Discussion
Striped hamsters suckling young at an ambient temperature of 32.5°C had a significantly lower sustained energy intake, produced less milk, and weaned lighter offspring, than those at 21°C. The temperature of a glass vessel wrapped in a fresh hamster pelt decreased at a significantly lower rate at 32.5°C than at 21°C, indicating that heat dissipation was considerably less at the higher temperature. This suggests that, consistent with the HDL hypothesis, the reduced capacity of female hamsters to dissipate heat at high temperatures may restrict their sustained energy intake and milk production. Females kept at an ambient temperature of 32.5°C that were exposed to simulated windy conditions increased their energy intake and milk production, which suggests that, by increasing the capacity to dissipate body heat, wind may allow an increase in milk production under hot conditions. More importantly, striped hamsters during the peak of lactation significantly preferred windy conditions at an ambient temperature of 32.5°C but not 21°C. Furthermore, the fact that significantly more lactating wild hamsters were captured on windy days than on calm days in summer, and on calm days than on windy days in spring, suggests that these are more active on windy days in summer and less active on windy days in spring. These findings support the hypothesis that wind increases female milk production by improving the capacity to dissipate body heat, thereby increasing reproductive performance and fitness under hot summer temperatures.
Lactation is the most energetically demanding part of the life cycle of small, female mammals and the increased food intake needed to meet the energy requirements of offspring frequently reaches a ceiling during the peak of lactation known as the limitation on sustained energy intake (Thompson 1992; Thompson & Nicol 2002). We found that the food intake of female striped hamsters increased during lactation and was significantly affected by temperature. The asymptotic food intake and gross energy intake of females lactating at an ambient temperature of 32.5°C were 51.2% and 54.9% less, respectively, than those of females lactating at 21°C. Adverse effects of high temperature on lactation have been observed in a variety of animals, including laboratory mice (Mus musculus, Król & Speakman 2003a; Król & Speakman 2003b; Wen et al. 2017), rats (Rattus norvegicus, Morag, Kali & Furman 1969; Leon & Woodside 1983; Jansen & Binard 1991), Brandt’s voles (Lasiopodomys brandtii, Wu et al. 2009), common voles (Microtus arvalis , Simons et al. 2011), Mongolian gerbils (Meriones unguiculatus, Yang et al. 2013), golden hamsters (Mesocricetus auratus , Ohrnberger et al. 2018), European brown hares (Lepus europaeus , Valencak, Hacklander & Ruf 2010), sheep (Ovis aries , Abdalla, Kotby& Johnson 1993), pigs (Sus scrofa , Black et al. 1993; Quiniou & Noblet 1999; Renaudeau & Noblet 2001; Renaudeau, Noblet & Dourmad 2003) and dairy cattle (Bos taurus ) (Cobble & Herman 1951). Collectively, these results suggest that the height of the food intake ceiling during peak lactation is lowered by high temperatures. As this ceiling defines the envelope within which all competing biological functions are constrained (Speakman & Król 2005), its reduction by high temperatures could adversely affect many aspects of physiology and behavior, in particular reproductive performance.
We found that the asymptotic food intake and gross energy intake of female hamsters during peak lactation were significantly affected by exposure to wind. The asymptotic food intake of hamsters lactating under simulated windy conditions at 21°C and 32.5°C were 17.1% and 25.4% higher, respectively, than those lactating under sheltered conditions. The gross energy intake of females kept at both 21°C at 32.5°C under simulated windy conditions was 21.7% and 28.8% higher, respectively, than that of females that were not exposed to simulated wind. This suggests that the response of female hamsters to wind is temperature dependent. The main energy output during lactation is meeting the energy requirements of offspring (Hammond & Diamond 1992; Hammond & Diamond 1997; Król & Speakman 2003a; Król & Speakman 2003b; Speakman & Król 2005; Valencak, Hacklander & Ruf 2010; Valencak et al. 2013). The marked increase in energy intake under windy conditions should therefore enhance milk production.
As expected, female hamsters lactating at an ambient temperature of 32.5°C had worse reproductive performance than those lactating at 21°C. Females lactating at 32.5°C produced, on average, 58.1% less milk, raised 29.5% fewer pups and had litters weighing 38.6% less, than those at 21°C. High temperatures have been found to reduce milk output in a variety of animal species (Cobble & Herman 1951; Morag, Kali & Furman 1969; Leon & Woodside 1983; Jansen & Binard 1991; Abdalla, Kotby& Johnson 1993; Black et al. 1993; Quiniou & Noblet 1999; Renaudeau & Noblet 2001; Król & Speakman 2003a; Król & Speakman 2003b; Renaudeau, Noblet & Dourmad 2003; Wu et al. 2009; Valencak, Hacklander & Ruf 2010; Simons et al. 2011; Zhao 2011; Valencak et al. 2013; Yang et al. 2013; Wen et al. 2017; Ohrnberger et al. 2018). These findings suggest that global warming could negatively affect the reproductive performance and fitness of many mammals. The HDL hypothesis predicts that the increased difficulty of dissipating body heat at higher temperatures limits both energy intake and milk production (Król & Speakman 2003a; Speakman & Król 2003b; Speakman & Król 2005; Wen et al. 2017). We found that the temperature of a water filled vessel wrapped in a fresh hamster pelt decreased at a significantly slower rate at 32.5°C than at 21°C, indicating that the thermal exchange of fur might be much less at 32.5°C than at 21°C. This is consistent with the HDL hypothesis’ prediction that the capacity of the body to dissipate heat could limit both maximum energy intake and milk production.
If the HDL is true, then any improvement in the capacity to dissipate body heat could increase milk production and thereby potentially increase fitness (Król & Speakman 2003a; Speakman & Król 2003b; Speakman & Król 2005). We found that exposure to simulated wind significantly increased both the evaporation and cooling rate of a fur-wrapped vessel at either 21°C or 32.5°C. This suggests that wind can considerably increase heat dissipation under both cool and hot conditions. Consistent with this prediction of the HDL hypothesis, exposure to simulated wind significantly increased the milk production of females at an ambient temperature of 32.5°C, but not at 21°C. An alternative hypothesis, the peripheral limitation hypothesis (PLH), proposes that the mammary glands reach the maximum extent of their capacity during peak lactation, thereby limiting both sustained energy intake and reproductive output (Hammond et al. 1994; Hammond, Lloyd & Diamond 1996; Hammond & Kristan 2000; Zhao & Cao, 2009 Zhao, Chi & Cao 2010c). The increased food intake we observed under simulated windy condition at 21°C could possibly be caused by the thermoregulatory demands of other tissues, such as the liver, skeletal muscle and brown adipose tissue, rather than that of offspring. Although this finding supports the peripheral limitation hypothesis, it does not refute the HDL hypothesis. The HDL and PLH are both likely to be valid under different conditions (Speakman & Król 2010; Speakman & Król 2011) i.e., reproductive performance could be limited both by the capacity of the mammary glands to produce milk and that of the body to dissipate heat; in other words, the PLH could be more applicable at room temperature and the HDL at higher temperatures (Wen et al. 2017). Reducing heat stress in lactating dairy cows is a major issue in the dairy industry where reduced milk production and increased mortality during heat waves cost many millions of dollars (Speakman & Król 2010; Speakman & Król 2011). We found that simulated wind significantly increased the thermal conductance and capacity to dissipate heat of striped hamsters at a relatively high ambient temperature, thereby increasing their milk energy output and reproductive performance. Exposure to wind during hot conditions could therefore reduce heat stress and improve the reproductive value and fitness of both wild animals and livestock.
It has been previously reported that wind has extensive effects on the behavior of animals, particularly birds (Smith & Weston 1990; Hayes & Huntly 2005; Chapman et al. 2010; Cornioley et al. 2016; Miller et al. 2016). For example, American white pelicans adopt different flying strategies in response to changes in wind conditions (Gutierrez et al. 2017). We found that female hamsters lactating at an ambient temperature of 21°C spent most of the day sheltering from simulated wind, whereas those lactating at 32.5°C spent significantly more time in simulated windy conditions. This indicates that lactating female hamsters prefer windy conditions when it is hot, but not when it is cool. As previously mentioned, wind increases heat exchange between the body and the environment (Porter & Gates 1969; Stevenson 1985). Heat loss under cool conditions is significantly exacerbated by wind (Porter and Gates 1969; Winne et al. 2001; Tracy & Christian 2005; Kearney & Porter 2009; Ortega, Mencía & Pérez-Mellado 2017). This suggests that under cool conditions animals exposed to wind increase their food intake to meet the increased energy demands of thermoregulation. Conversely, under hot conditions wind could improve the capacity to dissipate body heat, thereby increasing milk production and reproductive output. We caught more wild, lactating female hamsters on calm than on windy days in spring, which suggests that these are less active on windy days. However, in summer the reverse was true; we caught 5-times more lactating females on windy days than on calm days. Collectively, our results suggest that the effect of wind on the behavior of lactating females is temperature dependent. Birds are known to vary their migration routes and flight strategies according to the wind conditions (Wiltschko & Wiltschk 2003; McLaren, Shamoun-Baranes & Bouten 2012; Limiñana et al. 2013; Vansteelant et al. 2015; Vidal-Mateo et al. 2016; Gutierrez et al. 2017; Vansteelant et al. 2017). Female mammals may have a strong preference for windy conditions in the heat of summer because wind makes it easier to dissipate heat and thereby increase milk production and fitness.