Limits to sustained energy intake. XI. A test of the heat dissipation limitation hypothesis in lactating Brandt's voles (Lasiopodomys brandtii)

Abstract

SUMMARYThe maximum rate of sustained energy intake (SusEI) may limit reproductive effort, thermoregulatory capability and other aspects of an animal's energy expenditure. Consequently, factors that limit SusEI are of interest. The 'heat dissipation limitation hypothesis' suggests that maximum SusEI during lactation is limited by the capacity to dissipate body heat generated as a byproduct of processing food and producing milk. In the present study, we tested the heat dissipation limitation hypothesis in lactating Brandt's voles (Lasiopodomys brandtii). Female voles were mated and pregnant at 21(±1)°C. A random sample of animals was transferred into a hot room 30(±1)°C on the day of parturition. The energy intake of lactating voles at 30°C was always lower than that at 21°C. At peak lactation food intake was 3.3gday -1 lower at 30°C than at 21°C. There was no significant difference in digestibility. With similar mean litter sizes (7.26±0.46 pups at 21°C and 7.78±0.39 pups at 30°C at the beginning of parturition, 6.83±0.51 pups at 21°C and 7.73±0.50 pups at 30°C at weaning), the milk energy output of mothers, evaluated from the difference between metabolizable energy intake and daily energy expenditure measured by doubly labelled water, at 30°C was 23.3kJday -1 lower than that at 21°C on days 14-16 of lactation. As for reproductive performance, there was a difference in the response to the higher temperature between mothers raising large and those raising small litters. For small litters (<7) there was no significant change in litter mass, but for large litters (≥7) there was a significant decrease at the higher temperature. On average, in larger litters the pups were 15.5g heavier on day 12 of lactation when raised at 21°C. Our data from Brandt's voles support the suggestion that SusEI at peak lactation is limited by heat dissipation capacity, particularly for those voles raising large litters. In smaller litters the peripheral limitation hypothesis may be more relevant. The importance of heat dissipation limits in species raising exclusively small litters needs to be investigated.Key words: Brandt's voles (Lasiopodomys brandtii), lactation, heat dissipation limitation hypothesis, food intake, digestive efficiency, metabolizable energy intake, daily energy expenditure, milk energy output, pup energy content, doubly labelled water.

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

“…Similar effects of decreased or increased temperature on lactation performance were observed in common vole (Microtus arvalis), Mongolian gerbil (Meriones unguiculatus) and Brandt's vole (Lasiopodomys brandtii, only in females with a litter size exceeding seven) (Wu et al, 2009;Simons et al, 2011;Yang et al, 2013). Contrary to the predictions of the HDL theory, however, females of European hares (Lepus europaeus) were able to reach their maximum energy turnover under thermoneutral conditions (Valencak et al, 2010) and lactating striped hamster (Cricetulus barabensis) females increased their food intake in the cold, but were not capable of producing more milk (Zhao, 2011).…”

“…Rogowitz, 1998). Several experiments designed to resolve which of the two mechanisms limits females' energy budgets at peak lactation provided contradictory results (Hammond and Diamond, 1992;Speakman and McQueenie, 1996;Rogowitz, 1998;Hammond and Kristan, 2000;Johnson and Speakman, 2001;Johnson et al, 2001a,b;Wu et al, 2009;Duah et al, 2013).…”

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

“…Consistent with this idea, dorsally shaved MF1 mice had increased thermal conductivity, and were thus able to produce more milk and wean heavier litters (Król et al, 2007). Studies on Brandt's voles (Wu et al, 2009) and Mongolian gerbils (Yang et al, 2013) both revealed that high temperatures (30°C) induced a reduction in milk production. Although these data supported the HDL theory, the effect in voles was greatest in females raising the largest litters, and in small litters there was no significant effect of high temperature (Wu et al, 2009).…”

“…The factors that limit the intake of food at peak lactation, and hence overall reproductive performance, have been the subject of repeated experimentation (Peterson et al, 1990;Hammond and Diamond, 1992;Weiner, 1992;Hammond et al, 1994;Koteja, 1996a;Rogowitz, 1998;Hammond and Kristan, 2000;Johnson et al, 2001a;Bacigalupe and Bozinovic, 2002;Król and Speakman, 2003a;Król and Speakman, 2003b;Zhang and Wang, 2007;Zhang and Wang, 2008;Wu et al, 2009;Zhao and Cao, 2009;Speakman and Król, 2011;Zhao, 2011;Zhao, 2012). Among several others, two factors that have emerged from this work appear to be significant: (i) the capacity of the mammary glands to produce milk and (ii) the capacity of the female to dissipate body heat (Peterson et al, 1990;Hammond and Diamond, 1992;Weiner, 1992;Hammond et al, 1994;Koteja, 1996a;Rogowitz, 1998;Hammond and Kristan, 2000;Johnson et al, 2001a;Bacigalupe and Bozinovic, 2002;Król and Speakman, 2003a;Król and Speakman, 2003b;Speakman and Król, 2005;Speakman and Król, 2011).…”

“…Studies on Brandt's voles (Wu et al, 2009) and Mongolian gerbils (Yang et al, 2013) both revealed that high temperatures (30°C) induced a reduction in milk production. Although these data supported the HDL theory, the effect in voles was greatest in females raising the largest litters, and in small litters there was no significant effect of high temperature (Wu et al, 2009). This could mean that another limit was reached reflecting the capacity of the pups to grow.…”