Reproductive and Environmental Drivers of Time and Activity Budgets of Striped Skunks.

Predictable energetic costs incurred across an animal’s life can be broadly divided into those imposed by abiotic changes in their environment (e.g., temperature, photoperiod, and precipitation) (Forrest and Miller-Rushing 2010) and biotic changes in physiology and behavior. Animals that inhabit highly seasonal environments, such as those at high latitudes and altitudes, typically experience greater seasonal fluctuations than their lower latitude and altitude counterparts and thus experience significant constraints on time–energy budgets across the year. In addition, many species undergo predictable seasonal changes in physiology and behavior associated with reproduction. These physiological changes are accompanied by significant differences in an animal’s energetic requirements with the timing of peak energy demand often differing between sexes. As the relative importance of thermoregulatory and reproductive demands fluctuate across the day and year, how animals concomitantly allocate their time and energy determines their survival and reproductive success. Given that movement-based energy expenditure contributes significantly to total energy expenditure (Brown et al. 2013), many have hypothesized that animals behaviorally compensate via regulation of activity patterns (Gittleman and Thompson 1988; Logan and Sanson 2003; Terrien et al. 2011). Examining how animals regulate activity on both daily and seasonal time scales is necessary to understand the energetic consequences of adjustments to activity budgets. The daily light:dark cycle is one of the most predictable synchronizing agents of daily activity patterns of animals. The timing of activity across the day influences the fitness costs and benefits of many behaviors (Daan and Aschoff 1982). Some small mammals adjust their timing of activity seasonally to consolidate activity during the time of day that is thermally most efficient (Tachinardi et al. 2017; Kenagy 2002) or to match resource availability (Hut et al. 2011; van der Vinne et al. 2015). Within a species, individuals can vary in their propensity to be active at particular times of the day, referred to as their “chronotype” (Horne and Ostberg 1976; Roenneberg et al. 2007; Hau et al. 2017). Moreover, the timing of daily activity has been argued to be a sexually selected character trait in mammals, and sexual selection theory predicts that males should initiate daily activity earlier during the mating season relative to the rest of the year, as they seek to intercept receptive females (Hau et al. 2017). Timing as a sexually selected trait has been studied primarily in birds, with the most prominent example being the dawn song of male birds. Variation in the timing (substrate of sexual selection) of the onset of dawn singing is correlated with variation in extra-pair paternity (Krebs and Kacelnik 1983; Poesel et al. 2006; Kempenaers et al. 2010). Currently, there is a dearth of empirical evidence on whether chronotype is a sexually selected trait in mammals due to the difficulties associated with gathering fine-resolution data on daily patterns of individual activity. Seasonal life cycle transitions are associated with changes in physiology and behavior that allow animals to meet environmental and reproductive demands. For example, in temperate environments, the winter activity levels of mammals are often lower than in other seasons due to factors including snow cover (Raine 1983) and unfavorable thermoregulatory conditions (O’Farrell 1974; Owen-Smith 1998). Also, when negative energy balance can be anticipated because of predictable seasonal environmental changes, some species use daily torpor or seasonal hibernation to conserve energy (Ruf and Geiser 2015). However, the relative importance of thermoregulatory versus reproductive requirements will shift with onset of the breeding season, and sex-specific differences in the timing of energy allocation toward reproduction often results in time-activity budgets that differ between sexes. Breeders will begin to allocate more time and energy toward reproductive effort as food availability increases and thermoregulatory costs decrease (Massei et al. 1996; Geisser and Reyer 2005; Persson 2005). In species with polygynous and promiscuous mating systems, the most important resources for males are hypothesized to be receptive females during the breeding season and food during the non-breeding season. In contrast, successful reproduction by females is linked to their ability to acquire food during critical parts of the year to meet elevated maternal and offspring energy requirements (Erlinge and Sandell 1986). Yet, how sex-specific differences in reproductive effort relate to the intensity or timing of activity in polygynous/promiscuous species has rarely been investigated quantitatively. One logistical challenge to understanding activity patterns in free-living mammals is that tools such as camera-trapping, live-trapping, and radio tracking, do not provide continuous information on an animal’s activity across the day and year. Generally, studies on the biological timing of activity require long term and precise data to adequately estimate daily and seasonal trends (Hau et al. 2017). The reduction in size and cost of biologging devices, such as accelerometers, now enable researchers to understand the fine-scale activity patterns of mammals (Williams et al. 2016a). Accelerometers continuously measure and record acceleration on three orthogonal axes and provide an integrated measure of overall dynamic body acceleration (ODBA) (Halsey et al. 2008, 2009). ODBA reflects total movement of an animal and increases with increasing activity levels. The strong correlation between ODBA and activity-specific energy expenditure has been demonstrated in a range of mammals (Halsey et al. 2009; Pagano and Williams 2019), birds (Wilson et al. 2006), amphibians (Halsey and White 2010), and reptiles (Halsey et al. 2011). In North America, the striped skunk (Mephitis mephitis) is a common and abundant nocturnal mesocarnivore that likely experiences significant sex-specific differences in energetic requirements across the year (Storm 1972; Sunquist 1974; Lariviere and Messier 1997; Weissinger et al. 2009; Neiswenter et al. 2010). As polygynous/promiscuous breeders, male skunks actively search for mating opportunities with multiple females during the mating season. In captivity, females show aggressive behavior toward males soon after mating (Verts 1967), so mate guarding, if it occurs, is likely to be brief and males should maximize the number of receptive females they can encounter. Mating activities of male skunks typically begin in early spring and last 4 weeks (Ernst 1965). Gestation is ∼68 days, with parturition occurring during late spring–early summer (Wade-Smith and Verts 1982). Females are the sole contributors to the care of young (Wade-Smith and Verts 1982) and the altricial young are nursed in the maternal den for 6 weeks (Lariviere and Messier 1997). Young are at heel by mid- to late-summer, then disperse and begin fattening for the subsequent winter by fall (Wade-Smith and Verts 1982; Lariviere and Messier 1997). Given the solitary and secretive nature of many nocturnal carnivores, it is difficult to robustly sample their activity patterns. Here, we deployed accelerometers on striped skunks to understand how reproductive and environmental drivers may interact to influence patterns of activity across the day and year. In related hog-nosed skunks (Conepatus chinga), ODBA has been shown to be a proxy for oxygen consumption (Halsey et al. 2009). Because timing of daily activity is likely a sexually selected trait in mammals (Hau et al. 2017), we hypothesized that males would initiate activity earlier in the day during the mating season than during other times of year. We further hypothesized that activity levels of striped skunks would reflect sex-specific differences in timing and energy allocation toward reproduction. To better infer the physiological significance of activity and its association to overall energy balance in skunks, we also examined the timing of activity onset and offset, duration of activity bouts, and distribution of activity patterns (activity timing) across the day. Reproductive females have been shown to increase their foraging efforts during the energetically costly period of lactation (Kenagy et al. 1989; Fletcher et al. 2012). Thus, we predicted that daily activity of female skunks during lactation would be higher than during other seasons. As males compete for access to multiple females, we also predicted that activity of reproductive males would be greatest during the spring mating interval. Lastly, we hypothesized that unfavorable weather such as cold and wet conditions would decrease activity of both male and female skunks.