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Zapus Hudsonius Luteus) Jennifer K Variation in phenology of hibernation and reproduction in the endangered New Mexico meadow jumping mouse (Zapus hudsonius luteus) Jennifer K. Frey Department of Fish, Wildlife, and Conservation Ecology, New Mexico State University, Las Cruces, NM, United States of America Frey Biological Research, Radium Springs, NM, United States of America ABSTRACT Hibernation is a key life history feature that can impact many other crucial aspects of a species’ biology, such as its survival and reproduction. I examined the timing of hibernation and reproduction in the federally endangered New Mexico meadow jumping mouse (Zapus hudsonius luteus), which occurs across a broad range of latitudes and elevations in the American Southwest. Data from museum specimens and field studies supported predictions for later emergence and shorter active intervals in montane populations relative to lower elevation valley populations. A low-elevation population located at Bosque del Apache National Wildlife Refuge (BANWR) in the Rio Grande valley was most similar to other subspecies of Z. hudsonius: the first emergence date was in mid-May and there was an active interval of 162 days. In montane populations of Z. h. luteus, the date of first emergence was delayed until mid-June and the active interval was reduced to ca 124–135 days, similar to some populations of the western jumping mouse (Z. princeps). Last date of immergence into hibernation occurred at about the same time in all populations (mid to late October). In montane populations pregnant females are known from July to late August and evidence suggests that they have a single litter per year. At BANWR two peaks in reproduction were expected based Submitted 6 May 2015 on similarity of active season to Z. h. preblei. However, only one peak was clearly Accepted 9 July 2015 Published 6 August 2015 evident, possibly due to later first reproduction and possible torpor during late Corresponding author summer. At BANWR pregnant females are known from June and July. Due to the Jennifer K. Frey, [email protected] short activity season and geographic variation in phenology of key life history events Academic editor of Z. h. luteus, recommendations are made for the appropriate timing for surveys for Donald Kramer this endangered species. Additional Information and Declarations can be found on page 23 Subjects Conservation Biology, Ecology, Zoology Keywords Life cycle, New Mexico meadow jumping mouse, Zapus hudsonius luteus, Hibernation, DOI 10.7717/peerj.1138 Activity season, Reproduction, Endangerd species, Geographic variation, Elevation, Phenology Copyright 2015 Frey INTRODUCTION Distributed under Creative Commons CC-BY 4.0 Hibernation is an adaptive strategy that some mammals use to cope with long-term sea- sonal limitations in food or water (Davis, 1976; Heldmaier, Ortmann& Elvert, 2004 ; Ruf& OPEN ACCESS How to cite this article Frey (2015), Variation in phenology of hibernation and reproduction in the endangered New Mexico meadow jumping mouse (Zapus hudsonius luteus). PeerJ 3:e1138; DOI 10.7717/peerj.1138 Geiser, 2014). Hibernation is characterized by prolonged multiday bouts of torpor during which the animal’s metabolic rate is significantly lowered, body temperature decreases to- ward ambient temperature, and many physiological functions cease (Williamset al., 2011 ; Ruf& Geiser, 2014 ). Thus, while hibernation can confer profound savings of water and energy, and it has other indirect benefits such as increased survival through predator avoid- ance, it also bears costs related to altered physiological functions and reduced opportunity for reproduction (Ruf& Geiser, 2014 ). Despite a great deal of research on the physiology of hibernation, there has been disproportionately little research on the ecological conse- quences of hibernation (Lane, 2012). Elucidating the timing and duration of biological events associated with hibernation is central to understanding its ecological consequences, because hibernation is tightly linked to other crucial aspects of a species’ biology (Kirkland & Kirkland, 1979; Turbill, Bieber& Ruf, 2011 ). Recovery from hibernation, reproduction, and sequestering energy reserves to enter and survive the next hibernation all must happen within a brief active period during the warmer months. Thus, timing of emergence from hibernation influences subsequent timing of reproduction, number of litters possible, timing of entrance into hibernation (i.e., immergence), and ultimately overwinter survivorship (e.g., Muchlinski, 1988; Dobson, Badry& Geddes, 1992 ; Ozgulet al., 2010 ; SheriV et al., 2011). Thus, understanding the phenology of hibernation and reproduction is central to understanding the life history of hibernating species. Such questions have gained increased importance due to the potential for altered phenology and mismatches in the phenology of interacting species as a consequence of climate change (e.g., Inouyeet al., 2000; Lane, 2012; Boutin& Lane, 2013 ; SheriV et al., 2011; SheriV et al., 2013). Most studies on variation in phenology of the annual cycle of mammalian hibernators have been conducted on ground squirrels (Sciuridae: Marmotini) and dormice (Gliridae). The jumping mice (Dipodidae: Zapodinae) are another group of small mammal hiberna- tors that are confronted with strongly seasonal environments in the northern temperate zone. However, there has been comparatively little research on hibernation in jumping mice, especially with respect to variation in phenology of the annual cycle (e.g., Lyman, Willis& Malan, 1982 ). In comparison with most ground squirrels and dormice, jumping mice have much smaller body size (<25 g) and they have not been reported to cache food (Vander Wall, 1990). Although terrestrial mammal hibernators usually are small, in part to facilitate use of underground burrows that are buVered from thermal extremes, hibernators benefit from relatively large body size (while still remaining small enough to burrow) because the principle source of energy for most hibernators during torpor is body fat (Humphries, Thomas& Kramer, 2003 ; Florant& Healy, 2012 ). However, many granivorous hibernators also utilized cached seeds for food during the hibernation period, which allows greater flexibility in use of torpor (e.g., Vander Wall, 1990; French, 2000; Humphries, Thomas& Kramer, 2003 ; SheriV et al., 2011). Jumping mice are somewhat unique among granivores in that they apparently do not use food caches and hence must rely on body fat for all energy needs during hibernation (French, 1985; Humphries, Thomas& Kramer, 2003 ). Thus, the phenology of the annual cycle in jumping mice, with its attendant costs and benefits, may diVer in comparison with other taxonomic groups. Frey (2015), PeerJ, DOI 10.7717/peerj.1138 2/27 Other than through use of radio-telemetry, there are no eVective methods to detect most species while they are in hibernation, since they are inactive in underground burrows. Consequently, in order to study these animals in the wild, information must be available on when they are active above ground. This is particularly true for threatened and endangered species because populations must be monitored to detect trends, and surveys for the species’ presence are often required in areas of potential habitat when activities might cause harm to the animals if present. For instance, the New Mexico meadow jumping mouse, Zapus hudsonius luteus, was listed as endangered under the US Endangered Species Act in June 2014 due to substantial declines in populations over the last several decades (US Fish& Wildlife Service, 2014 ). This subspecies was originally described as a distinct species (Miller, 1911) and recent molecular analyses have validated it as relatively diverged monophyletic clade (Malaney& Cook, 2013 ). Zapus h. luteus occurs in the American Southwest, with an historical range that included portions of southern Colorado, New Mexico, and central and eastern Arizona (Hafner, Petersen& Yates, 1981 ; Frey, 2012; Malaney, Frey& Cook, 2012 ). It is a specialist of riparian habitats and hence its distribution includes both low elevation sites within desert biomes and high elevation sites within boreal biomes (Frey& Malaney, 2009 ; Malaney, Frey& Cook, 2012 ). The known distribution of Z. h. luteus extends between 32.7◦N and 37.2◦N latitude and between 1,375 m and 2,926 m elevation, possibly as low as 935 m (i.e., Camp Verde, Yavapai County, Arizona; Frey, 2008; Frey, 2012). Given the large size and extreme topographic variability of this region, Z. h. luteus is expected to exhibit geographic variation in phenology of its hibernation and reproduction. However, there is little existing information on phenology of the annual cycle in this taxon. In addition, there are relative few studies on phenology of the annual cycle in other taxa of jumping mice. Within other subspecies of the meadow jumping mouse, Z. hudsonius, phenology has been described at four locations, three in the eastern US (Minnesota, Quimby, 1951; New York, Whitaker, 1963; Michigan, Nichols& Conley, 1982 ; Muchlinski, 1988) and one in Colorado (Meaney et al., 2003), but none of these studies evaluated variation in phenology at locations in diVerent environments. Within the western jumping mouse, Z. princeps, phenology has been described for a population in Alberta (Falk& Millar, 1987 ), and three studies have evaluated variation in phenology of diVerent populations living in diVerent environments in Wyoming (Brown, 1967) and Utah (Cranford, 1978; Cranford, 1983). No studies have evaluated
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