Life in an extreme environment: a historical perspective on the influence of temperature on the ecology and evolution of woodrats

Journal of Mammalogy, 95(6):1128–1143, 2014 Life in an extreme environment: a historical perspective on the influence of temperature on the ecology and evolution of woodrats FELISA A. SMITH,* IAN W. MURRAY, LARISA E. HARDING, HILARY M. LEASE, AND JESSICA MARTIN Department of Biology, University of New Mexico, Albuquerque, NM 87131, USA (FAS, IWM, LEH, HML, JM) School of Physiology, Faculty of Health Science, University of the Witwatersrand, Parktown, 2193, South Africa (IWM, HML) Arizona Game and Fish Department, 5000 W Carefree Highway, Phoenix, AZ 85086, USA (LEH) * Correspondent: The heterogeneous topography of the Great Basin province leads to one of the most climatically variable regions in the Northern Hemisphere. Along the southwestern edge lies Death Valley, an area of even more extreme climate and physiographic relief; Death Valley has the dubious distinction of being the hottest place on earth. Our research investigates the adaptive response of Neotoma (woodrats) to temperature fluctuations over the late Quaternary on the valley floor and along a nearby elevational and environmental gradient. By combining fieldwork on extant animals living on the valley floor with historical information from museum specimens and paleomiddens, we reconstruct the evolutionary histories of 2 species (N. lepida and N. cinerea) differing significantly in size and habitat preferences. Here, at the modern limit of both species’ thermal and ecological thresholds, we find fluctuations in body size and range boundaries over the Holocene as climate shifted. Although N. cinerea is extirpated on the east side of the valley today, it was ubiquitous throughout the late Quaternary. Moreover, we find fundamental differences in the adaptive response of woodrats related to elevation and local microclimate. Modern work suggests the mechanism is physiological; exposure to consistently high temperatures leads to high mortality. Thus, high temperatures strongly restrict time available for the essential activities of foraging and mating. Our results illustrate the profound influence temperature has on all aspects of woodrat life history, ecology, distribution, and evolution. Key words: adaptation, body-size evolution, climate change, Furnace Creek, late Pleistocene, Titus Canyon Ó 2014 American Society of Mammalogists DOI: 10.1644/13-MAMM-S-070 Yesterday afternoon I put out 49 rodent traps thru the big mesquites and sand-dunes south of the ranch about 1½ miles. Absolutely the only vegetation in sight for hundreds of yards is the mesquite . . . . It would appear that the mesquite foliage and beans, and the insects [that] live on these and in the wood of dead trunks and branches (which are abundantly bored) furnish the prime food supply of all the vertebrates in that tract. Wood rat sign is abundant, consisting of small accumulations of mesquite twigs, pieces of [illegible word] and cow and horse manure . . . . Many cutoff twig ends high in the mesquites show that the wood rats climb all over these trees . . . The Great Basin is a unique and striking region of North America. The basin-and-range topography, which is characterized by literally hundreds of parallel-running mountain ranges interposed with deep valleys, leads to substantial physiographic relief, and not surprisingly, quite variable environmental conditions (Hunt 1967; King 1977; Fiero 1986). At the southwestern edge of the geological province lies Death Valley, an extreme region in this already heterogeneous landscape. Death Valley is an ~250-km basin located between 2 major block-faulted mountain ranges, the Amargosa on the east side and the Panamint on the west side. It contains the greatest physiographic relief in the contiguous United States; the gradient from Badwater (86 m) to Telescope Peak (3,392 m) rises some 3,479 m within a scant 24 km (Fig. 1). Because —Field notes of Joseph Grinnell, 10 April 1917 Archives of the Museum of Vertebrate Zoology, University of California, Berkeley www.mammalogy.org 1128 December 2014 SPECIAL FEATURE—LIFE IN AN EXTREME ENVIRONMENT 1129 FIG. 1.—Location of study sites. a) Death Valley National Park, California. The park is situated in the southwestern edge of the Great Basin geological province and lies between the Panamint Mountains on the west, and the Amargosa Range on the east. b) Location of 2 study sites within the valley. Paleomiddens were collected during 2006, 2007, and 2009 along a 1,500-m elevational transect following Titus Canyon; livetrapping was conducted during 2003–2008 in mesquite thickets at Furnace Creek. c) Reconstruction of the Lake Manly lake system as it would have appeared during the Last Glacial Maximum (~21,000 years ago). Selected roads (lines) and towns (dots) are shown for context; arrows indicate direction of water flow. Note the location of the Furnace Creek and Titus Canyon study sites. Redrawn after United States Geological Survey image from Wikipedia Commons (http://en.wikipedia.org/wiki/File:Lake_Manly_system.png; National Park Service 2013). d) A composite elevational profile for 2 parallel due-west geographical transects. The transect in pink bisected the highpoint of the Panamint Mountains, Telescope Peak, as well as the low point in Death Valley, Badwater Basin (86 m). The gray transect bisects just north of Titus Canyon. Elevational profiles were constructed using due-west paths created in Google Earth and were standardized for distance and elevational gain. The extreme topography leads to significant heterogeneity in habitats as well as climate. of the extreme topography, Death Valley lies in a severe rain shadow, which coupled with below-sea-level elevation, contributes to a hyperarid climate. Indeed, Death Valley has the dubious distinction of being the hottest place on earth (El Fadli et al. 2013), with maximum temperatures regularly exceeding 508C during the summer months (Western Regional Climate Center 2013). Living in the hottest place on earth poses significant challenges to animals (Fig. 2). The intense heat is coupled with highly irregular annual precipitation averaging only 4.8 cm/year (Western Regional Climate Center 2012; Fig. 2). It is not just the extreme heat—temperatures of up to 578C (1348F) have been recorded in the shade (Roof and Callagan 2003)— but also the duration of heat episodes. In 2001, for example, Death Valley experienced 154 consecutive days with temperatures at or above 388C (1008F—Western Regional Climate Center 2012). Such severe climatic occurrences are likely to become more common over the next few decades. The recent report by the Intergovernmental Panel on Climate Change (2012) on extreme events concluded: ‘‘Models project substantial warming in temperature extremes by the end of the 21st century. It is virtually certain that increases in the frequency and magnitude of warm daily temperature extremes and decreases in cold extremes will occur in the 21st century at the global scale. It is very likely (...truncated)