̇O2sum. Age influenced several aspects of body composition (lean and fat mass). However, these changes were insufficient to explain the age-related declines in aerobic performance, suggesting that mass-specific oxidative capacity of lean tissue decreased with age. The performance changes we found could engender substantial reductions in the mobility and thermal tolerances of old deer mice. However, very few wild mice are likely to survive to ages where substantial performance decreases occur, so these declines are probably not subjected to strong selection in natural populations.

Development partly determines the aerobic performance of adult deer mice, Peromyscus maniculatus

SUMMARY Previous studies suggest that genetic factors and acclimation can account for differences in aerobic performance (V̇O2max) between high and low altitude populations of small mammals. However, it remains unclear to what extent development at different oxygen partial pressures (PO2) can affect aerobic performance during adulthood. Here we compared the effects of development at contrasting altitudes versus effects of acclimation during adulthood on V̇O2max. Two groups of deer mice were born and raised for 5 weeks at one of two altitudes (340 and 3800 m above sea level). Then, a subset of each group was acclimated to the opposite altitude for 8 weeks. We measured V̇O2max for each individual in hypoxia (PO2=13.5 kPa, 14% O2 at 3800 m) and normoxia (PO2=20.4 kPa, 21% O2 at 340 m) to control for PO2 effects. At 5 weeks of age, high altitude born mice attained significantly higher V̇O2max than low altitude born mice (37.1% higher in hypoxia and 72.1% higher in normoxia). Subsequently, deer mice acclimated for 8 weeks to high altitude had significantly higher V̇O2max regardless of their birth site (21.0% and 72.9% difference in hypoxia and normoxia, respectively). A significant development × acclimation site interaction comparing V̇O2max in hypoxia and normoxia at 13 weeks of age suggests that acclimation effects depend on development altitude. Thus, reversible plasticity during adulthood cannot fully compensate for developmental effects on aerobic performance. We also found that differences in aerobic performance in previous studies may have been underestimated if animals from contrasting altitudes were measured at different PO2.

Contribution of Shivering and Nonshivering Thermogenesis to Thermogenic Capacity for the Deer Mouse (Peromyscus maniculatus)

Small mammals that are active all year must develop ways to survive the cold winters. Endotherms that experience prolonged cold exposure often increase their thermogenic capacity. Thermogenic capacity incorporates basal metabolic rate (BMR), nonshivering thermogenesis (NST), and shivering thermogenesis (ST). Increasing the capacity of any of these components will result in increased thermogenic capacity. It is often thought that NST should be the most plastic component of thermogenic capacity and as such is the most likely to increase with cold acclimation. We used deer mice to test this hypothesis by acclimating 27 animals to one of two temperatures (5° or 22°C) for 8 wk. We then measured and compared values for thermogenic capacity—BMR, ST, and NST—between the two groups. Thermogenic capacity and NST increased by 21% and 42%, respectively, after cold acclimation. Neither BMR nor ST showed any change after acclimation. Therefore, it appears that deer mice raise their thermogenic capacity in response to prolonged cold by altering NST only.