Thermogenesis, food intake and serum leptin in cold-exposed lactating Brandt's voles Lasiopodomys brandtii

SUMMARYLimits to sustained energy intake (SusEI) during lactation in Swiss mice have been suggested to reflect the secretory capacity of the mammary glands. However, an alternative explanation is that milk production and food intake are regulated to match the limited growth capacity of the offspring. In the present study, female Swiss mice were experimentally manipulated in two wayslitter sizes were adjusted to be between 1 and 9 pups and mice were exposed to either warm (21°C) or cold (5°C) conditions from day 10 of lactation. Energy intake, number of pups and litter mass, milk energy output (MEO), thermogenesis, mass of the mammary glands and brown adipose tissue cytochrome c oxidase activity of the mothers were measured. At 21 and 5°C, pup mass at weaning was almost independent of litter size. Positive correlations were observed between the number of pups, litter mass, asymptotic food intake and MEO. These data were consistent with the suggestion that in small litters, pup requirements may be the major factor limiting milk production. Pups raised at 5°C had significantly lower body masses than those raised at 21°C. This was despite the fact that milk production and energy intake at the same litter sizes were both substantially higher in females raising pups at 5°C. This suggests that pup growth capacity is lower in the cold, perhaps due to pups allocating ingested energy to fuel thermogenesis. Differences in observed levels of milk production under different conditions may then reflect a complex interplay between factors limiting maternal performance (peripheral limitation and heat dissipation: generally better when it is cooler) and factors influencing maximum pup growth (litter size and temperature: generally better when it is hotter), and may together result in an optimal temperature favouring reproduction.

Section: Discussionsupporting

confidence: 50%

Section: Discussionmentioning

confidence: 99%

Limits to sustained energy intake. XVIII. Energy intake and reproductive output during lactation in Swiss mice raising small litters

Zhao

Song

et al. 2013

“…In mammals, particularly small ones, lactation is the most energetically expensive period (Thompson and Nicoll, 1986;Speakman, 2008). Lactation often results in an increase in caloric intake by more than 100%, increased metabolic rate (Zhang and Wang, 2007) and elevated body temperature (Gamo et al, 2013). Thus, the discussion on limits to sustained metabolic rate (SusMR) has been largely focused on lactating females.…”

Section: Introductionmentioning

confidence: 99%

Limits to sustained energy intake. XXIII. Does heat dissipation capacity limit the energy budget of lactating bank voles?

Sadowska

Król

Chrząścik

et al. 2016

Understanding factors limiting sustained metabolic rate (SusMR) is a central issue in ecological physiology. According to the heat dissipation limit (HDL) theory, the SusMR at peak lactation is constrained by the maternal capacity to dissipate body heat. To test that theory, we shaved lactating bank voles (Myodes glareolus) to experimentally elevate their capacity for heat dissipation. The voles were sampled from lines selected for high aerobic exercise metabolism (A; characterized also by increased basal metabolic rate) and unselected control lines (C). Fur removal significantly increased the peak-lactation food intake (mass-adjusted least square means±s.e.; shaved: 16.3±0.3 g day ; P<0.0001), average daily metabolic rate (shaved: 109± 2 kJ day ; P=0.028). Thus, fur removal increased both the total energy budget and reproductive output at the most demanding period of lactation, which supports the HDL theory. However, digestive efficiency was lower in shaved voles (76.0±0.3%) than in unshaved ones (78.5±0.2%; P<0.0001), which may indicate that a limit imposed by the capacity of the alimentary system was also approached. Shaving similarly affected the metabolic and reproductive traits in voles from the A and C lines. Thus, the experimental evolution model did not reveal a difference in the limiting mechanism between animals with inherently different metabolic rates.

“…During lactation food intake increases enormously (Johnson et al, 2001a) and conspicuously reaches a plateau in late lactation that is resistant to attempts to breach it by imposing additional workloads on the female, for example, by manipulating litter size or pup demands (Hammond and Diamond, 1992;Johnson et al, 2001a;Laurien-Kehnen and Trillmich, 2003;Duah et al, 2013), by making females simultaneously pregnant (Johnson et al, 2001c), or by forcing them to run to obtain their food (Perrigo, 1987;Zhao et al, 2013a). However, when lactating animals are placed in the cold, they are able to eat significantly more than at room temperature Hammond and Kristan, 2000;Johnson and Speakman, 2001;Rogowitz, 1998;Zhang and Wang, 2007), and conversely when kept in hot conditions their maximal intake declines (Król and Speakman, 2003a;Wu et al, 2009;Yang et al, 2013). This effect could be explained either by the HDL theory, the summed peripheral demands idea or temperature-dependent variations in pup energy demands.…”

Section: Introductionmentioning

confidence: 99%

Limits to sustained energy intake. XXII. Reproductive performance of two selected mouse lines with different thermal conductance

Jothery

Król

Hawkins

et al. 2014

Maximal sustained energy intake (SusEI) appears limited, but the factors imposing the limit are disputed. We studied reproductive performance in two lines of mice selected for high and low food intake (MH and ML, respectively), and known to have large differences in thermal conductance (29% higher in the MH line at 21°C). When these mice raised their natural litters, their metabolisable energy intake significantly increased over the first 13 days of lactation and then reached a plateau. At peak lactation, MH mice assimilated on average 45.3% more energy than ML mice (222.9±7.1 and 153.4±12.5 kJ day −1 , N=49 and 24, respectively). Moreover, MH mice exported on average 62.3 kJ day −1 more energy as milk than ML mice (118.9±5.3 and 56.6±5.4 kJ day, N=subset of 32 and 21, respectively). The elevated milk production of MH mice enabled them to wean litters (65.2±2.1 g) that were on average 50.2% heavier than litters produced by ML mothers (43.4±3.0 g), and pups that were on average 27.2% heavier (9.9±0.2 and 7.8±0.2 g, respectively). Lactating mice in both lines had significantly longer and heavier guts compared with non-reproductive mice. However, inconsistent with the 'central limit hypothesis', the ML mice had significantly longer and heavier intestines than MH mice. An experiment where the mice raised litters of the opposing line demonstrated that lactation performance was not limited by the growth capacity of offspring. Our findings are consistent with the idea that the SusEI at peak lactation is constrained by the capacity of the mothers to dissipate body heat.