Introduction
Global warming and increasing climatic variability could alter the distribution of animals and change their morphology, physiology, behavior and life history (Mifsud et al. 2011; IPCC Working Group 1 2014; Smith et al. 2014; Martin, Mead & Barboza 2018). High temperatures adversely impact small mammals by making it harder to dissipate heat, thereby increasing the risk of hyperthermia (Quiniou & Noble 1999). This risk is particularly high for lactating females because ingesting the additional food required to produce milk increases energy expenditure, and therefore heat production (Speakman & Król 2005). Therefore, the adverse effects of high temperature on small mammals are greatest during reproduction, and in particular, during lactation.
Exposure to high ambient temperatures has been widely reported to decrease food intake and milk yield in a variety of animals, including both small and large mammals (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; Valencak, Hacklander & Ruf 2010; Valencak et al. 2013; Wu et al. 2009; Simons et al. 2011; Zhao 2011; Yang et al. 2013; Wen et al. 2017; Ohrnberger et al. 2018). Exposure to high temperatures typically reduces milk production, and thereby litter growth rate and other indicators of maternal reproductive performance (Król & Speakman 2003a; Król & Speakman 2003b; Wen et al. 2017). Król and Speakman (2003a, 2003b) advanced the heat dissipation limitation hypothesis (HDL) to explain the adverse effect of high temperatures on female reproductive performance. This proposes that ability to dissipate body heat limits a female’s maximum rate of sustained energy intake and milk output. If this is true, female mammals lactating under hot conditions should compensate by either decreasing their milk production and extending the duration of lactation, or by decreasing their litter size or the size of their offspring. The latter two strategies should decrease the risk of hyperthermia, albeit at the cost of reduced reproductive performance and fitness. However, an alternate possibility is that females may attempt to maintain their reproductive performance under hot conditions by actively seeking out conditions that improve their ability to dissipate heat. This possibility is, to the best of our knowledge, so far untested.
Heat exchange between animals and the environment includes radiation, convection, conduction and evaporation, and the difficulty of dissipating heat under hot conditions is due, at least to some degree, by the low thermal conductance of the fur, which is important for insulation against cold. Wind increases heat exchange by increasing the effective thermal convection, conduction and evaporation (Porter & Gates 1969; Stevenson 1985). Many animal species frequently experience unpredictable changes in wind speed that can affect their activity and thermoregulation (Sun et al. 2001; Maia-Carneiro, Dorigo & Rocha 2012; Scheers & Van Damme 2002; Logan, Fernandez & Calsbeek 2015). Wind decreases the ambient air temperature thereby promoting heat loss by convection (Porter & Gates 1969; Kearney & Porter 2009; Ortega, Mencía & Pérez-Mellado 2017). In addition, wind increases water loss, which increases heat dissipation via convection and evaporation (Winne et al. 2001; Tracy & Christian 2005; Ortega, Mencía & Pérez-Mellado 2017). Migratory birds are known to select favorable wind conditions allowing faster, safer, and more direct, migration routes (Wiltschko & Wiltschk 2003; McLaren, Shamoun-Baranes & Bouten 2012; Vansteelant et al. 2015; Gutierrez et al. 2017). The flight of larger, soaring birds is particularly likely to be strongly affected by wind currents (Limiñana et al. 2013; Vidal-Mateo et al. 2016; Gutierrez et al. 2017; Vansteelant et al. 2017). For example, American white pelicans (Pelecanus erythrorhynchos ) adopt different flying strategies to cope with different wind conditions (Gutierrez et al. 2017). Changing wind conditions have been found to markedly affect the locomotion, foraging, activity levels and reproductive success of not only birds, but also insects and small mammals (Smith & Weston 1990; Hayes & Huntly 2005; Chapman et al. 2010; Cornioley et al. 2016; Miller et al. 2016). Although the effect of temperature on animals’ physiology and behavior has been extensively studied, relatively is known about the effect of wind on the capacity to dissipate body heat and reproductive performance.
The striped hamster (Cricetulus barabensis ) is a common rodent in northern China, Russia, Mongolia and Korea (Zhang & Wang 1998). This species is nocturnal and granivorous, feeding mainly on the stems and leaves of plants during summer and seeds in the winter (Lu, Li & Zhang 1987; Zhang & Wang 1998; Song & Wang 2002, 2003; Zhao et al. 2010a; Zhao et al. 2010b). The striped hamster prefers sandy areas, as well as farmland and grassland. Breeding occurs from February to November, during which there are two reproductive peaks; one in spring and one in autumn (Xing, Feng & Lu 1991; Zhu & Qin 1991; Dong et al. 1993; Hou et al. 1993; Jiang et al. 1994; Bao et al. 2001; Wang et al. 2003; Zhao, Chi & Cao 2010c). The species experiences considerable seasonal fluctuations in both ambient temperature and wind speed, particularly in spring, autumn and winter. Although temperature is known to have a significant effect on the striped hamster’s thermoregulation and reproduction, the effect of wind is unknown. This paper presents the results of four experiments designed to determine the effects of both temperature and wind on the maximum energy intake, reproductive output and thermal conductance, of lactating striped hamsters. We also examined the activity of wild hamsters on windy and calm days during both cool spring and hot summer conditions. We hypothesized that exposure to wind during hot weather may increase females’ reproductive performance by improving their ability to dissipate body heat.