Limits to sustained energy intake XXIX: the case of the golden hamster (Mesocricetus auratus)

Abstract

Golden hamster females have the shortest known gestation period among placental mammals, and at the same time raise very large litters of up to 16 offspring, which are born in a naked and blind state and are only able to pick up food from days 12 to 14 onwards. We quantified energy metabolism and milk production in female golden hamsters raising offspring under cold (8°C), normal (22°C) and hot (30°C) ambient temperature conditions. We monitored energy intake, subcutaneous body temperature, daily energy expenditure, litter size and pup masses over the course of lactation. Our results show that, in line with the concept of heat dissipation limitation, female golden hamsters had the largest energy intake under the coldest conditions and a significantly lower intake at 30°C (partial for influence of ambient temperature: =5.6;=0.004). Metabolisable energy intake as well as milk energy output showed the same pattern and were significantly different between the temperatures (partial for milk energy production: =86.4;<0.0001), with consistently higher subcutaneous temperatures in the reproductive females ( =36.77;<0.0001) compared with baseline females. These data suggest that raising offspring in golden hamsters comes at the cost of producing large amounts of body heat up to a level constraining energy intake, similar to that observed in some laboratory mice. Notably, we observed that females seemed to adjust litter size according to their milk production, with the smallest litters (3.4±0.7 pups) being raised by hot-exposed mothers. Future research is needed to unravel the mechanism by which females assess their own milk production capabilities and how this may be linked to litter size at different ambient temperatures. Golden hamsters reach 8-10 times resting metabolic rate when raising offspring under cold conditions, which is compatible with the findings from laboratory mice and other rodents.

Exposure to hot temperatures during lactation stunted offspring growth and decreased the future reproductive performance of female offspring

“…Reproduction is the period of highest energy demand for small mammals, during which females must increase food intake considerably to meet the energy requirements of raising their offspring (Kenagy et al, 1989(Kenagy et al, , 1990Hammond and Diamond, 1994;Koteja, 1996a,b;Hammond and Diamond, 1997;Rogowitz, 1998;Johnson et al, 2001;Valencak et al, 2010Valencak et al, , 2013Sadowska et al, 2016;Kagya-Agyemang et al, 2018;Ohrnberger et al, 2018).…”

Late lactation in small mammals is a critically sensitive window of vulnerability to elevated ambient temperature

“…This issue is in theory more significant during periods of high energy requirements (22,23). Lactation is the most energy-demanding period for female mammals, during which both food intake and energy expenditure are maximized to meet the energy requirements of their offspring (22)(23)(24)(25). For example, the energy expenditure components including resting metabolic rate (RMR), daily energy expenditure (DEE), and milk energy output (MEO) are considerably increased during lactation, and accordingly energy intake is also increased to offset the energy expended (26)(27)(28)(29)(30)(31)(32).…”

Exposure to artificial wind increases energy intake and reproductive performance of female Swiss mice (Mus musculus) under hot temperature

“…The reduced milk production of females at 32.5°C resulted in these females having significantly lighter litters than females kept at 21°C. Reduced milk production has been also observed in many other mammals lactating under warm or hot ambient temperatures, including laboratory mice (Mus musculus; Król and Speakman, 2003a,b), rats (Rattus norvegicus; Morag et al, 1969;Leon and Woodside, 1983;Jansen and Binard, 1991) Ohrnberger et al, 2018), dairy cattle (Bos taurus; Cobble and Herman, 1951;Brody et al, 1958), sheep (Ovis aries; Abdalla et al, 1993) and pigs (Sus scrofa; Black et al, 1993;Quiniou and Noblet, 1999;Renaudeau and Noblet, 2001;Renaudeau et al, 2003). This suggests that the capacity to dissipate body heat is significantly reduced by higher ambient temperatures resulting in considerable reductions of both energy intake and milk output.…”

“…For example, lactating laboratory MF1 mice kept under hot temperature conditions produced less milk and had slower-growing pups (Król and Speakman, 2003a) than those kept at cooler temperatures (Król and Speakman, 2003b). Exposure to high ambient temperatures has consistently been found to decrease food intake and milk output during lactation, in small mammals and medium and large domestic animals (Cobble and Herman, 1951;Brody et al, 1958;Morag et al, 1969;Leon and Woodside, 1983;Jansen and Binard, 1991;Abdalla et al, 1993;Renaudeau and Noblet, 2001;Król and Speakman, 2003a,b;Renaudeau et al, 2003;Wu et al, 2009;Valencak et al, 2010Valencak et al, , 2013Simons et al, 2011;Zhao, 2011;Zhao et al, 2013;Yang et al, 2013;Wen et al, 2017;Ohrnberger et al, 2018;Bao et al, 2020).…”