Microrefuges and the occurrence of thermal specialists: implications for wildlife persistence amidst changing temperatures

Microrefuges may help to buffer climate-sensitive species against temperature changes in warming environments [21, 75]. Our research provides evidence that the quality of microrefuges may be essential to the occurrence of mammalian thermal specialists, especially in ecosystems where temperatures are highly variable, such as in the alpine. Importantly, our work connects fine-scale, in-situ measurements of both the mean and the variability in microrefuge temperatures with species occurrence. Although other studies have quantified the extent to which microhabitats buffer ambient conditions [21, 23, 25, 76], comparatively few have evaluated the difference between the temperatures that an organism experiences in the surrounding territory (e.g., rock-surface conditions) and the operative conditions within available microrefuges. Even fewer have linked this difference to empirical species-occurrence information (but see [26]). Similar to caves and subterranean burrows, talus habitats provide non-living refuges to animals. Living microhabitats (e.g., ground vegetation) are more impacted by novel climates and, therefore, may provide less stable refuges compared to a non-living resource, such as talus [23].

We found robust support for our Microrefuge Hypothesis. The mean daily difference between surface and subsurface temperatures was the single-best predictor of pika occurrence. This result was particularly evident during the warm season, when green vegetation was available and pikas are most active on the surface of the talus (Fig. 4). Pikas were more likely to occur at sites where the subsurface environment substantially moderated surface temperatures, regardless of local-habitat characteristics or surface temperatures. The Interstitial-temperature Hypothesis received comparatively little support, indicating that the temperature within talus interstices alone was not sufficient to explain variation in pika occurrence. Relatively poor support for the Interstitial-temperature Hypothesis, coupled with strong support for the Microrefuge Hypothesis, especially during the warm season, suggests that microrefuges may shelter pikas from stressful surface conditions while simultaneously allowing access to resource benefits associated with particularly warm surface temperatures. Sites with warm mean daily surface temperatures, for example, are likely to experience earlier spring snowmelt, which provides earlier access to high-quality forage [77, 78]. Variation in dates of parturition and initiation of first litters, moreover, has been positively correlated with snowmelt in North American pikas (O. princeps and O. collaris; [79–81]). Additionally, sites that provide a substantial gradient between surface and subsurface temperatures may allow individuals to shed heat quickly, thereby facilitating rapid cooling during particularly warm periods. Cape ground squirrels (Xerus inauris), for example, frequently retreat to subterranean burrows during periods of high solar insulation, thereby moderating body temperature and quickly dissipating heat load [82].

Observed microrefuge temperatures at occupied and unoccupied sites (year-long). The observed differences between surface and subsurface temperatures at sites that were occupied and unoccupied by American Pika (Ochotona princeps) in the central Rocky Mountains, June – October 2010 – 2012. Data are summarized by Julian date, years averaged, and fit with a 3-day moving average. Two vertical, dashed lines denote the beginning and end of the warm season (1 June, 30 September, respectively), during which green vegetation was available, and pikas were collecting vegetation for overwinter food stores

During the warmest 7-day period of the study, below-talus temperatures were generally cooler than surface temperatures in the hottest parts of the day (1400–1800 hours), and warmer than surface conditions during the coldest (0200–0600 hours; Fig. 3). This is similar to findings by Henry et al. 2012, which showed that subsurface temperatures at pika-occupied sites were lower during the afternoon, and higher in the morning and night, compared to above-talus conditions [83]. The increased degree of temperature moderation at occupied sites likely provided animals with enhanced opportunities for rapid cooling, as well as greater protection from potentially stressful conditions.

The maximum mean daily difference between surface and subsurface temperatures was 2.0 C° over the duration of the sampling period (Fig. 1) and 5.6 C° during the warm season (Fig. 4). While these differences may seem small, a magnitude of even 2 C° reflects consistent modulation of surface-temperature extremes. The instantaneous difference between the surface and subsurface environment routinely exceeded 20 C° at some sites. Pikas maintain a high resting body temperature (( overline{x} ) = 40.1 °C) and a relatively low upper lethal temperature (( overline{x} ) = 43.1 °C; [30, 84]). Endothermic animals compensate for ambient temperatures that exceed their upper critical temperature (UCT) by increasing metabolism [85], or by taking advantage of convective/conductive heat loss. Even a few degrees of surface-temperature moderation may protect pikas from costly shifts in metabolism, as long as refuge temperatures remain below the UCT.

The subsurface temperatures that we observed during the warm season (( overline{x} ) = 12.69 °C, SD?=?5.39 C°; range ?2 °C – 21.94 °C) were comparable to other studies across the species’ range. Similarly, the average subsurface temperature during the summer in the southern Rocky Mountains was 10.6 °C (SD?=?2.9 C°) [86]; and 12.40 °C (SD?=?1.00 C°) at pika-extant sites and 17.05 °C (SD?=?0.81 C°) at pika-extirpated sites in the hydrographic Great Basin [31]. Lower mean interstitial temperatures were recorded in the Columbia River Gorge [21], though this is likely due to the temperature-buffering effects of moss cover prevalent on the surface of the talus, as well as topographical forcings that moderate temperatures in the gorge [21, 87].

Macrohabitat temperatures and biotic habitat characteristics may also influence the importance of microrefuges. For example, microrefuges might be especially important to pika occurrence where surface temperatures exceed physiological tolerances for prolonged periods. Surrounding vegetation can buffer interstitial temperatures through shading or through increased albedo [21]. Similarly, rock-ice features or subsurface water can influence microrefuge temperatures [38, 76]. Subsequent studies with sufficient sample sizes to fit a context-dependent model could provide useful insights on the merits of this hypothesis.

We found little support for our Local-habitat Hypothesis. Pika occurrence was positively associated with steeper slopes and northerly aspects, however, the effects of these local-habitat characteristics were relatively unimportant compared with effects of subsurface microrefuges. We expected pika occurrence to be positively associated with both forage availability [49, 56, 57] and elevation [36, 50]. However, there was little support for either term in our models. Compared with more arid parts of the species’ range, our study sites received relatively high annual precipitation. Consequently, pika populations in our system may be limited less by access to vegetation, compared with dryer areas containing lower plant biomass. The average forage availability at unoccupied sites was only 0.19 vegetation ‘hits’ less than occupied sites. Although individual pikas have unique diet-selection criteria [88], as a species they are generalist herbivores capable of consuming a variety of graminoids, forbs and bryophytes [61, 62]. Our measure of forage availability, however, did not address either vegetation diversity or the ratio of forbs: graminoids, both of which have been closely linked with metrics of pika population density elsewhere in the species’ range [86]. Given comparable forage availability across study sites, and relatively flexible diets, forage likely did not constrain pika occurrence in our system.

Elevation has been linked to pika-abundance indices across the range of the species [49, 50, 56], however, elevation itself likely does not limit pika distribution. Rather, elevation indexes relevant biological parameters that affect persistence. We directly measured the parameters that often are indexed by elevation, such as forage availability and temperature. Temperature metrics were more predictive of pika occurrence than elevation, which only indirectly reflected variation in climate conditions. Efforts both to understand current pika distribution, and to forecast future pika persistence under warming scenarios will be improved by incorporating in-situ temperature measurements [21], rather than surrogate variables such as elevation.

Microrefuges have the potential to buffer temperature-sensitive species against warming temperature trends [21, 26, 43]. They are not, however, a one-size-fits-all solution to facilitate species persistence. Use of microclimates can be costly, for example, if organisms shelter at the expense of other essential activities, such as foraging [22]. In addition, not all species have the behavioral capacity to capitalize on favorable microrefuges (e.g. [89]). If organisms are unable to take advantage of microrefuges, or if exploitation of microclimates inhibits essential processes, then reduced fitness ultimately will lead to extirpation. Species that can modulate behaviors to counter temperature extremes often are better able to exploit beneficial microenvironments. American pikas are capable of proximately adjusting to temperature variation through changes in body shape [33], food cache placement [62] and sheltering [34]. The degree to which behavioral flexibility, in combination with acclimatization and developmental plasticity [85], will facilitate the persistence of pikas and other animals in rapidly warming environments merits additional research.

Warming climate conditions have caused changes in the occurrence, abundance, morphology and phenology of species across the globe [3, 4]. The magnitude of these changes, however, is inconsistent among clades, biogeographic regions or even within subpopulations of the same species. Some of this variation may be attributable to fine-scale differences in microclimatic conditions [44]. Broad-scale temperature changes do not inherently produce the same magnitude of change at finer spatial scales [20]. Our understanding of species’ responses to changing climate dynamics will be substantially improved by quantifying the relationships between broad-scale temperature increases and microclimatic variation. One of the simplest steps towards this understanding is to measure climate parameters on scales that are relevant to the organisms under study [20, 90], including quantifying climate conditions associated with microrefuges.