Energy budget during lactation in striped hamsters at different ambient temperatures

Abstract

The maximal rates of energy intake and expenditure that animals can sustain for protracted periods of days and weeks [sustained energy intake (SusEI) or sustained metabolic rate] are very important because they define upper energetic limits to the ability of animals to distribute, survive and reproduce (Karasov, 1986;Root, 1988;Bozinovic and Rosenmann, 1989;Peterson et al., 1990;Thompson, 1992;Hammond and Diamond, 1997;Bryan and Bryant, 1999;Speakman, 2000;Johnson and Speakman, 2001;Johnson et al., 2001a;Johnson et al., 2001b;Johnson et al., 2001c;Speakman and Król, 2005;Zhao and Cao, 2009a). It is widely believed that SusEI is constrained intrinsically by some aspects of physiology (Daan et al., 1990;Peterson et al., 1990;Weiner, 1992;Hammond and Diamond, 1997;Speakman, 2000;Speakman and Król, 2005;Speakman and Król, 2010). For example, SusEI limitation is suggested to be set by the expenditure capacities of the energyconsuming organs, such as skeletal muscle during physical exercise, brown adipose tissue and muscles during cold exposure, and the mammary glands during lactation, i.e. the peripheral limitation hypothesis (Hammond and Diamond, 1997;Speakman and Król, 2005;Speakman, 2007;Speakman, 2008;Zhao and Cao, 2009a;Zhao et al., 2010a;Zhao, 2010). Alternatively, SusEI limitation may be driven by the capacity of animals to dissipate heat, i.e. the heat dissipation limits hypothesis (Król and Speakman, 2003a;Król and Speakman, 2003b;Speakman and Król, 2005;Król et al., 2007).Lactation is the most energetically demanding period encountered by small mammals (Thompson and Nicol, 1986; Hammond and Diamond, 1997;Johnson et al., 2001a;Johnson et al., 2001b;Speakman and Król, 2005;Speakman, 2007). In general, mammals exposed to cold have to increase their energy demands for additional thermogenesis to maintain constant thermoregulation (Heldmaier et al., 1982;Wang and Wang, 1989;Wang and Wang, 1990;Bozinovic et al., 2004;Li and Wang, 2005;Wang et al., 2006;Zhang and Wang, 2007). Wild animals may experience lactation at cold temperature; thus, the combination of the two stressors is an excellent model with which to study factors limiting SusEI (Hammond and Diamond, 1997;Johnson and Speakman, 2001;Speakman and Król, 2005;Zhang and Wang, 2007). A previous study showed that Swiss mice lactating at cold increased their food intake and did not raise heavier litters compared with mice lactating at normal temperatures, suggesting that limits on SusEI were not driven by the capacity of the gut, but were likely imposed by the capacity of mammary tissue to produce milk (Hammond et al., 1994). Additionally, during lactation, cotton rats (Sigmodon hispidus) did not increase milk energy output compared with controls lactating in warm conditions (Rogowitz, 1998). Zhang and Wang also reported similar results in cold-exposed lactating Brandt's vole (Lasiopodomys brandtii) (Zhang and Wang, 2007). These studies provide support for the peripheral limitation hypothesis (Zhang and Wang, 2007).However, MF1 mice (Mus musculus) lactating at ...

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). Such manipulations of ambient temperature affect not only the mother but also the offspring and their growth, which makes the results of such experiments difficult to interpret.…”

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

“…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).…”

“…Food intake was calculated as the mass of food missing from the hopper every day, subtracting orts mixed in the bedding (Zhao, 2011). FI GE (kJday ).…”

Heat dissipation does not suppress an immune response in laboratory mice divergently selected for basal metabolic rate (BMR)

“…We therefore used T b measurement as a reliable and direct proxy of metabolic costs incurred by an immune challenge in favour of food intake, which typically decreases in warm-exposed mice (e.g. Król et al, 2003;Wu et al, 2009;Zhao, 2011). A reduction of food intake is difficult to interpret, as it may induce the re-allocation of resources between the reduced costs of maintenance of digestive organs and the increased need for an immune response (Ksiazėk et al, 2003).…”

“…To date, the limiting effect of heat dissipation (HD) has been exclusively tested under peak metabolic demands, mostly in lactating rodents and lagomorphs (Król et al, 2007;Wu et al, 2009;Zhao and Cao, 2009;Valencak et al, 2010;Simons et al, 2011;Gamo et al, 2013a;Valencak et al, 2013;Yang et al, 2013;Zhao, 2011;Zhao et al, 2013a,b). It remains to be seen, however, whether the effect of HD also holds for energy expenditures incurred by physiological processes other than peak metabolic demands induced by reproduction.…”