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Spring 5-19-2017 Understanding the complex relationships between climate, vegetation, and foraging behavior of a climate-sensitive alpine mammal in order to explain patterns of persistence Evan Cole University of San Francisco, [email protected]
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Recommended Citation Cole, Evan, "Understanding the complex relationships between climate, vegetation, and foraging behavior of a climate-sensitive alpine mammal in order to explain patterns of persistence" (2017). Master's Projects and Capstones. 566. https://repository.usfca.edu/capstone/566
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This Master's Project
Understanding the complex relationships between climate, vegetation, and foraging behavior of a climate-sensitive alpine mammal in order to explain patterns of persistence
by
Evan Cole
is submitted in partial fulfillment of the requirements for the degree of:
Master of Science in Environmental Management
at the
University of San Francisco
Submitted: Received:
5/17/17 ...... ………...... …………. Evan Cole Date John Callaway, Ph.D. Date
Table of Contents
Abstract …………………………………………………………………………………………1
Background …………………………………………………………………………………….2 - Mountain Ecosystems - Study Organism: The American Pika - Current Status and Distribution - A Model Organism - Vegetation as a predictive variable: A brief literature review
Research Methods …………………………………………………………………………..10
Results ………………………………………………………………………………………...11 - What plant characteristics are important to pikas, and how do they influence behavior and survival? - How do pikas alter their local plant community? - How does climate (and climate change) influence pika persistence and alpine plant communities?
Discussion ……………………………………………………………………………………36 - Climate and Forage Tightly Linked - Conditional Importance of Plant Secondary Chemistry - Interactive Effects of Climate on Forage Selectivity and Availability - Lessons from an Indicator Species
Management Recommendations …………………………………………………………40 - Habitat Restoration and Enhancement - Legal and Regulatory Actions - Adaptive Capacity as a Conservation Metric
Appendix ………………………………………………………………………………………43
Acknowledgements …………………………………………………………………………51
Literature Cited ………………………………………………………………………………51
Abstract
Mountain ecosystems offer substantial ecosystem services but are highly sensitive to climate change. The American pika (Ochotona princeps) serves as an indicator species of climate change and a model organism for studying its impacts on mountain mammals. Certain aspects of plant community composition and structure can function as predictors of pika distribution, but understanding the links between climate, forage quality, and foraging behavior is necessary to identify the mediating mechanism. Pika foraging pressure help shape the local plant community, which can confound modeling efforts and must be considered when evaluating the influence of vegetation on pika persistence. Plant Secondary Metabolites (PSMs) appear to be the most important indicators of forage quality, driving winter diet selection, especially in high elevation areas with extreme seasonality. Nutritional components, such as protein, nitrogen, and water content, are more important to summer diet. Foraging selectivity for nutritional components changes in response to environmental conditions and forage availability, suggesting increased importance as climate warms and dries. While metrics of heat stress, cold stress, and water budget appear to be significant divers of pika distribution, the heterogeneity with which climate impacts pikas across their range calls for a place- based perspective. The transformation of alpine plant communities in response to climate change may further stress pika populations as preferred forage items become scarcer. Pikas highlight the complexity and idiosyncrasy of alpine ecosystems. In order to address the challenges faced by pikas, managers should identify refugia and vulnerable populations, install plants high in PSMs and nutritional components, work to control invasive plants, consider legal and regulatory protections, and expand monitoring efforts.
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Background
Mountain Ecosystems Covering nearly a quarter of the Earth’s land surface, mountains are quite literally springs of life and civilization. Functioning as natural water towers, mountains are the ultimate source of drinking water, hydroelectricity, and irrigation for 40% of the world’s population (UNESCO 2014). Steep topographic and vegetative gradients promote high beta and gamma diversity, and most of the protected landscapes across the western U.S. and the world are in mountains (Beever et al. 2013). Additionally, mountains are key sources of timber, mineral resources, medicinal plants, and flood control, as well as significant recreational opportunities and aesthetic value. These vital ecosystem services, which reach well beyond the isolated geography of mountain ecosystems, are becoming increasingly jeopardized by global change.
Mountain ecosystems serve as early warning indicators of climate change impacts, but further attention and research are necessary to adequately interpret the signals. High- elevation areas are warming at a significantly accelerated rate compared to low- elevation areas (Figure 1) due to a variety of potential mechanisms and interacting feedback loops, such as the loss of snow and ice and the associated reduction in albedo, the increasing release of latent heat in the high atmosphere as water vapor condenses, and the cooling effect of aerosols at lower elevations (Pepin et al. 2015). Despite our reliance on mountain ecosystems for ecological, economic, and recreational benefits, they are poorly monitored due to their isolated nature. Long-term climatic trends are difficult to characterize for high-elevation areas, as meteorological stations become increasingly sparse at higher elevations (Pepin 2015). Mountain ecosystems offer a unique laboratory for studying the ecological implications of climate change, and understanding how these sentinels of global change respond can inform conservation strategies and secure essential natural resources for the future.
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Figure 1. Rate of warming is greater at high elevations. Note that average temperatures are lower at high elevations. (Beever 2016)
Study Organism: The American Pika The American pika (Ochotona princeps) is a small, egg-shaped mammal found in alpine and subalpine ecosystems of western North America. Though commonly mistaken for a rodent, the pika is actually in the order Lagomorpha and is related to rabbits and hares. The pika is a generalist herbivore, feeding upon a variety of available vegetation, and a habitat specialist, generally found only on rocky outcroppings and talus slopes (Dearing 1996). One defining life history trait of the pika is that it does not hibernate, instead
Page 3 of 62 caching plant material in haypiles, upon which it feeds throughout the winter while most other vegetation has died back (Dearing 1997a). While the pika is typically considered diurnal, it can shift its behavior to be crepuscular or even nocturnal based on stressful environmental conditions, such as high daytime temperatures (Smith 1974). Pikas are highly territorial, with a single individual occupying its own home range, and maximum dispersal distances are likely around just 10-20 km (USFWS 2010). Despite its small size and undeniably adorable disposition, the pika is actually quite hardy and highlights the rugged adaptability of high elevation species.
Current Status and Distribution Widely considered an indicator species, or ‘canary in the coal mine,’ foreshadowing climate change impacts on montane mammals, the American pika has garnered significant interest from scientists and the environmental community. Due to the isolated and limited extent of its habitat (talus fields and rocky outcroppings), as well as its small size, limited mobility, and poor thermoregulation, the pika is extremely sensitive to climatic changes (Castillo et al. 2014). Recent studies have shown evidence of widespread distributional loss, including upslope retractions and local extirpations, with climate change implicated as a likely cause (Beever et al. 2016a). Population shifts have varied by region, with steeper declines observed in the Great Basin compared to the Sierra Nevada. In fact, a recent study involving resurveying nearly one thousand talus patches in three geographic regions – the Sierra Nevada, Great Basin, and northern Utah – found extirpations of the pika from five of nine sites in the Great Basin (sites defined as all talus patches within a 3 km radius of a historical occupancy record) and eleven of twenty-nine sites in northeastern California (sites defined as all talus patches within a 1 km radius of a historical occupancy record, consistent with earlier survey methods in that area). Strikingly, even though pikas had been observed in Zion National Park and Cedar Breaks National Monument in northern Utah as recently as 2011 and 2012, respectively, the study concluded that they are now extirpated from both locations. Despite growing concern, the American pika was denied listing by the US Fish and Wildlife Service (USFWS) in 2010, and another petition was rejected in September 2016; the reasoning in both cases was cited as lack of substantial evidence
Page 4 of 62 demonstrating a need for federal protections based on the range of identified threats. Further study and monitoring of climate change impacts on pika range, distribution, and population dynamics can inform management decisions for the benefit of both the species and the entire ecosystem.
A Model Organism Due to its distinctive life history, behavioral patterns, and sensitivity to climatic stressors, the American pika is considered an excellent model organism for studying the impacts of climate change on montane mammals. Firstly, the pika is uniquely sensitive to rising temperatures due to its low physiological tolerance for heat – succumbing to hyperthermia in as little as 6 hours of exposure to 25.5 °C (77.9 °F) (Smith 1974) and 2 hours of exposure to 28 °C (82.4 °F) (MacArthur and Wang 1973). The cage experiments utilized by Smith (1974) and MacArthur and Wang (1973), though tragic for the participating pikas, offered a valuable indication of the animal’s upper physiological tolerance for heat – a metric that would be difficult to obtain by today’s ethics standards. Second, pikas are locally abundant and easily detectable. While most mammals are nocturnal (70%; Bennie et al. 2014) and are monitored primarily using camera traps and tagging, pikas are diurnal or crepuscular, depending upon the locality and season, and can be easily observed. Their distinct vocalizations, used for conspecific attraction, announcing territory, and signaling alarm (Ray et al. 1991), as well as their large haypiles, scat, and urine stains on the talus (personal communication), provide further evidence of occupation. Additionally, their populations display relatively high interannual stability, which decreases the likelihood of incorrectly identifying a patch as extirpated due to a sudden and temporary drop in the local population (Beever et al. 2010). Finally, the pika is a habitat specialist, relying upon talus patches and rocky outcroppings, which makes it easier to locate and monitor pika metapopulations. Individual pikas do not share territories (Peacock 1997), which are typically only about 20 meters in diameter (Moyer-Horner et al. 2016). Maximum dispersal distances are generally considered to be just a few hundred meters (Castillo et al. 2014). Due to its isolated nature, talus habitat has largely escaped direct transformation or degradation by humans and is relatively stable across biologically relevant timescales, which allows researchers to
Page 5 of 62 evaluate the effects of climate independent of habitat loss (Beever et al. 2010). As an indicator species within a larger sentinel of global change – mountain ecosystems – the pika offers a first look at the mechanisms of biological response to climate change. Understanding the factors that mediate this biological response, either through direct climatic stress or through indirect impacts like altered food or water availability, may help managers to preserve the species and get ahead of further ecological consequences.
Vegetation as a predictive variable: A brief literature review While climate has been implicated as the primary driver of rapid range shifts and extirpations of pika populations in the Great Basin (Beever et al. 2010, 2011, 2016) and in other parts of its range (Erb et al. 2011, Calkins et al. 2012, Jeffress et al. 2013), vegetation (i.e., plant community composition and structure) has been suggested as a potential mechanism to either buffer or facilitate climate impacts. Recent attempts to characterize this relationship between climate, vegetation, and pika persistence have largely focused upon margins and leading-edges of the pika’s range (Rpdhouse et al. 2010, Varner and Dearing 2014, Varner et al. 2015, 2016). Range margins often feature atypical habitat or microclimates that allow the species to persist where it otherwise could not, making them ideal locations for research into the mechanisms and determinants of range limitations, the effects of extreme environmental conditions and stress on individuals and populations, and the adaptive capacity of the study organism (Ray et al. 2016, Varner et al. 2016).
Metrics of forb cover seem to be the most prevalent and significant predictors of pika occupancy or population density across most studies. Though relatively less abundant among the talus – more commonly found in nearby alpine meadows or the talus margin – forbs are selectively collected and cached by pikas and make up a relatively large portion of the winter haypile (Huntly et al. 1986). The Plant Secondary Metabolites (PSMs), particularly phenolics, found in many forbs act as preservatives and deter the pikas from eating the plants until the winter and spring months when the compounds have degraded (Dearing 1997). At Lava Beds National Monument, a range margin with
Page 6 of 62 atypically warm and arid conditions for the pika, the two best predictors of site-use intensity have been metrics of graminoid:forb cover and total forb cover (Ray et al. 2016). The ratio of graminoid:forb cover serves as a metric for plant secondary chemistry, as graminoids do not contain PSMs while forbs are generally high in them, and indicates the importance of PSMs to pika occupancy dynamics. Forb cover was also implicated as a key predictor of pika occupancy in the range periphery lava flow habitat of Craters of the Moon National Monument and Preserve (Rodhouse et al. 2010). In Glacier National Park, a leading-edge of the pika’s range that could represent an important refugium as the climate warms, average forb height and moss cover – an evergreen, persistent food source – have been demonstrated as the two strongest predictors of short-term pika occurrence (Moyer-Horner et al. 2016). Forb height suggests the importance of plant morphology for facilitating the efficient gathering of winter haypile components (Millar and Zwickel 1972). Interestingly, relative forb cover outperformed absolute cover of forbs or graminoids in Glacier National Park, indicating that there may be an interactive effect between forb and graminoid cover that is more important than the total cover of either plant type. Studies in the Southern Rocky Mountains have suggested similar measures of vegetation quality – the diversity and relative cover of forbs – to be superior predictors of pika population density (Erb et al. 2014). This growing evidence of correlations between metrics of forb cover and pika distribution, considering the established importance of forbs to pika behavior and diet, indicates a potentially significant link between forage quality and pika persistence and also raises the question of what other plant qualities and types may be influential.
A few studies in the Great Basin have incorporated broad vegetative components into larger analyses of climate-mediated extirpations, but these have been limited in spatial and temporal scope, as well as in the types of vegetative predictors considered. In agreement with finding from other parts of the pika’s range, relative forb cover has been demonstrated as a powerful predictor of pika persistence in the Great Basin (Wilkening 2007, Wilkening et al. 2011). Overall vegetation cover, foliar cover, and relative tree cover negatively correlate with pika persistence, perhaps because a dense canopy impedes a pika’s ability to surveil its territory and provides perches for predatory birds
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(Wilkening 2007). Sites with higher mean summer temperatures and lower relative cover of forbs show greater rates of extirpation, potentially indicating that pikas in areas with less forb cover must expose themselves to more heat stress as they spend more time searching for suitable plant material for their winter haypile (Wilkening 2011). However, this inverse relationship between mean summer temperature and relative forb cover may simply reflect the long-term climate’s simultaneous influence on plant community composition and pika population dynamics, as xeric conditions may limit both forbs and pikas.
Pikas in atypical habitats spend more time foraging and less time haying, reflecting the warmer winters and greater winter forage availability found at lower elevations. Research at the Columbia River Gorge, a range margin characterized by higher temperatures and lower elevations than those typically occupied by pikas, has demonstrated a strong relationship between plant community composition and pika persistence, as well as provided a unique example of climate adaptation through dietary plasticity – the shifting of diet to accommodate what food items are available. Here, vegetation species richness and percentage moss cover have been shown to be the most significant predictors of pika density (Varner et al. 2015). Dietary plasticity through utilization of moss is a key adaptation that pikas exhibit in order to exist in such atypical, harsh environments (Varner and Dearing 2014). More than 60% of the pika’s diet consists of moss in some areas of the Columbia River Gorge, more than has been observed for any wild mammalian herbivore. In contrast to the seasonal growth and die- back of grasses and forbs, moss is available year-round, releasing pikas from needing to collect and store sizeable haypiles for winter during the summer and early fall months, and thereby minimizing energy expenditure and exposure to extreme heat (Varner et al. 2016). In fact, the Siberian northern pika (Ochotona hyperborea) actively avoids evergreen forbs, cushion plants, mosses, and lichens when collecting for its haypile, as those types of forage are available throughout winter and do not need to be cached (Gliwicz et al. 2006), further suggesting that the relative value of grazed plants compared to hayed plants may depend upon local climatic and environmental factors.
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The reliance on moss also reduces the need for pikas to venture away from the talus to forage, mitigating the risk of predation.
As further evidence of adaptive utilization of vegetation, pikas existing in atypical habitats are more likely to be found in forested habitat away from the talus during midday compared to pikas existing in the more typical, high-elevation habitat of nearby Mt. Hood, suggesting the potential for forested stands to act as thermal refuge off the talus (Varner et al. 2016). Pikas in the atypical habitats of the Columbia River Gorge exhibit higher population density and smaller home ranges than their high elevation counterparts, but do not display increased signs of territoriality, suggesting an abundance of local resources or a decrease in territoriality due to the lack of a need to defend large winter hay piles. Although it is important to note the potential influence of genetic differentiation between the two study groups, which would indicate genetic adaptation rather than behavioral plasticity, evidence from range margins like the Columbia River Gorge highlight the mediating power of vegetation in pika persistence in the face of climatic stress.
Though limited, recent research has demonstrated a clear, if difficult to interpret, relationship between pika occurrence and certain metrics of vegetation quality. In an attempt to explain the apparent significance of vegetation’s role in determining pika distribution, three general hypotheses have been proposed: 1) quality of available forage is important for pika persistence, 2) pikas shape the composition and structure of the local plant community and so the perceived relationship merely reflects correlation rather than causation, and 3) microclimate is the true driver affecting pikas and plants simultaneously (Wilkening et al. 2011, Ray et al. 2016). Though the interactions between pikas, their respective plant communities, and microclimate are complex, understanding the mechanisms of persistence and extirpation in the face of a changing climate is essential for developing useful conservation strategies. Further research with expanded spatial and temporal scopes, such as in this study, may help rank these three hypotheses and elucidate the mechanisms of biological response to climate change. In the following sections, I address these three explanations in order to provide context for
Page 9 of 62 my primary research and to clarify the mechanisms at work that potentially produce the correlations I have identified.
For the main, secondary research portion of this paper, I seek to identify how climate, vegetation, and pika foraging behavior interact to produce evident correlations between pika persistence/extirpation and various plant community features. In order to characterize this relationship, I pose three sub-questions: 1) What plant characteristics are important to pikas, and how do they influence behavior and survival? 2) How do pikas alter their local plant community? 3) How does climate (and climate change) influence pika persistence and alpine plant communities? Building off these findings, the appendix includes a preliminary investigation into the vegetative features that potentially predict pika occurrence in the Great Basin. This primary research complements the main portion of the paper as an example of how statistical analyses can be utilized to test hypotheses based on pika foraging dynamics.
Research Methods
In order to address my overall research question and subquestions, I employed secondary research methods through the evaluation of the peer-reviewed literature and personal communications with researchers in the field. The researchers I conferred with were able to direct me to pertinent journal articles and studies, as well to advise my statistical analyses featured in the appendix. I attended a professional conference where I was able to view presentations on the latest research, participate in working groups to discuss and address key issues related to pika conservation, and meet with some of the researchers cited in this paper. In particular, I learned about the research conducted by Wickhem (2016), which utilized cafeteria-style experiments to assess pika foraging preferences. This study emphasized previous findings related to the importance of Plant Secondary Metabolites to pika foraging behavior, and helped guide
Page 10 of 62 my further research. Personal communications with Erik Beever, Ph.D., cited extensively in this paper, provided valuable perspective that allowed me to recognize the often variable and sometimes contradictory findings of many studies related to climatic impacts on the pika across its range. Through synthesis and integration of the secondary literature, I identify common themes and provide evidence to characterize the relationship between pika foraging behavior, climate, and plant community composition and structure.
Results
What plant characteristics are important to pikas, and how do they influence behavior and survival?
Foraging Behavior Unlike many montane mammals, the pika does not hibernate, and instead stores plants in haypiles, upon which it feeds throughout the course of the winter. The American pika is a generalist herbivore, capable of foraging upon a broad range of local vegetation depending on relative availability and accessibility, but its complex foraging behavior and phenology complicates its nutritional requirements. Despite being a dietary generalist, the pika actively selects plants based on quality rather than prevalence or abundance (Smith and Erb 2013). The pika largely relies upon metabolic water from plants for hydration and preferentially collects and stores plants for winter based on specific nutritional, chemical, and structural characteristics (Huntly et al. 1986, Dearing 1997), prompting some researchers to ironically label it a “selective generalist” (Kristina Ernest, Ph.D., personal communication, February 7, 2017). Pikas have exceptionally high metabolic demands, especially at high altitudes, and the availability of adequate nutrients and water could limit fitness and survival (Sheafor 2003, Erb et al. 2014). Selectivity is expected to be enhanced in areas of extreme seasonality and relatively high ambient temperatures (Moyer Horner et al. 2016), such as the isolated mountain ranges of the Great Basin. The availability of high quality forage, dependent upon local
Page 11 of 62 plant community composition and structure, may very well mediate pika persistence in these harsh environments.
Grazing and haying behavior serve separate purposes for the pika, and limitations to either behavior, either via environmental constraints or plant availability, have distinct consequences on fitness. Grazing sustains continuous metabolic needs and daily activity, while the sole purpose of haying is for winter survival and to ensure adequate fitness for spring mating and reproduction (Huntly et al. 1987, Dearing 1997a). Importantly pikas graze throughout the year but only hay during the summer and early fall months, coinciding with peak vegetative biomass (Huntly et al. 1987). Therefore, haying, and thus winter survival and spring fitness, is constrained by the timing and duration of the growing season, as well as by extreme summer heat, which limits the amount of time spent foraging each day (Stafl and O’Connor 2015). In addition, pikas use different parts of plants when grazing versus haying and prefer to cache plants high in secondary chemical compounds that help preserve them through the winter months (Dearing 1997), making plant chemical composition especially important to haypile production.
In agreement with Central Place Foraging Theory, which attempts to explain how an organism maximizes foraging efficiency by balancing risks and costs with energy won, pika foraging behavior is heavily influenced by predation risk and environmental conditions, just as it is also influenced by selectivity for specific plant characteristics (Huntly et al. 1985, 1986). Pika foraging is concentrated around the talus and decreases with distance, while forage selectivity becomes more focused further away from the talus, suggesting the influence of predation risk and energy budgeting (Huntly et al. 1987, Holmes 1991). Females venture further from the talus when lactating compared to when pregnant, as their priorities shift from predator avoidance when carrying young to maximization of food when nursing (Holmes et al. 1991). The phenological timing of plant growth and the availability of high quality forage may be most important during pregnancy when mothers cannot risk exposing themselves for extended durations. Pikas are positively correlated with sites of high visibility for predator surveillance (i.e.,
Page 12 of 62 negative correlation between pika persistence and overall vegetation cover, foliar cover, and relative tree cover), as vegetation structure can inhibit their ability to safely forage (Wilkening 2007, Moyer-Horner et al. 2016). Human disturbance can also disrupt foraging behavior, as pikas respond to hikers with antipredator behaviors by reducing foraging time (Stafl and O’Connor 2015). Trail traffic could be especially deleterious to pika winter survival and spring fitness during summer and early fall, when pikas are actively collecting for their haypiles. Similarly, pikas reduce their foraging time at higher ambient temperatures, which can be particularly limiting to vital summer haying activities, especially as the climate continues to warm (Stafl and O’Connor 2015). Pika foraging selectivity can be highly site-specific and variable in response to environmental heterogeneity (Smith and Erb 2013). Understanding the external factors that influence foraging behavior is essential to realistically characterize the relationship between plant community composition and structure and pika persistence.
Considering the complexity of the pika’s foraging behavior and phenological requirements, combined with the extreme seasonality and unforgiving conditions of the pika’s high-elevation habitat, metrics of forage quality may be especially important in buffering or facilitating environmental stressors, and could improve efforts to model pika distribution and to identify important refugia. As central place foragers, pikas do not venture far beyond the talus in search of food and are thus limited by the abundance, variety, and quality of available local forage plants (Huntly et al. 1985, 1986). Forage quality can be best quantified by considering the relative importance of 1) plant nutritional components, 2) Plant Secondary Metabolites (PSM), and 3) plant morphology.
Nutritional Components Metabolic water content The metabolic water content of local vegetation may be most important to pika persistence at sites where climate is drier and warmer, especially at lower elevations and during periods of drought. Smith and Erb (2013) demonstrated that, while selection for plants with high water content negatively correlates with elevation (i.e., selectivity is
Page 13 of 62 higher at lower elevations) in the southern Rocky Mountains, the water content of commonly available vegetation does not correlate across the same elevation gradient, indicating that pikas do not select for water content based upon differences in available forage but rather are likely responding to differences in climate and free water availability at different elevations. One metric of water balance, annual evapotranspiration, has been shown to be a strong predictor of pika persistence in the Great Basin; however, it can be mediated by regional and local environmental variables, such as temperature, water inputs (i.e., precipitation), and soil characteristics, which makes its influence on vegetation quality and pika persistence difficult to interpret (Beever et al. 2016a).
Protein and Nitrogen Content Another important nutritional component of forage plants consumed by pikas can be defined in terms of digestible protein or digestible nitrogen (Wickhem 2016). High protein diets can increase reproduction rates and improve overall fitness in mammals (Smith 1988). Similarly, diets high in digestible nitrogen can improve growth rates in offspring and increase reproduction rates (DeGabriel et al. 2009). In order to quantify the protein content of a plant, scientists often measure concentrations of leaf nitrogen, which makes up amino acids, the building blocks of protein, and thus can serve as a proxy for protein content (Wickhem 2016). However, tannins in consumed forage can actually bind to protein and reduce its availability for digestion (Robbins et al. 1987). This defense mechanism against herbivory by which tannins reduce the digestible protein content in plants confounds the assessment of what constitutes ‘high quality’ forage for a species like the pika that actively selects for plants containing tannins in order to help preserve its winter haypile.
Pikas have been shown to preferentially collect and store plant species with higher crude protein content (Millar and Zwickel 1972). Considering nitrogen a metric of protein content, and so of forage quality, Smith and Erb (2013) found that selectivity for nitrogen increases for pika populations with low-quality vegetation and decreases for pika populations with high quality vegetation, suggesting pikas balance the energetic costs of
Page 14 of 62 haying by increasing selectivity for higher-energy food when it is less available. Similarly, pika selectivity for nitrogen increases at sites with higher average summer temperatures, allowing the pika to reduce its exposure to heat stress by spending less time foraging – focusing on quality over quantity for cached items. However, high- nitrogen foods may be more important for the pika’s summer diet than for the winter haypile, as more focus is given to secondary chemistry when selecting for the winter diet (Dearing 1996).
Plant Secondary Metabolites Due to the unique foraging behavior and dietary requirements of a non-hibernating alpine mammal, the driver of the pika’s haypile preferences and selective caching may be the most critical indicator of forage quality. Plant Secondary Metabolites (PSMs), a key adaptation of many plants in defense against herbivory, which can produce negative effects ranging from reduced digestibility of vital nutrients to toxicity, appear to be a dominant driver of haypile selectivity in both the American pika and the Siberian pika (Dearing 1996, 1997a, 1997b, Gliwicz et al. 2006). Though classifications vary, the three major types of PSMs include alkaloids, terpenes, and phenolics. Strikingly, the concentration of phenolics, the most common class of PSMs, found in all angiosperms (Wickhem 2016), in cached plants is three to six times higher than that of plants consumed during summer (Dearing 1996, 1997). Somewhat counterintuitively, pikas actually prefer plants with high concentrations of PSMs for their haypiles, as they can provide the dual advantage of preserving plant material through the winter and delaying consumption until the compounds have degraded sufficiently to make the plant palatable (Dearing 1997b). Phenolics and terpenes possess antifungal and antimicrobial properties that resist decomposition (Dearing 1996). The preservative qualities of PSMs help to maximize the biomass and nutritional content of the haypile during winter and early spring when forage availability is highly limited, allowing for approximately 70 more days of food than if it were comprised of plants typical of the summer diet (Dearing 1997b). By early spring, the concentration of secondary compounds in the haypile becomes as low as in summer forage, just in time for the crucial period of mating and reproduction when proper diet and fitness are essential. The unpalatability of tannins (a
Page 15 of 62 common form of phenolic) and their associated decreased digestibility of proteins and carbohydrates is reduced by the drying of the plant material, and terpenes lose their harmful volatiles following harvest, allowing pikas to utilize plant resources that were previously unavailable for consumption (Gliwicz et al. 2006, Wickhem 2016). In fact, pikas are able to monitor the concentration of secondary compounds in the vegetation, testing the palatability of the plants until concentrations are acceptable for consumption (Dearing 1997b). Rather than developing chemical-specific, physiological adaptations, the generalist pika is able to overcome a variety of plant chemical defenses through simple behavioral modifications (Dearing 1996). This preference for PSMs allows pikas to circumvent extreme seasonal changes in forage availability and climate in their harsh, high-elevation habitat, potentially indicating a significant link between metrics of forage quality and persistence.
In a recent study, in which ten plant species commonly present in pika habitats were offered to pikas through a series of cafeteria-style experiments, Wickhem (2016) found alkaloid and tannin content to be the top drivers of pika foraging preference. Of the plants tested, the top species included Douglas fir (Pseudotsuga menziesii), Sitka alder (Alnus viridis), willow (Salix spp.), and black cottonwood (Populus balsamifera trichocarpa). Interestingly, pikas preferred plants with either high concentrations of tannins or alkaloids, but not both, potentially in response to an interaction between the two compounds (Figure 3). Protein and water content did not appear to be strong drivers of pika foraging preference, further supporting the hypothesis that PSMs dictate summer caching behavior and winter diet (Dearing 1997b). Incorporating a variety of PSMs from different plant species may help prevent a single detoxification pathway from becoming overloaded (Freeland and Janzen 1974). Understanding the relative levels and combinations of PSMs present in a given plant community may help characterize forage quality and inform restoration approaches.
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Figure 3. Pika foraging preference for tannins is negatively associated with alkaloid concentration, suggesting pikas prefer one or the other secondary compound. (Wickhem 2016).
Plant Morphology and Structure Plant morphology does correspond with pika foraging preferences, but morphological bias is not consistent across the pika’s range and may not be as influential or useful of a predictor as nutritional or secondary chemical content. According to Central Place Foraging Theory, which highlights how organisms maximize foraging rates and efficiency when venturing from a home base (e.g., talus patch), pikas should preferentially collect larger plant species for their winter haypiles in order to reduce the time and energy spent foraging. In Alberta, Millar and Zwickel (1972) concluded that pikas preferentially harvest shrubs and clumped herbs in order to maximize the amount of cached plant material for minimal effort. Similarly, Huntly et al. (1986) found that pikas preferentially cache tall bunch grasses over shorter graminoids, forb flowering stalks over forb leaves, and more woody plants compared to its summer grazing diet (Huntly et al. 1986). However, both of these studies occurred before Dearing (1996) first provided evidence of pika selectivity based on Plant Secondary Metabolites (PSMs), and neither study considered the role of secondary chemistry in defining the observed
Page 17 of 62 foraging preferences. The generally higher concentrations of secondary compounds in forbs and woody plants compared to graminoids could partly account for these observed relationships. While mean forb height positively correlates with short-term pika abundance (defined as the number of occupants per pika home range) in Glacier National Park, this could just as well reflect local microclimate (i.e., mesic habitat) or foraging patterns (i.e., late harvest of forbs in response to the extreme seasonality and relatively high summer temperatures of the park) and may not represent convincing evidence of forage quality (in this case, defined by plant morphology) driving pika abundance (Moyer-Horner et al. 2016). Looking to other species of Ochotona fails to offer any further clarity on the matter; collared pikas (Ochotona collaris) in the Yukon Territory actively select plant species with larger leaf sizes for their haypiles (Hudson et al. 2008), while the Siberian northern pika (Ochotona hyperborea) does not appear to have a clear preference for certain plant morphologies (Gliwicz et al. 2006). Although the size of plants and plant structures may contribute to pika forage selection, the tendency of plant morphology to reflect other factors, from nutritional and chemical components to environmental conditions and herbivory pressure, makes it unreliable at best as a predictor of foraging preferences.
In addition to the forage implications of plant morphology, vegetation structure is an important habitat characteristic that may influence foraging behavior and survival. Dense canopy cover may obstruct visibility and impair the pika’s ability to surveil the talus, a vital behavior by which pikas maintain their territories and avoid predators (Tyser 1980, Wilkening 2007). Trees can serve as perches for avian predators, which would enhance the threat of predation. The persistence of pygmy rabbit (Brachylagus idahoensis) populations in the Great Basin has been negatively associated with pinyon and juniper encroachment, as these trees gradually reduce the understory and provide perches for predators (Larrucea 2007). The height of forbs, which has been positively associated with pika abundance, can indicate shade for foraging pikas, reducing heat stress and allowing for prolonged activity during the crucial haying period of summer and early fall (Moyer-Horner et al. 2016). Further research on the influence of trees and plant community structure on pika persistence via alteration of microclimate and
Page 18 of 62 predator dynamics is needed to clarify the importance of these predictors in the context of other, potentially collinear, variables.
Place-based Foraging Behavior Despite general patterns in dietary preferences, pika forage selection appears to be highly site-dependent (Hudson et al. 2008). Microclimate and local plant phenology play important roles in determining pika foraging behavior and preference. While selectivity for high-nitrogen plants relates to both the availability of nitrogen within the local plant community and abiotic environmental factors, the selectivity for water content appears to be solely based upon abiotic environmental factors (Smith and Erb 2013). Pika preference for specific plant nutritional qualities may be location-specific and heterogeneous across its range, depending upon local plant community composition and environmental conditions. Further, summer and winter dietary preferences can vary between locations. While pikas avoid caching lichens and evergreen cushion plants, such as mosses, they still frequently graze them during spring and presumably during winter as a haypile-supplement (Millar and Zwickel 1972, Conner 1983, Gliwicz et al. 2006). In warmer, drier areas where haypiles are less advantageous, pikas take this a step further and shift their diet to become much more reliant on cushion plants (Varner and Dearing 2014). Even when experimentally presented with harvested cushion plants, pikas still avoid incorporating them into haypiles, suggesting they do not avoid the cushion plant because of the difficulty and high-energy cost of harvesting a matted plant (Dearing 1996). Instead, pikas may instinctually avoid caching plants that are available throughout winter and spring (Hudson et al. 2008). This careful budgeting of resources based upon seasonal availability may be most beneficial in high-elevation, montane habitats forage resources can be restricted by extreme seasonality (Gliwicz et al. 2006). Local plant phenology in relation to seasonal microclimate may outweigh the importance of plant secondary chemistry to pika persistence in some areas, and could be especially important in mediating the effects of a changing climate.
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How do pikas alter their local plant community?
The interpretation of the seeming significance of plant community composition and structure to pika persistence is complicated by the effects that the pika has on its local plant community. In other words, does vegetation actually mediate pika persistence, or does the pika mediate the plant community, giving rise to spurious correlations?
Pika foraging pressure can confound modeling efforts but does not contradict importance of forage quality. Well understood mechanisms of foraging pressure, including lessons offered by Central Place Foraging Theory, can be compared against established vegetative predictors of pika occupancy and persistence in order to assess the relative role that foraging behavior plays in creating these linkages. Central Place Foraging Theory correctly predicts that an increasing gradient of plant abundance and species richness follows a declining gradient of grazing pressure away from the home base – in this case, the talus (Huntly et al. 1986) (Figure 4). Concentration of foraging near the talus results in a local decline in biomass and plant species richness (Huntly 1985), which disagrees with the positive relationship between pika occupancy and vegetation species richness (Varner et al. 2015), suggesting forage quality is a more consequential predictor than foraging pressure. Similarly, while pika foraging selectivity tends to cause an increase in plants of lower calorie and protein content (Huntly 1985), pika occupation and persistence are positively associated with relative forb cover compared to graminoids (Wilkening 2007, Erb et al. 2014, Ray et al. 2016), despite forbs generally having higher energy and protein value than graminoids (Holechek 1984). Heightened selectivity in areas of extreme seasonality may cause pikas to graze more graminoids and delay forb collection until late in the season, resulting in a greater forb-to-graminoid ratio and taller forbs, both of which have been shown to be strong predictors of pika occupancy and abundance (Moyer-Horner et al. 2016). A comparable argument could be made regarding the negative relationship between pika persistence and total vegetation cover, foliar cover, and relative tree cover (Wilkening 2007). Pika foraging pressure can suppress vegetation and biomass (Huntly 1986), which could explain the negative correlation. However, the pika’s tendency to remove, but not
Page 20 of 62 consume, obstructive vegetation in areas of dense cover (Markham and Whicker 1973) – a behavior that has been shown to improve predator avoidance in other small mammals (Hansen and Gold 1977) – suggests that the negative relationship between canopy cover and pika presence may actually reflect a plant-to-pika effect rather than the other way around. Gradated plant community transformations caused by intense foraging pressure, as well as the pika’s ability to actively engineer its habitat to promote its own survival, complicates efforts to model pika-vegetation relationships and must be considered when developing hypotheses and evaluating results.
Figure 4. Change in vegetation cover and vegetation grazed by pikas in relation to distance from talus patch. (Huntly et al. 1986)
How does climate (and climate change) influence pika persistence and alpine plant communities?
What has (pre)history shown us? The paleontological record indicates that the American pika has experienced significant range expansions and contractions over previous millennia, largely in response to
Page 21 of 62 glacial and interglacial cycles. Near the end of the Pleistocene epoch (c. 12,000 radiocarbon years ago), pika populations existed at much lower elevations – about 1750 m on average – than at present and did not exclusively utilize talus habitat (Grayson 2006). The cooler conditions of the Pleistocene epoch facilitated gene flow between different high elevation pika populations, promoting a regional genetic cohesion that still characterizes pika lineages today (Galbreath et al. 2009). Since the last glacial maximum of the late Wisconsinan (c. 40,000-10,000 radiocarbon years ago), the average elevation of pika populations in the Great Basin has risen by 783 m (Figure 5), and the distance between now-extirpated populations and currently extant populations declined dramatically as the range contracted around the high elevation mountain ranges that transect the xeric valleys (Grayson 2005) (Figure 6). Low-elevation populations were extirpated from most of the Great Basin by or during the mid- Holocene, a period marked a warm period known as the climatic optimum (Grayson 2000). Losses were most severe in the southern Great Basin and along the Utah- Nevada border, where conditions became too hot and dry to support viable pika populations (Grayson 2006). These rapid distributional shifts and extirpations in response to Holocene warming have produced considerable demographic decline across all five genetic lineages of pika (Figure 7) since the Last Glacial Maximum; the potential for further demographic retraction, population fragmentation, and even lineage extinction may threaten the pika’s ability to cope with continued warming (Galbreath et al. 2009). Comparable demographic impacts caused by postglacial warming can provide valuable insight into the trajectory of pika populations in the future, though the unprecedented rate of contemporary climate change and associated range contraction elicit considerable uncertainty and concern.
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Figure 5. Rise in elevation of pikas in the Great Basin since the late Wisconsinan. (Grayson 2005)
Figure 6. Extirpations and range retraction across the Great Basin since the late Winsconsinan. Closed circles indicate prehistorically occupied (and now extirpated) sites. Open circles with crosses indicate historically occupied (and now extirpated) sites. Open circles indicate currently extant sites. The gray dotted line indicates the boundary of the hydrographic Great Basin. (Grayson 2005) Page 23 of 62
Figure 7. Major mitochondrial DNA lineages of the American pika. The broken line represents the approximate southern extent of the continental ice sheet during the LGM. The numbers indicate sampling locations. (Galbreath et al. 2009)
Just as past climate change has shaped the pika’s current distribution, climate has also shaped the evolution of plant communities and the pika’s dietary niche. The evolutionary history of the pika family, Ochotonidae, and its current geographic range has been closely tied to climate and associated shifts in dominant vegetation. Ochotonids strongly prefer C3 plants, while many leporids (rabbits and hares) are able to incorporate significant amounts of C4 plants into their diet (Ge et al. 2013). Plants using the C4 metabolic pathway for carbon fixation attained their current dominant status in the late Miocene to early Pliocene (4-8 million years ago), coinciding with a decline in global ambient temperatures. C4 plants, most of which are monocots in the Poaceae family, are largely fire adapted and characterized by a high carbon-to-nitrogen ratio and low protein (Ge et al. 2012). This poorer nutritional quality, as well as the fact that not all herbivores are equally capable to digest C4 plant material, resulted in large- scale faunal shifts after the C4 expansion of the late Miocene (Osborne 2008). In
Page 24 of 62 parallel with the shift from C3 dominated plant communities to mixed C3 and C4, and C4 dominated, drove large scale extinctions and range contractions of Ochotonids, resulting in today’s single extant genus (Ochotona), which includes 28 species of pika found in talus habitats of North America and Asia (Ge et al. 2013) (Figure 8). While the current increase in atmospheric carbon dioxide is expected to promote primary production and plant biomass, it may offer a competitive advantage to C3 plants over C4 plants, with potentially positive implications for Ochotona spp.; however, the relationship between carbon dioxide levels and C3 and C4 plant community dynamics is exceptionally complex, and the associated consequences of future climate change are still poorly understood (Wand et al. 1999). The pika’s current dietary niche does not appear to have been altered by the last century of climate change, with the greatest pattern of dietary variation occurring in individuals between seasons rather than in populations across decades or latitudes (Westover 2017). The question that remains is how plant communities will shift in response to contemporary climate change, and whether pikas will have the capacity to adapt and evolve along with these vegetative transformations.
Figure 8. Changes in climate and vegetation in relation to the number of ochotonid and leporid genera from the Paleocene to the early Pleistocene. (Ge et al. 2013)
Impacts of Climate Change on Alpine Plant Communities Alpine plant communities may be some of the most impacted by climate change, as rising temperatures and increasing aridity across steep elevation gradients force
Page 25 of 62 species to either tolerate or avoid environmental stressors. The elevational distributions of many plants species are rising dramatically in response to recent climate change (Kelly and Goulden 2008). Alpine species face a greater risk of localized extinction, as they have a narrower elevation tolerance than subalpine species and species with ranges spanning lower elevations (Guisan and Theurillat 2000). Due to the conic shape of mountains, habitat area becomes reduced as species migrate higher to cope with shifting environmental conditions. Some high elevation plant communities in the western U.S. have experienced significant compositional transformations, including more bare ground and graminoids and shrubs, and fewer forbs (Zorio et al. 2016).
Forbs appear to be particularly vulnerable to climate change, and alpine plant communities may see a trend towards more xeric shrubs, with unknown consequences for the pika’s winter dietary requirements. Concerningly, climate change impacts on water balance may mediate changes in vegetation more significantly than the direct consequences of rising temperatures (Franklin et al. 2016). Based upon the severe, long-term drought that occurred across the western United States in conjunction with the Medieval Warm Period (900-1300 AD), the continued rise in temperatures can be expected to trigger a shift towards extreme, long-term aridity in the region (Cook et al. 2004). Increased warming promotes aboveground biomass (AGB) production of shrubs while reducing AGB of forbs in montane meadows, indicating a potential shift in dominant vegetation of montane plant communities (Harte and Shaw 1995). Warming may favor evergreen shrubs compared to deciduous forbs via changes in soil moisture and inhibitions to the light-capturing protein complex, photosystem II (PSII) (Loik et al. 2000).
A reduction in forb biomass may negatively impact forage quality and availability for pika haypiles. In addition, reduction in annual snowpack caused by global warming may expose overwintering perennial forbs in montane meadows to more extreme cold, potentially delaying bloom and decreasing seed production (Inouye and McGuire 1991). Low population density and altered phenology of forbs might limit haypile production and influence foraging behavior, forcing pikas to expose themselves to further heat
Page 26 of 62 stress and predation risk in order to cache sufficient plant material for winter. Though forbs are frequently cited as significant predictors of pika persistence (Rodhouse et al. 2010, Moyer-Horner et al. 2016, Ray et al. 2016), some shrub species have also proven beneficial (Ray et al. 2016). Improved understanding of the dietary preferences of pikas at the plant species level, as well as how alpine plant communities transform in response to climate change, will be necessary to inform long-term conservation strategies.
Climatic Predictors of Extirpation Explored The direct effects of specific climatic variables on pika distribution must be considered in conjunction with the indirect effects mediated through vegetation so as to distinguish the mechanisms of change and account for synergistic effects. In order to assess the full impact of climate change on species distributions, scientists have largely focused on investigating the realized niche of a species through the development of species distribution models (SDMs) (Schwalm et al. 2016). SDMs seek to estimate potential range shifts and the vulnerability of populations by assessing the relationship between occupancy and a range of biotic and abiotic variables. When a model has a good fit (i.e., the chosen predictor variables adequately explain the variation in the response variable), it can then be extrapolated to evaluate future distributions and identify the key limiting factors. The pika’s unique position as a model organism threatened by climate has spurred research focusing on developing realistic SDMs based on climatic variables in order to better understand how montane mammals react to environmental change.
Temperature Given the pika’s physiological sensitivity to extreme heat, rising temperatures have unsurprisingly been widely implicated in the observed collapse of pika populations throughout much of the species’ range. Recent studies have focused on resurveying historically occupied sites and comparing shifts in abundance, elevation, or evidence of extirpation to climatic data, such as ambient vs. sub-talus temperatures (Beever et al. 2010, 2013, 2016a). Researchers can place thermal sensors below the talus and compare temperature trends to ambient temperature derived from weather stations in
Page 27 of 62 order to hindcast temperatures and search for correlations between temperature and patterns of persistence. Testing alternative models of climate-mediated extirpations in the Great Basin, researchers found chronic heat stress and acute cold stress to be the strongest predictors of pika persistence (Beever et al. 2010). Importantly, chronic heat stress often appears to be more important than acute heat stress (Beever et al. 2013), though this is not consistent across the pika’s range. While pikas may largely be able to avoid acute heat stress through behavioral adaptations, such as seeking refuge under the talus during the hottest part of the day, the sub-lethal impacts of chronic heat stress on foraging behavior and fecundity may actually be the more important driver of extirpation (Beever et al. 2010). Chronic heat stress may be more influenced by climate change, given that minimum temperatures increased several times more than maximum temperatures during the 20th century (Beever et al. 2011), a trend that may become more critical as temperatures continue to rise.
Projections of further warming suggest a dramatic decline in habitat for the pika across its range. While average global temperatures are predicted to increase by 2.4-6.4°C by the year 2100, a 4°C increase is expected to reduce suitable habitat for the 31 traditional American pika subspecies (which, through genetic analyses, have now been synonymized into five distinct lineages) by, on average, 73% across their range (Calkins et al. 2012) (Figure 2). Further, a 7°C increase could cause 19 of the 31 pika subspecies to lose more than 98% of their habitat. The consequences of high elevation warming are not restricted to the pika, as a scenario of warming by 3°C could cause more than 20% of high-elevation small mammals in the Great Basin to go extinct (McDonald and Brown 1992).
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Figure 2. Reduction in pika habitat under different scenarios of warming. (Calkins et al. 2012)
Importantly, the impacts of temperature are not consistent across the pika’s range. While average temperature has been strongly correlated with pika persistence in the Great Basin and northern Utah, it was outperformed by habitat area as a predictor variable in northeastern California, reflecting the heterogeneous and place-based relative importance of different climatic impacts (Beever et al. 2016a). The presence of pikas in atypically warm habitat, such as at Craters of the Moon National Monument where maximum July temperatures regularly exceed the pika’s upper physiological temperature threshold, further suggests that temperature is not consistently or definitely the most important limiting factor at work across their range (Rodhouse et al. 2010). The interactive effects of temperature with other environmental factors, as well as the pika’s significant adaptive capacity, require a place-based perspective, despite the temptation to charge temperature as the “smoking gun” driving extirpations.
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Snowpack One of the most surprising relationships linking climate and pika persistence is that of acute and chronic cold stress and snowpack. While most research has focused upon the effects of rising temperatures in relation to the pika’s upper physiological tolerance for heat, cold stress also appears to be a growing concern in relation to climate change. Since pikas are so small (i.e., high surface-to-volume ratio leads to rapid loss of heat) and do not hibernate (i.e., faster metabolism enhances heat loss), they rely on the snowpack for insulation from the coldest winter temperatures (Beever et al. 2010). The mountain snowpack has displayed a declining trend since the mid-20th century, exposing pikas to increasingly extreme cold. Consistent exposure of pikas to lower temperature thresholds (-5°C and -10°C), as well as to their upper physiological thresholds, can strongly predict pika extirpation risk (Beever et al. 2011)
Possible ways in which snowpack, commonly measured as the snow-water equivalent (SWE), or the theoretical depth of water if the snowpack was melted, may influence pika persistence include: 1) mediating the number of days in which pikas are exposed to c vhnb of insulation, and 2) controlling how far into the year that freshwater would be available (Beever et al. 2013). Maximum SWE has been demonstrated as an excellent indicator of pika density in contemporary surveys, with a strong link between number of acutely cold days and pika extirpations. The synergistic relationship between SWE, growing-season precipitation, and average temperature suggests potential indirect mechanisms of climatic influence, reinforced by the strong correlation between relative pika density and total aboveground gross annual productivity (Beever et al. 2013).
Hydrology In combination with temperature, hydrologic variables – including metrics of precipitation, evapotranspiration, humidity, and water balance – have been implicated as determinants of pika persistence and extirpation across much of its range. In the Southern Rocky Mountains, annual precipitation is an important limiting factor of pika persistence, which contributed to the extirpation of several populations within the region during the last few decades (Erb et al. 2011). Extirpations in this region, though
Page 30 of 62 relatively few compared to other parts of the pika’s range (e.g., the Great Basin), have only been documented in areas that were consistently dry throughout the 20th century. It can be difficult to confidently identify evidence of climate change impacts, particularly for precipitation, which is far more variable and difficult to predict than temperature, but the relationship between low precipitation and pika extirpations in this region helps to inform future management through prioritization of conservation efforts in areas of extended drought.
To evaluate the impacts of hydrology on pika persistence, it is important to consider biologically relevant ‘ecohydrological variables,’ such as actual evapotranspiration, SWE, growing-season precipitation, and climatic water-deficit. Together, these variables reflect the climatic water balance in an ecologically relevant context. Drought results from an imbalance between water inputs (measured as precipitation) and water demand (measured as evapotranspiration, or the amount of water transpired through vegetation and evaporated from the soil), and can stress pikas directly (i.e., via the lack of available drinking water) or indirectly (i.e., via reduced primary productivity and available forage). In fact, ecosystem productivity and plant population dynamics have been shown to be highly sensitive to changes in water balance, and the impact of climate change on water balance could be even more consequential for vegetation than the direct effects of rising temperatures (Franklin et al. 2016). When assessing the impacts of water imbalance on a system, it is important to distinguish between potential evavotranspiration (PE) and actual evapotranspiration (AE); whereas PE represents the maximum amount of water that could be evapotranspired given adequate water inputs and is used to represent the water demand of a system, AE represents the actual amount of water transpired given the limited inputs (NOAA National Centers for Environmental Information). Therefore, AE is always equal to or less than PE, and can reflect the degree of water stress in a system. In the Great Basin, annual evapotranspiration, calculated as the sum of the monthly actual evapotranspiration, was found to be the strongest predictor of pika occupancy in an assessment of multiple competing models based on a range of climatic variables (Beever et al. 2016a). Annual actual evapotranspiration is regularly mediated by precipitation, temperature, and soil moisture storage, and can offer a more realistic,
Page 31 of 62 ecologically meaningful measure of water balance than annual precipitation. Similarly, maximum snow-water equivalent and average growing-season precipitation more strongly predict pika population size than average annual precipitation, as they more precisely influence water and forage availability in relation to the phenological patterns of the pika (Beever et al. 2013). The relationship between water balance and pika persistence and extirpation may be especially pronounced in the driest, hottest reaches of the pika’s range and where severe droughts may occur.
Fire Regime Given the evident relationship between pika occurrence and environmental variables like heat, dryness, and plant community composition and structure, one might expect fire disturbance to have huge consequences for pika survival and fecundity. While limited research has been conducted to evaluate the potential impacts of increased fire severity and frequency on montane mammals, Varner et al. (2015) had the unique opportunity to study these impacts after their pika monitoring project at Mt. Hood was interrupted by wildfire at the study location. Thermal sensors had been placed at the talus surface and interstices in order to compare microclimate and thermoregulatory behavior with other, already surveyed sites at nearby low elevations. One week after placing the sensors, a nearby lightning strike ignited a wildfire that would burn 2430 hectares over the course of twenty-two days, impacting four of the nine previously surveyed sites and two of the three new sites with thermal sensors. The researchers seized this opportunity to analyze the data from the thermal sensors and conduct subsequent survey monitoring of the locations in order to look for potential relationships between pika occupancy and abundance and different metrics of fire severity. Resulting statistical analyses demonstrated a surprisingly muted importance of the burn severity indices in predicting pika density in the burned areas (Varner et al. 2015). On the contrary, indices of vegetation and habitat structure strongly explained patterns of density. The apparent quick recovery of vegetation at burned sites facilitated the persistence and widespread distribution of pikas in the area. Moss, a component of the highest-weighted model, can serve as a persistent and abundant food source for the pika when other plants are limited, and can also allow pikas to avoid venturing out from
Page 32 of 62 the stable microclimate of the talus to forage. Thermal sensors placed within the talus showed that the temperature in talus interstices never exceeded 19°C, demonstrating the importance of talus as a thermal refuge for small animals during and after fire disturbance (Varner et al. 2015). The resilience and behavioral adaptability displayed by the pika, as well as the buffering capacity of an atypical forage source, in the face of fire disturbance emphasizes the need for further, species-specific study of biotic response to altered fire regimes.
Heterogeneity and Nuance of Climate Impacts As evidence continues to accumulate associating rapid distributional losses of the pika, including upslope retractions and local extirpations, with climate change, a unifying theme has emerged in the scientific literature – that of the heterogeneity and nuance with which climate acts upon a species’ range (Jeffress et al. 2013, Beever et al. 2016a, Schwalm et al. 2016). The importance of different climatic variables in determining pika persistence and extirpation is not consistent across the pika’s range. In some areas, pikas appear to have a wider tolerance for climatic stress, and factors of habitat quality seem to be the most important determinants of pika distribution. Rock-ice feature till functions as an important landform refuge in warmer conditions of the southwestern U.S., allowing pikas to tolerate a wider range of elevation, temperature, and average precipitation conditions than expected (Millar and Westfall 2010). In fact, habitat composition and connectivity can be even more important than climatic variables in modeling pika occurrence (Schwalm et al. 2016). However, sites where pikas have been extirpated do display significantly higher average maximum temperatures, suggesting a potential limit to either the adaptive capacity of the species or to the buffering capacity of certain habitat features.
The variability in importance of climate and other predictors of pika distribution can be readily distinguished when comparing models across different regions of the pika’s range. Under Island Biogeography Theory, the Sierra-Cascade extent of the pika’s range in northeastern California could be considered a ‘mainland’ habitat, while the isolated mountains of the Great Basin and nearby Zion National Park and Cedar Breaks
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National Monument in northern Utah represent ‘island’ habitat. Species richness in ‘island’ habitats, a subset of the species richness found in ‘mainland’ habitats, reflects the balance between extinction and colonization rates, which in turn are mediated by habitat area and magnitude of isolation (Beever et al. 2016a). Localized extinctions should theoretically be more extensive in montane ‘island’ habitats due to the smaller habitat area and population size (i.e., genetic pool), as well as the narrower elevation gradients compared to the ‘mainland.’ As predicted by Island Biogeography Theory, localized pika extirpations are far more severe in the Great Basin and northern Utah compared to northeastern California (Beever et al. 2016a). Interestingly, metrics of water balance and mean temperature strongly predict pika occupancy in the two ‘island’ regions, but habitat area outperforms these variables in the ‘mainland’ region, further suggesting the reduced limitations imposed by climatic stressors in areas of substantial, ecologically-connected habitat.
The heterogeneity and nuance of climate impacts can be distinguished by comparing models at different scales, as well. At macroecological scales, impacts of climate on pika distribution appear unequivocal (Beever et al. 2010, 2013, 2016a). At the local level, however, pika occurrence varies widely across bioclimatic gradients (Jeffress et al. 2013). Local-scale differences in the realized niche of the pika makes the relative importance of various predictor variables highly heterogeneous across the species' range; therefore, a place-based approach is important in modeling pika distribution and density. In addition, the interactions between climatic variables can often mediate their relative influence on pika populations. In a study of the impacts of a suite of climatic factors on local patterns of pika distribution across bioclimatic gradients in eight U.S. National Parks, precipitation alone was not found to be a strong predictor, but heat stress performed better in the driest parks, suggesting an interaction between the magnitude of temperature effects and position along precipitation gradients (Jeffress et al 2013).
In addition to the spatial heterogeneity of climate’s importance, the primary drivers of extirpations appear to be changing over time, with elevation best explaining historical
Page 34 of 62 extirpations and metrics of temperature best explaining recent extirpations in the Great Basin (Beever et al. 2011). However, the magnitude and rate of contemporary climatic changes do not appear to be significant drivers of extirpation compared to the long- term, microclimatic conditions at extirpated sites (Erb et al. 2011). Though a clear signal implicating rapid change as the cause of extirpation has not yet been identified, the clear importance of microclimate (particularly temperature and water balance) suggests limiting effects posed by future climate change.
Mechanisms of Climate-driven Extirpation Despite mounting support for climate as a primary driver of recent distributional shifts of the American pika, the precise mechanisms of fatality and extirpations are still poorly understood, as well as how these mechanisms will respond to a changing climate. Climate may impact pika persistence in a number of ways, including through transformations of available forage, shifting timing of forage and water availability, reduced ability to forage and reproduce due to chronic stress, and acute stress like hyperthermia. However, food resource decline has been cited as the most common mechanism through which contemporary climate change has caused extirpations (Cahill et al. 2013). Adult survival rate of the collared pika (Ochotona collaris) in the Ruby Range of western Canada has been positively linked to effects of the Pacific Decadal Oscillation (PDO), which tends to result in below-average snowpack and earlier timing of spring snowmelt in that region, suggesting the importance of plant phenology and forage availability (Morrison and Hik 2007). An earlier and longer growing season would allow more time to collect vegetation for haypiles and could lead to improved fitness during the spring breeding season and the climatically stressful summer. Conversely, a declining snowpack could result in advanced exposure to acute and chronic cold stress during the winter, reducing survival rate (Beever et al. 2010, 2011). Climatic conditions have also been linked to reproduction rates of O. princeps, as reproduction may be significantly reduced during periods of extreme weather (Millar 1974). Pika foraging behavior is closely mediated by temperature, as time spent foraging by O. princeps decreases by 3% for ever 1°C increase in average daily temperature (Stafl and O’Connor 2015). Potentially, rising temperatures could produce extirpations by limiting
Page 35 of 62 foraging and haying time, causing a reduction in fitness that might be exacerbated by alternative mechanisms like cold stress. One might expect the benefits of an extended growing season to be most offset by chronic heat and cold stress in trailing edges of the pika’s range where conditions are most hot and arid, such as in the Great Basin.
Discussion
The relationship between climate, local plant community composition and structure, and pika distribution is exceptionally complex and place-based, highlighting the idiosyncrasies of alpine ecosystems. Climatic influence on pika persistence is heterogenous across its range, though metrics of heat stress, cold stress, and water budget appear to explain recent shifts in distribution (Jeffress et al. 2013, Beever et al. 2016a). Pika foraging behavior, as well as forage availability, are, in turn, influenced by microclimate and cyclic weather patterns (Smith and Erb 2013, Gliwicz et al. 2006). The accelerated warming and drying of the climate in western North America that is expected to occur as a result of climate change may further stress pikas and limit the quality of their diet (Beever et al. 2013, Stafl and O’Connor 2015), putting their demonstrated adaptive capacity to the test. Further research into the direct and indirect mechanisms by which climate induces fatality and extirpations is necessary to elucidate the relative role of vegetation.
Climate and Forage Tightly Linked In order to characterize the relationship between climate, vegetation, and pika occurence, and to evaluate the significance of forage quality in predicting pika persistence, I considered the three general explanations for apparent correlations between various vegetative metrics and pika occurrence: 1) quality of available forage is important for pika persistence, 2) pikas shape the composition and structure of the local plant community and so the perceived relationship merely reflects correlation rather than causation, and 3) microclimate is the true driver affecting pikas and plants simultaneously (Wilkening et al. 2011, Ray et al. 2016). In regards to the second
Page 36 of 62 explanation, although pika foraging pressure can confound modeling efforts and should be considered when interpreting results, it is likely not as significant as the effects of climate or forage quality in determining persistence patterns. Positive associations with forb cover and plant species richness (Wilkening 2007, Erb et al. 2014, Varner et al. 2015) contradict expectations that pika selective foraging would promote a less diverse local plant community dominated by graminoids and plants of poor nutritional quality (Huntly 1985). However, the pika’s dynamic dietary niche across seasons (Westover 2017) suggest that the complex relationship between microclimate, foraging behavior, and forage availability – a combination of the first and third explanation – may, in fact, have significant implications for pika persistence in the face of environmental change.
Conditional Importance of Plant Secondary Chemistry Despite being generalist herbivores, pikas commonly exhibit selective foraging behavior in order to capitalize on available plant resources and ensure fitness and survival. Pikas select for Plant Secondary Metabolites (PSMs), nutritional composition (e.g., nitrogen and digestible protein), water content, and structural characteristics that facilitate efficient collection (Dearing 1997a, 1997b, Gliwicz et al. 2006). PSMs appear to be the most important driver of winter diet composition, while nutritional composition is more predictive of summer diet (Dearing o91996). Winter diet quality is highly important to winter survival and to fitness for the spring breeding season, especially in high elevation areas where seasonality is extreme (i.e., hot, dry summers and freezing winters), as summer heat stress can limit vital caching time and harsh winters can limit forage availability and cause cold stress (Wilkening 2011, Beever et al. 2016a). PSMs ensure adequate food storage and allow pikas to utilize plant resources that would be otherwise unavailable (Gliwicz et al. 2006, Wickhem 2016). However, this selectivity is largely influenced by other environmental factors, including microclimate and local seasonality, and can vary dramatically between regions and populations. Pikas display impressive adaptive capacity, able to shift their diets to evergreen, persistent resources like moss in order to tolerate atypical, low elevation habitats where haypiles are less essential and summer heat is more limiting (Varner et al. 2016). Understanding the limits of pika adaptive capacity may inform efforts to gauge pika response to future climate change.
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Interactive Effects of Climate on Forage Selectivity and Availability Pikas become more selective and reliant on metrics of high quality forage (i.e., PSMs, metabolic water content, and digestible protein) as an adaptive response to dynamic climatic stressors; however, these same stressors threaten to transform alpine plant communities, making them less appealing and beneficial to pikas. The importance of forage quality is spatially variable relative to local forage availability and environmental constraints on foraging behavior and fitness, adding a layer of complexity to the heterogeneity of climatic limitations on pika distribution (Smith and Erb 2013). Pikas prefer plants with high water content at low elevations where heat and aridity are more limiting, just as temperature is a stronger predictor of pika occurrence when coupled with aridity (Smith and Erb 2013, Jeffress et al. 2013). Concerningly, climate change is expected to transform montane plant communities, resulting in drier, warmer, habitats favoring xeric shrubs and grasses and discouraging PSM-rich forbs (Inouye and McGuire 1991, Franklin et al. 2016). The interactive effects of climatic variables with foraging preferences and dietary requirements constitute indirect mechanisms by which climate may mediate pika persistence through a simultaneous increased demand and reduced availability of high quality forage. Understanding the specific plant community composition and structure that benefit pikas at the local level can help prioritize areas for conservation and inform restoration efforts.
Lessons from an Indicator Species As an indicator species, the pika offers valuable insight into the mechanisms of biological response to climate change and reflects pervasive challenges faced by a range of montane mammals. Marmots, large squirrels common at high elevations, face similar threats from climate change, as water availability impacts survival and fecundity and reduced snowpack induces further cold stress in the winter months (Armitage 2013). Just as tree cover negatively correlates with pika persistence, as it may reflect a reduction in available understory forage and can limit their ability to surveil their territory and avoid avian predators (Wilkening 2007), tree encroachment into subalpine meadow habitat has been linked to population fragmentation in the Olympic marmot (Marmota
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Olympus) in Washington (Griffin et al. 2009). The upslope migration of trees and shrubs associated with climate change is also reducing habitat for the Alaska marmot (Marmota broweri) in Alaska’s Brooks Range (Gunderson et al. 2012). Similarly, juniper-pinyon encroachment has contributed to extirpations of pygmy rabbits (Brachylagus idahoensis) in Nevada and California (Larrucea 2007), just as juniper-pinyon percent cover appears to be a significant predictor of pika absence in the Great Basin (see Appendix). Mirroring the hardiness and complexity of pika response to atypical climatic conditions, some populations of marmots appear to be better adapted to warmer climates than others, though the rate of warming will likely outpace that adaptive capacity; widespread extinction seems unlikely, but localized extirpations focused at low elevation, marginal habitat are expected (Armitage 2013). Pikas exemplify the fragility and limitations of high elevation ecosystems.
Despite the similar challenges, researchers must use caution when comparing the pika’s response to climate with other montane species, as its unique life history and behavioral plasticity may limit its applicability. Montane mammals employ different strategies to respond to the challenges posed by the dynamic seasonality and harsh winters of mountain ecosystems, each with their own unique obstacles posed by climate change. While pikas cache haypiles for the winter, a behavior that is limited by high summer temperatures and shifting plant communities (Smith and Erb 2013, Stafl and O’Connor 2015), marmots and other mountain squirrels hibernate to endure the low temperatures and limited plant availability of winter. Marmots are emerging from hibernation earlier in response to warmer spring temperatures, out of sync with the timing of snowmelt and the growing season, with potential impacts on their fitness and survival (Inouye et al. 2000). In this case, the timing of warming may be more important than the warming itself, as hibernating animals depend upon environmental cues to maximize the efficiency of their adaptive response. When considering mutual climatic stressors facing different montane species, it is important to understand the unique limiting factors associated with their life histories and evolutionary strategies.
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Management Recommendations
Developing a conservation strategy for an indicator species at the frontier of climate change impacts offers both a novel challenge and a significant learning opportunity. The main question, though, is how we protect a species whose primary threat is climate change – a global phenomenon that cannot be directly or significantly mediated by local or regional management actions. Most likely, the answer is an integrated approach informed by a place-based, comprehensive understanding of the pika’s life history and foraging behavior as it relates to changes in local climate. First, we must prioritize conservation efforts by identifying genetically significant populations, high-quality sites that could function as habitat refugia, and areas of vital habitat connectivity to allow for adequate gene flow and population stability. Species Distribution Models (SDMs) can tell us where pikas are the most vulnerable to shifts in temperature or water availability. Field surveys and remote sensing can be used to characterize habitat quality and assess plant community composition and structure. Though little can be done to combat the source of the issue (i.e., temperature stress, altered hydrologic regimes, etc.), there are some opportunities to address the mechanisms and mitigate the ecological impacts.
Habitat Restoration and Enhancement Understanding the vegetation types and characteristics that have either promoted or limited pika persistence can inform restoration decisions and buffer future climate stressors. Land managers could potentially install plants high in PSMs, particularly in areas where seasonality is extreme. Plants with high metabolic water content might be selected for low-elevation sites where moisture is limiting, and plants with significant nutritional components (e.g., digestible protein, nitrogen) may be added at locations where the nutritional quality of available forage is poor. Habitat restoration, including the installation of preferred plant species and beneficial habitat features (e.g., fallen logs), can be used to support vulnerable populations and establish habitat connectivity and wildlife corridors. Habitat features relevant to pika dispersal and recolonization are currently being tested along Interstate-90 in the Cascade Range of Washington (Personal communication). Areas seeing rapid successional changes in plant
Page 40 of 62 community, such as through juniper-pinyon encroachment or the replacement of alpine meadows or aspen woodlands with conifer forests, should be prioritized for monitoring and potential restoration, as these changes may reflect a reduction in forage diversity and quality or a shift in microclimatic conditions. Restoration of alpine meadows and other high elevation plant communities can benefit a range of species beyond the pika, including birds and other montane mammals.
Researchers are now considering novel experiments to test restoration methods and to evaluate limiting factors. Hamster bottles are being places among the talus in order to bolster stressed populations, which will be followed by careful monitoring to assess the importance of water availability as a limiting factor (Personal communication). Additionally, targeted plantings of shrubs like fernbush that have been shown to positively correlate with pika persistence (Ray et al. 2016) are being pursued. Field trials like these are necessary to provide ground-truthed data that validates models and informs conservation strategies.
Legal and Regulatory Actions Conservation strategies can also involve legal action and regulation. Simple management decisions like placing trail restrictions in areas where vulnerable pika populations are known to exist, as heavy trail traffic may disrupt foraging behavior (Stafl and O’Connor 2015). On the larger scale, the Endangered Species Act (ESA) may be utilized as a tool to protect the pika. This could prevent further habitat degradation or fragmentation, and allocate resources and attention to restoring populations. However, federal and even state listing is a highly contentious decision, as protections to such a widely distributed species could create significant restrictions on activities like mining, timber production, and watershed management. Due to the isolation and inaccessibility of mountain areas, the listing of the pika does not pose many of the same problems presented by other species at lower elevation where urban development and agriculture can be interrupted; however, mountain ecosystems are hotspots for recreation, and activities like skiing, snowboarding, camping, hiking, and tourism could be inhibited. One important question is whether the natural resource agencies (e.g., U.S. Forest
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Service, Bureau of Land Management) will take the lead in pursuing further, objective research to determine whether listing is necessary, despite these potential challenges and disputes. Legal protections for the pika may very well begin at the local level with Ecologically Significant Unit designations and state agency regulations. Although efforts to list the pika under the ESA have been deterred twice in the last decade (2010 and 2016 due to lack of evidence, the rapidly growing body of research may soon facilitate legal action. Whether or not the species and habitat protections afforded by the ESA can adequately balance climate impacts in the face of the infamous bureaucracy and limitations associated with the contentious rule remains unknown.
Adaptive Capacity as a Conservation Metric Natural resource managers can enhance their ability to address the issues of biodiversity loss and reduced ecosystem services related to the ecological impacts of climate change by considering species’ adaptive capacity (AC) when developing conservation strategies. Reflecting the ability of a species to tolerate stress (such as climate change), AC corresponds with phenotypic plasticity, genetic diversity, and dispersal ability, and is not to be confused with a species’ sensitivity to stress. However, a firm distinction must be made between fundamental AC and realized AC (Beever et al. 2016b). Realized AC is the actual expression of AC after accounting for the limitations of extrinsic factors, such as land use and land cover, pollution, interspecific competition, and habitat loss or fragmentation. For example, the fundamental ability of pikas to shift their diet to a more readily available and persistent food source like moss could be hampered by anthropogenic disturbance that alters moss cover in the landscape (Beever et al. 2016b). Furthermore, dietary plasticity can only go as far as the availability of adequate vegetation. Conservation strategies can work to reduce the vulnerability of the target species, such as the pika, by taking measures that either improve the expression of the fundamental AC or reduce extrinsic constraints limiting that expression.
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Appendix: Preliminary Vegetation Data Analyses for the Great Basin
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Background
Objective The results of my secondary research presented in the main portion of this paper suggest that the quality and availability of forage, including its interactions with climate, may influence the persistence or extirpation of pika populations. A diverse understory of forbs and other plants high in secondary metabolites and nutritional components may promote pika persistence, while extensive tree cover and graminoid-dominated plant communities may drive extirpation, especially in areas of extreme seasonality where warm, dry summers may limit foraging time and where winter haypiles are essential to survival and fitness. However, these relationships are highly location-specific and vary across the pika’s range.
In order to test the conclusions generated by my secondary research and to shed light on the role of vegetation in the Great Basin – the part of the pika’s range most heavily affected by recent extirpations (Beever et al. 2016a) – I utilized statistical methods to test various plant species and types as predictors of pika presence. Specifically, I am interested in finding if any of the vegetative variables in question can serve as significant predictors of pika occurrence in the Great Basin, which may help further characterize the ultimate drivers of pika persistence and extirpation. An information- theoretic framework was employed to assess multiple competing hypotheses based on a model set constructed a priori. These preliminary analyses help demonstrate what can be learned from statistical exploration and modeling of data collected in the field, and also lay the foundation for a forthcoming, more robust investigation.
Hypotheses Development For my preliminary occupancy analyses, I chose to investigate the following predictors (independently and in combination), measured as continuous variables (percent cover):
- Juniper (Juniperus spp.) - Single-leaf pinyon (Pinus monophyla)
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- Cheatgrass (Bromus tectorum) - Aspen (Populus tremuloides) - Fernbush (Chamaebatiaria millefolium) - Oceanspray (Holodiscus discolor) - Forb total (sum of percent cover for all forb species)
Juniper and pinyon encroachment has been identified as one of the most significant determinants of pygmy rabbit (another lagomorph found at mid-to-high elevations) extirpation in the Great Basin (Larrucea 2007). Fire suppression and other land-use changes have allowed juniper-pinyon woodland communities to expand into sagebrush and grass-dominated plant communities, increasing their distribution approximately 2.5 times over the last 150 years, and resulting in a rapid, drastic reduction in understory vegetation and habitat. Pollen records suggest that a dramatic decline in pygmy rabbits during the mid-Holocene correspond with an expansion of juniper-pinyon woodlands (Grayson 2006). Similarly, cheatgrass, an invasive grass that has ravaged native grasslands across the Great Basin, has been negatively associated with pygmy rabbit presence (Larrucea 2007), and may result in a reduction in forage quality and diversity for pikas. In addition to altering fire regimes and disturbing plant community successional dynamics, cheatgrass, in its later phenological stages, is difficult to digest and offers little in nutritional value to foraging pikas (Beever et al. 2008). Representing a sort of inverse of juniper-pinyon woodlands, aspen woodlands, which are negatively associated with juniper-pinyon woodlands and have seen dramatic reductions across the western U.S. over the past century, provide a complex understory and vital habitat for an array of birds and mammals (Wall et al. 2006, Stam et al. 2008), potentially offering high quality forage and habitat for pikas, as well. Fernbush is being considered as a potential predictor of pika occupancy because it was recently implicated as a significant predictor of distribution at an interior range margin, Lava Beds National Monument (Ray et al. 2016). Anecdotal evidence has suggested oceanspray as another shrub that potentially serves as an important source of high-quality forage for pikas (Personal communication). Finally, forb total – the summed percent cover of all forb species present – is included as a potential predictor, since forb cover and species
Page 45 of 62 richness has been demonstrated as a significant predictor of pika occupancy and density in a variety of recent studies across the pika’s range (Rodhouse et al. 2010, Erb et al. 2014, Ray et al. 2016).
I hypothesize that juniper, pinyon, and cheatgrass will negatively predict pika occupancy (or positively predict pika absence), and that aspen, fernbush, oceanspray, and forb total will positively predict pika occupancy (or negatively predict pika absence). Following my preliminary findings, I plan to incorporate more community-level hypotheses (e.g., relative tree/shrub and forb/graminoid cover) in later analyses.
Methods
Dataset The dataset, covering transect data from hundreds of locations in the Great Basin across twelve years, was imported into R as a CSV file. Occupancy, a binary variable (0=absent, 1=present), was defined as any talus patch where unequivocal evidence of pika presence was found, including actually seeing pika individuals, hearing pika calls, and locating fresh haypiles. Old haypiles (i.e., desiccated or degraded haypile that has clearly been abandoned) were recorded in the dataset but insufficient for classification of a patch as occupied. Percent cover was recorded for the five plant species with the greatest cover value along the transects, assessed using ocular cover estimations. As a potential source of error, this methodology may underestimate the importance of some plant species that are not as abundant but function as preferred, high quality sources of nutrition, metabolic water, or PSMs. Additionally, percent cover was recorded as zero if the plant was not included in the five species, even though it may still have been present at low density.
Statistical Analyses The R Console was used to conduct a series of logistic regressions, with pika occupancy as the dependent (response) variable and percent cover as the independent (predictor) variables. In order to test the normality of the distribution of the predictor
Page 46 of 62 variables, I constructed histograms of each. Due to the size of the dataset and the number of zero values present for percent cover, each of the predictor variables were left skewed and needed to be log-transformed to correct this. Next, I ran correlation functions between each of the predictor variables to determine if any were covariates of each other, in which case they should not be included in the same model. Since none of the predictors were significantly correlated with each other, I was able to proceed with running my model sets. I ran generalized linear model (glm) functions on my predictors and called summaries of the resulting models, which gave me the Akaike’s Information Criterion (AIC) value for each. Akaike’s Information Criterion (AIC) is a metric for comparing model fit between a set of models constructed a priori. Lower AIC values indicate better fit, and models with differences in AIC values (ΔAIC) great than two are considered significantly different in fit (Burnham and Anderson 2002).
Results
The most predictive model of the set includes the additive variables of juniper, pinyon, and cheatgrass (Table 1). Juniper and/or pinyon show up in each of the best fitting models. The null model features the highest AIC score and so the poorest fit, followed by forb total). Juniper, pinyon, cheatgrass, and forb total each display negative relationships with pika occupancy in their respective models, while aspen, fernbush, and oceanspray each display positive relationships. The strongest models are composed of negative predictors, while the weakest models feature positive predictors with the exception of the weakest model (exluding the null model), forb total. AIC values range from 1624.4 (strongest model) to 1727.6 (null model), and ΔAIC values range from 0 to 103.2. The two strongest models are the combinations with the most predictors (3 independent variables and 1 response), and thus the least parsimony.
Table 1. Relative support for selected models of pika occupancy in the hydrogeographic Great Basin. K indicated the number of fitted parameters. Models are ranked in order of increasing AIC value (lower value indicated better fit). ΔAIC indicated the difference between the AIC value of the indicated model
(AICi) and the model with lowest AIC value (AIC0).
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Model: Predictor (effect sign) K AIC ΔAIC Juniper (-), Pinyon (-), Cheatgrass (-) 4 1624.4 0 Juniper (-), Pinyon (-), Forb Total (-) 4 1636 11.6 Juniper (-), Pinyon (-) 3 1638 13.6 Pinyon (-) 2 1655 30.6 Juniper (-) 2 1695.8 71.4 Cheatgrass (-), Forb Total (-) 3 1707.1 82.7 Cheatgrass (-) 2 1709.3 84.9 Fernbush (+) 2 1711.9 87.5 Aspen (+), Forb Total (+) 3 1717.2 92.8 Aspen (+) 2 1718.4 94 Oceanspray (+) 2 1722.1 97.7 Forb Total (-) 2 1726.2 101.8 Null (Intercept-only) 1 1727.6 103.2
Discussion
Juniper and pinyon appear to be significant predictors of pika absence in the hyrdrogeographic Great Basin (Figure1). Although the precise mechanisms are unclear, the supplemental effect of cheatgrass in the strongest model may indicate that successional shifts in plant community composition and structure, and resulting decline in forage quality, may be a driver. These negative variables exhibit the strongest predictive power of the model set, potentially suggesting that loss of adequate forage or habitat is a more important driver of extirpation than high quality forage is of persistence. However, since juniper, pinyon, and cheatgrass are each associated with xeric conditions, the negative relationship between these plant species and pika occupancy may simply reflect the negative effects of warmer, drier microclimates. Further analyses of how juniper-pinyon and cheatgrass have changed at each site over time in relation to changes in pika density could offer insight into how these plant community shifts affect pika populations.
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Figure 1. Plots of pika occupancy versus total percent cover of juniper and pinyon. On the y-axis, 1 indicates occupied talus patches (presence) and 0 indicates unoccupied patches (absence).
Surprisingly, total forb cover did not offer a significantly better fit compared to the null model and actually exhibited a weakly negative relationship with pika occupancy. Metrics of forb cover have received strong support as determinants of pika distribution in the Great Basin and elsewhere, potentially due to their relatively high nutritional content and prevalence of PSMs, as well as a reflection of a more favorable, mesic microclimate (Wilkening 2007, Rodhouse et al. 2010, Erb et al. 2014, Ray et al. 2016). Part of my hypothesis for why juniper-pinyon encroachment might negatively impact pikas – the reduction in understory and forage quality – is at odds with the lack of support for forbs as a predictor of pika occupancy. Inserting total forb cover as an additional predictor to models featuring juniper and pinyon did not contribute significantly to model fit, nor did it strengthen models of cheatgrass or aspen. Perhaps total forb cover is not as essential as the cover of particular, preferred forb species. Further analysis at a finer taxonomic resolution, exploring particular forb species based on common haypile components at the sites, might better represent the influence of forb cover as a predictor. Forb diversity would be another interesting metric to explore, but the transect methodology, which only recorded the five most pervasive species, does
Page 49 of 62 not lend itself to species richness estimates, since species found at lower densities would not be represented.
Puzzlingly, parsimony does not seem to matter much for my model set. While AIC is meant to favor models balancing the number of variables with goodness of fit (i.e., more variables only strengthen the explanatory power of the model up to a certain point before it becomes profligate), higher K values consistently equate to greater fit in each case (Table 1), as well as in other tested combinations not shown. Further examination of the plots of occupancy against each variable and combination may help explain patterns of model ranking. Additionally, calculations of the AICc values (AIC corrected for small sample size) and Akaike weights for the different variables and models may provide more accurate estimates of model fit and prediction strength.
These results represent preliminary findings that will precede a more robust exploration and analysis of this dataset, with the intention of eventual publication in the peer- reviewed literature. Subsequent analyses will cover a range of levels, comparing averages across different sites (defined as all talus patches within a 3 km radius of a historical pika record) in the Great Basin, as well as comparing individual occupied and unoccupied patches within sites. These analyses will consider issues of persistence rather than just occupancy in order to potentially identify relationships between changes in occupancy or population density and shifts in plant community composition at the locations across the twelve years of monitoring. Population density will be approximated using estimated number of individual pikas present and corresponding number of transects conducted, which will offer a higher-resolution perspective on population dynamics and mechanisms of extirpation. The preliminary analyses have facilitated my exploration of the dataset and provided a baseline upon which to base further investigation; however, the results of the final analyses should be more credible and interpretable in order to pass peer review and to justify publication.
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Acknowledgements John Callaway, Ph.D., Professor and Graduate Program Director for M.S. in Environmental Management at the University of San Francisco, served as my advisor for this project and offered countless hours of assistance and invaluable feedback on my paper as it was being developed. I received guidance from Erik Beever, Ph.D., Research Ecologist with the U.S. Geological Survey (USGS), and Jennifer Wilkening, Ph.D., Wildlife Biologist and Habitat Conservation Plan Coordinator with the U.S. Fish and Wildlife Service (USFWS), both of whom are experts in the field of pika ecology and have published relevant articles in peer-reviewed journals, many of which are cited in this paper, and were able to direct me to many other pertinent studies. Dr. Beever provided the data and R script used in my data analyses in the appendix, and Dr. Wilkening advised me on the statistical implementation procedures. Finally, Amalia Kokkinaki, Ph.D., Assistant Professor at the University of San Francisco, worked with me to prepare my data and to develop my approach for the statistical analyses.
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