Thermoregulation and the maternal behaviour of the rat

SUMMARYLactating animals consume greater amounts of food than non-reproductive animals, but energy intake appears to be limited in late lactation. The heat dissipation limit theory suggests that the food intake of lactating mice is limited by the capacity of the mother to dissipate heat. Lactating mice should therefore have high body temperatures (T b ), and changes in energy intake during lactation should be reflected by variation in T b . To investigate these predictions, 26 mice (Mus musculus) were monitored daily throughout lactation for food intake, body mass, litter size and litter mass. After weaning, 21days postpartum, maternal food intake and body mass were monitored for another 10days. Maternal activity and T b were recorded every minute for 23h a day using implanted transmitters (vital view). Energy intake increased to a plateau in late lactation (days 13-17). Daily gain in pup mass declined during this same period, suggesting a limit on maternal energy intake. Litter size and litter mass were positively related to maternal energy intake and body mass. Activity levels were constantly low, and mice with the largest increase in energy intake at peak lactation had the lowest activity. T b rose sharply after parturition and the circadian rhythm became compressed within a small range. T b during the light period increased considerably (1.1°C higher than in baseline), and lactating mice faced chronic hyperthermia, despite their activity levels in lactation being approximately halved. Average T b increased in relation to energy intake as lactation progressed, but there was no relationship between litter size or litter mass and the mean T b at peak lactation. These data are consistent with the heat dissipation limit theory, which suggests performance in late lactation is constrained by the ability to dissipate body heat. Supplementary material available online at

Section: Physical Activity and Body Temperature In Lactating Micementioning

confidence: 99%

Limits to sustained energy intake XX: body temperatures and physical activity of female mice during lactation

Gamo

Troup

Mitchell

et al. 2013

“…According to the peripheral hypothesis, milk secretion may not be changed in the females during peak lactation, regardless of the PRL levels produced. However, the heat dissipation limits hypothesis predicts that the suckling unit of mother and pup(s) may generate heat that leads to maternal hyperthermia and forces the female to discontinue suckling, ultimately resulting in lower levels of PRL produced and lower reproductive output (Croskerry et al, 1978;Speakman and Król, 2005). Thus, the measurements of PRL levels and the analysis of correlations between PRL and food intake or reproductive output may be helpful to distinguish the peripheral hypothesis from the heat dissipation limits hypothesis.…”

Section: Introductionmentioning

confidence: 99%

Energy budget during lactation in striped hamsters at different ambient temperatures

Zhao

2011

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 ...

“…One possible explanation for this apparently anomalous result is that mice with large litters were at risk of hyperthermia owing to increased milk production. These animals may consequently have attempted to reduce milk production, especially during peak lactation, leading to a reduction in prolactin production and release (Croskerry et al, 1978;Speakman and Król, 2005) and the consequent absence of between-group differences in prolactin levels. Regulation of the mammary glands by prolactin in the WT group may have be attenuated, which suggests that SusEI may be regulated by downstream physiological, morphological and behavioral factors associated with mammary gland function.…”

Section: Prolactin and Neuropeptide Gene Expression In The Hypothalamusmentioning

confidence: 99%

“…Continual maternal hyperthermia in relation to the suckling unit of mother and pups at peak lactation forces the female to discontinue suckling, and therefore directly inhibits prolactin secretion, thereby reducing milk production (Croskerry et al, 1978;Speakman and Król, 2005). Prolactin, released from the pituitary in response to suckling stimulation, has been implicated in a wide range of physiological systems, including reproduction, development and metabolism (Woodside, 2007;Carré and Binart, 2014).…”

Section: Introductionmentioning

confidence: 99%

Sustained energy intake in lactating Swiss mice: a dual modulation process

Wen

Tan

Qiao

et al. 2017

Limits to sustained energy intake (SusEI) during lactation are important because they provide an upper boundary below which females must trade off competing physiological activities. To date, SusEI is thought to be limited either by the capacity of the mammary glands to produce milk (the peripheral limitation hypothesis) or by a female's ability to dissipate body heat (the heat dissipation hypothesis). In the present study, we examined the effects of litter size and ambient temperature on a set of physiological, behavioral and morphological indicators of SusEI and reproductive performance in lactating Swiss mice. Our results indicate that energy input, energy output and mammary gland mass increased with litter size, whereas pup body mass and survival rate decreased. The body temperature increased significantly, while food intake (18 g day −1 at 21°C versus 10 g day −1 at 30°C), thermal conductance (lower by 20-27% at 30°C than 21°C), litter mass and milk energy output decreased significantly in the females raising a large litter size at 30°C compared with those at 21°C. Furthermore, an interaction between ambient temperature and litter size affected females' energy budget, imposing strong constraints on SusEI. Together, our data suggest that the limitation may be caused by both mammary glands and heat dissipation, i.e. peripheral limitation is dominant at room temperature, but heat dissipation is more significant at warm temperatures. Further, the level of the heat dissipation limits may be temperature dependent, shifting down with increasing temperature.