Peak energy turnover in lactating European hares: the role of fat reserves

Abstract

SUMMARYEuropean hares (Lepus europaeus) in central Europe have high energetic costs of reproduction, mainly due to precocial, rapidly growing young that rely largely on energy-rich milk. Thus, hares in this climate build up large fat stores during winter that are then gradually depleted during the spring-to-autumn breeding season. We hypothesized that the diminishing fat stores of females over the breeding season might affect resource allocation, peak energy assimilation during lactation or the total investment in offspring. Therefore, we measured energy intake, milk quality and milk production throughout lactation in spring, summer and autumn in females raising (size-manipulated) litters with three young each, under a natural photoperiod but at buffered ambient temperatures inside our facility. Over the course of the breeding season, the amount of milk production remained constant, but the fat content of the milk decreased. Hence, total energy transfer to young decreased significantly in autumn. By using undecanoic acid as a tracer of body fat mobilization, we were able to show that milk fat partially originated from maternal fat stores, particularly in spring. The peak sustained energy assimilation rates of lactating females were significantly higher in autumn, due to increased rates of food intake. We conclude that fat stores allow female hares to downregulate energy intake and expenditure early in the breeding season, whereas late breeding forces them to reach peak energy intake levels. Accordingly, we suggest that in hares, peak energy turnover during lactation varies with the availability of fat reserves. Limits to the sustained metabolic rate serve as variable constraints on reproductive investment. Thus, there might be a trade-off in energetic costs to mothers rearing early versus late litters in the year.

Plasticity in gastrointestinal morphology and enzyme activity in lactating striped hamsters (Cricetulus barabensis)

“…Lactation is the most energy-demanding state in the lifetime of most female mammals, which in small mammals is met primarily by increasing energy intake (Hammond and Kristan, 2000;Król and Speakman, 2003;Rogowitz, 1998;Speakman and Król, 2005;Valencak et al, 2009Valencak et al, , 2010Weiner, 1992). In the present study, energy intake increased by 292.8% in lactating hamsters compared with the non-reproductive group.…”

“…Although digestive plasticity is used by females to meet the energetic demands of lactation, a limit to sustained energy intake (SusEI) or total energy expenditure exists during peak lactation (Hammond and Diamond, 1992;Hammond et al, , 1996Król and Speakman, 2003;Król et al, 2003;Rogowitz, 1998;Valencak et al, 2009Valencak et al, , 2010Weiner, 1992). During the search for the mechanism behind limitations on SusEI, studies focused on several hypotheses, one of which is the central limitation hypothesis (Koteja, 1996b;Simons et al, 2011;Król, 2005, 2011).…”

Limits to sustained energy intake. XVII. Lactation performance in MF1 mice is not programmed by fetal number during pregnancy

“…Although fat stores may have contributed relatively little to overall lactation performance in the current study, we do not mean to imply this low contribution is the same in all small mammals. Valencak and colleagues, for example, found that female brown hares (Lepus europaeus) adjusted their investment in their young in relation to the size of their fat reserves (Valencak et al, 2009).…”

Why marathon migrants get away with high metabolic ceilings: towards an ecology of physiological restraint

“…We have also seen that free-living birds, except in the case of the marathon migrants, generally do not work harder than this either. The considerable gap between the maximum sustained working level of 4 or 5 times BMR that hard-working parent birds are prepared to give (Drent and Daan, 1980) and the physiological maxima of 7-10 times BMR that can be achieved under exceptional conditions makes evolutionary sense if working hard comes at a survival cost (Valencak et al, 2009). My reading of the literature suggests that any kind of hard work, perhaps above taxon-(or rather, ecology-) dependent thresholds (Speakman et al, 2002;Speakman, 2005;Furness and Speakman, 2008), comes with wear and tear.…”

“…My reading of the literature suggests that any kind of hard work, perhaps above taxon-(or rather, ecology-) dependent thresholds (Speakman et al, 2002;Speakman, 2005;Furness and Speakman, 2008), comes with wear and tear. A precipitous increase in the likelihood of organ or performance failure, and mortality associated with increases in energy expenditure (Ricklefs, 2008), would explain why animals are reluctant to habitually spend as much as they are physiologically capable of (Valencak et al, 2009); that is, if such precipitous increases the likelihood of death are not compensated for by increases in reproductive output (Williams, 1966;Lessells, 1991;Daan and Tinbergen, 1997). Evolutionary trade-offs would then select for animals that are not prepared to work harder than what we heuristically called the optimal working capacity (Fig.4) (Royama, 1966).…”