An International Journal of Ecology, Evolution and Environment

An International Journal ofEcology, Evolution and Environment

Hibernation and Overwinter Body Temperatures inFree-Ranging Thirteen-Lined Ground Squirrels,

Ictidomys tridecemlineatus

BROOKE KISSER1AND H. THOMAS GOODWIN2

Department of Biology, Andrews University, Berrien Springs, Michigan 49104

Hibernation and Overwinter Body Temperatures inFree-Ranging Thirteen-Lined Ground Squirrels,

Ictidomys tridecemlineatus

BROOKE KISSER1AND H. THOMAS GOODWIN2

Department of Biology, Andrews University, Berrien Springs, Michigan 49104

ABSTRACT.—Free-ranging, juvenile thirteen-lined ground squirrels (Ictidomys tridecemlineatus)in southwestern Michigan were fitted in late summer or fall with external skin-temperatureloggers. Data were obtained the following spring for five males and three females. During theheterothermal period, all squirrels exhibited 11–22 prolonged (x 5 9.4 d) torpor boutspunctuated by typically brief (x 5 14.3 h) arousal bouts, with mean monthly torporbouts becoming longer and deeper until Feb. and reversing thereafter. Torpor-bout duration increased as minimum skin and soil temperatures decreased. Onaverage, males initiated the first torpor bout later in fall, terminated the last torporbout significantly earlier in spring and thus spent less time in the heterothermalperiod than did females. Three males displayed relatively short torpor bouts andlong arousal bouts as they approached the end of hibernation. Squirrels gainedweight variably in fall and spring, and one female lost 39% of body mass duringhibernation.

INTRODUCTION

Hibernation has been intensively studied in ground-dwelling squirrels (family Sciuridae)within the tribe Marmotini. In captivity, marmotine and other mammalian hibernatorsstudied at controlled ambient temperatures in cold chambers universally display acharacteristic body-temperature profile during hibernation: multiple, prolonged bouts oftorpor punctuated by much shorter bouts of arousal when the animal returns to euthermy.Above ,0 C ambient, minimum body temperature during torpor scales directly withambient temperature; and duration of torpor scales inversely with both ambient and bodytemperature, as well as with metabolic rate (Twente and Twente, 1965; Pivorun, 1976; Geiserand Kenagy, 1988; Geiser et al., 1990; Buck and Barnes, 2000). Below ,0 C ambient, animalstypically defend body temperature, decrease duration of torpor and increase metabolic rate(Pivorun, 1976; Geiser and Kenagy, 1988; Buck and Barnes, 2000).

Under field conditions with seasonally variable soil temperatures, these body-temperaturepatterns likewise hold, at least qualitatively, for free-ranging hibernators within Tamias(chipmunks–Humphries et al., 2003), Marmota (marmots and woodchucks–Florant et al.,2000; Zervanos and Salsbury, 2003; Lee et al., 2009; Zervanos et al., 2010), Cynomys (prairiedogs–Lehmer and Biggins, 2005), Spermophilus [Old World ground squirrels–Hut et al., 2002(studied under semi-natural conditions)] and Urocitellus (Holarctic ground squirrels–Wang,1973, 1979; Young, 1990; Michener, 1992; Buck et al., 2008; Frank et al., 2008). However,comparisons of free-ranging and captive hibernators sometimes reveal quantitativedifferences in body-temperature patterns (Geiser et al., 2000). For example, free-rangingarctic ground squirrels (Urocitellus parryii) display average torpor bouts in mid-winter nearly

1 Present address: Biology Department, Everett Community College, Everett, Washington 98201;Telephone: (425) 388-9043; e-mail: [email protected]

2 Corresponding author: e-mail: [email protected]

Am. Midl. Nat. (2012) 167:396–409

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10 d longer than predicted based on studies of captive animals of the same species (Buck etal., 2008).

Furthermore, field studies document ecologically-relevant variation in the phenology ofand body temperatures within hibernation across species, along altitudinal or latitudinalgradients within a species (Lehmer and Biggins, 2005; Zervanos et al., 2010) and across ageand sex classes within a population (Young, 1990; Michener, 1992; Zervanos and Salsbury,2003; Buck et al., 2008). They also demonstrate that under field conditions, hibernation (theperiod of sequestration below ground) and the heterothermal period (the period betweenonset of first torpor and arousal from final torpor) are not necessarily equivalent; squirrelsmay spend several days euthermic but sequestered below ground before and especially afterthe heterothermal period (Michener, 1992; Barnes and Ritter, 1993). To avoid confusion,we follow the distinction between hibernation and the heterothermal period in this paper.

Here, we report overwinter skin temperatures (as a proxy for body temperatures) for free-ranging thirteen-lined ground squirrels (Ictidomys tridecemlineatus), the first such study forthe genus Ictidomys. For each individual, we document attributes of the heterothermalperiod shown to vary seasonally within hibernation, or between age cohorts (juveniles,adults) or sexes, in other free-ranging marmotines (Young, 1990; Michener, 1992; Zervanosand Salsbury, 2003; Buck et al., 2008). These include timing and duration of theheterothermal period, duration and depth of torpor bouts, lowest skin temperature duringhibernation, duration of arousal bouts, and the proportion of the heterothermal period intorpor. We also examined correlations among torpor-bout duration, minimum skintemperature during torpor, and soil temperatures (measured regionally); exploreddifferences between sexes and across months during the heterothermal period ofhibernation; and obtained body masses before and after hibernation to estimate growthpatterns, and weight loss during hibernation.

Thirteen-lined ground squirrels appear to be obligate hibernators across their range, withhibernation demonstrated as far north as Manitoba (Criddle, 1939) and southward to Texas(McCarley, 1966). A previous study documented the typical pattern of torpor and arousalduring hibernation under semi-natural conditions, but it did not report skin or bodytemperatures (Scheck and Fleharty, 1980). Vernal emergence from hibernation typicallytakes place in Mar. and Apr. (on average, males usually before females) and autumnalimmergence into hibernation extends from Jul. to Oct. or even early Nov. (on average, adultmales typically before adult females, which on average precede juveniles–Wade, 1927;Criddle, 1939; Beer, 1962; Rongstad, 1965; McCarley, 1966; Clark, 1971; Scheck andFleharty, 1980).

MATERIALS AND METHODS

SQUIRREL CAPTURE AND OBSERVATION

Fifteen thirteen-lined ground squirrels were initially captured between 22 Aug. and 2Sept. 2007 at Rosehill Cemetery in Berrien Springs, Michigan (41u55.97N, 86u20.47W) usingSherman live traps (9.0 3 7.5 3 23.5 cm) baited with oats and peanut butter. A resident catsubsequently killed two squirrels, and their collars (see below) were retrieved and placed ontwo additional animals captured 7 Sep. and 12 Oct. 2007. Traps were set opportunisticallyadjacent to burrows that we observed squirrels to enter, were checked every 0.5–1.0 h oncethey were set and were promptly moved to shade (if necessary) when a squirrel wascaptured. Captured animals were handled and released within 1 h after we noted theircapture.

2012 KISSER & GOODWIN: GROUND SQUIRREL WINTER BODY TEMPERATURES 397

Each ground squirrel was sexed, inspected for sores or lesions, and weighed to the nearestgram with hand-held hanging scales, and its capture-location coordinates were recorded.Each animal was fitted with a temperature-sensitive iBcollar data logger (2.8–3.1 g for loggerand collar; data loggers obtained from Alpha Mach Inc., Mont St-Hilaire, Quebec) set torecord skin temperature every 2 h. Data loggers were initially attached around the neck withthin wire; but after we observed one animal with irritated skin under the wire uponrecapture, we modified all collars upon first subsequent recapture to cover the wire withplastic insulation stripped from standard electrical wire. A unique insulation color was usedfor each day that we modified collars on recaptured squirrels, and this facilitated subsequentfield identification. Collars were uniquely numbered to allow firm identification at capture,and collar numbers always matched field identifications based on insulation color.

After ground squirrels were fitted with collars, we visited the colony 1–3 d/wk (except 9–14 Sept.) for, on average, 2.8 h/d (ranged from 0.5 to 7 h/d) until 1 wk after abovegroundactivity ceased (last visit 18 Nov.). Daily time at the colony (h/d) is a minimum estimate; itwas not recorded directly but was estimated from times of first and last sightings or capturesof collared animals. We recorded the presence and location of all collared animals that wereobserved and opportunistically recaptured collared animals to reweigh them.

We assigned ground squirrels to age cohorts (juvenile and adult) based on body mass atfirst capture in late Aug. or early Sept., using for comparison data presented by Hohn andMarshall (1966) for a colony in Minnesota. They recorded minimum adult body masses inAug. of ,160–170 g and maximum juvenile body masses of ,170 g. Thus, we conservativelyidentified squirrels that weighed less than 150 g in late Aug. or early Sept. as juveniles.

Beginning 24 Mar. 2008 when the first squirrel of the spring (not collared) was observedaboveground, the colony was checked for activity 3–5 d/wk until 1 d after the last of thecollared squirrels active during spring was recaptured (last visit 6 May). Because weestimated daily time at the colony from times of first and last sightings or captures, we donot have estimates before 4 Apr. on account of inadequate sightings (0–1 sightings/d).Beginning 4 Apr., we usually made .1 sightings/d, and spent, on average, 4.6 h/d (rangedfrom 0.5 to 9 h/d) at the colony.

We initially attempted to recapture collared ground squirrels using the same procedure asin fall, but this was often ineffective. Instead, we built a portable fence that was set uparound a burrow after a collared squirrel entered and placed a heavy board with attachedstring within the fence and adjacent to the burrow. When the squirrel emerged and movedaway from the burrow, the string was manually pulled to shift the board over the burrowopening, and the squirrel was captured with gloved hands. Within 1 h of spring capture,squirrels were transported 4.6 km to the laboratory where collars were removed andsquirrels were weighed. Because study animals were used in a broader study to examine howdental tissues reflect body temperature variation over winter, they were euthanized by rapidapplication of compressed CO2 into a closed chamber. All procedures were reviewed andapproved by the Andrews University Animal Use Committee (approved 21 Jun. 2007) andfollowed published guidelines of the American Society of Mammalogists’ Animal Care andUse Committee (Gannon et al., 2007).

ANALYSIS OF BODY TEMPERATURE DATA

Temperature data were downloaded from each data logger and transferred to a MicrosoftExcel spreadsheet. Data loggers were individually pre-calibrated by the supplier at threeknown temperatures (0.1, 15.0, 30.0 C), and calibrated temperature readings were all within60.2 C of known temperatures. The supplier provided a calibration routine specific for eachdata logger to translate raw values into temperature (C). Skin temperatures were plotted

398 THE AMERICAN MIDLAND NATURALIST 167(2)

against time and the resulting profile inspected for the timing of onset and termination ofthe heterothermal period and patterns of skin-temperature variation during the hetero-thermal period. We marked the commencement and termination of the heterothermalperiod by onset of the first deep torpor bout and arousal from the last deep torpor bout,respectively. Total time spent in the heterothermal period (d) was calculated from theseendpoints.

The number of torpor bouts during the heterothermal period was determined for eachground squirrel and the duration of each torpor and arousal bout recorded. The onset andtermination of bouts of torpor and arousal typically are defined by when body temperaturecrosses an arbitrary threshold, usually 30 C (Young, 1990; Michener, 1992; Buck and Barnes,2000; Zervanos and Salsbury, 2003; Karpovich et al., 2009; Zervanos et al., 2010) butsometimes a higher temperature (Lehmer and Biggins, 2005). We could not use thismethod to compare all squirrels because three study animals (2 males and 1 female) neverachieved skin temperatures $30 C during 1–3 well-defined arousal bouts. Thus, we followedan alternative published method (Hut et al., 2002): torpor-bout duration was calculatedfrom the recording just before the first drop in a sustained skin-temperature decline goinginto torpor until the recording just before arousal at the end of that torpor bout. Arousalbout duration was calculated from the recording just before the first increase in bodytemperature during arousal to the recording just before body temperature dropped with theonset of torpor. In addition, to facilitate comparison with previous studies, we comparedtorpor-bout durations obtained by both methods (paired t-tests) for five squirrels with allarousal bouts reaching skin temperatures $30 C.

We graphically explored seasonal trends in torpor-bout duration, minimum skintemperature during torpor (torpor depth), and arousal-bout duration by first binning,for each individual, each torpor and arousal bout to the month that includes its midpoint.Then, we calculated and plotted the mean monthly values per individual through theheterothermal period.

We compared male and female ground squirrels for duration and date of entry into andexit from the heterothermal period; number of torpor bouts during the heterothermalperiod; lowest skin temperature during hibernation; overall and monthly average torpor-and arousal-bout durations; monthly average minimum skin temperatures during torpor;and body mass at first capture (for squirrels first captured 22–27 Aug.). Body massesmeasured within 5 d of first torpor or final arousal were used as estimates of body mass atentry into and termination of hibernation, respectively. If both pre- and posthibernationbody masses were available for a single individual, we estimated mass loss during hibernationas a percentage of prehibernation mass.

We examined associations among torpor-bout duration, minimum skin temperature pertorpor bout, and soil temperature measured at ,10-cm depth beneath sod. Soiltemperatures were obtained from the closest weather station to record these data (Wanatah,IN, 74 km SW of the study site). Unfortunately, this station did not record soil temperaturesat depths .10 cm, which would be more relevant to the soil conditions experienced byhibernating squirrels. We also examined associations between prehibernation body massand Julian day, and between posthibernation body mass and number of days after finalarousal.

Graphical and statistical analyses were done with SPSS 19.0 (IBM, Armonk, New York)using non-parametric tests for sample comparisons due to small sample sizes. Male andfemale values were compared with a Mann-Whitney U-test, and monthly values werecompared with the Kruskal-Wallis test. Linear regression was used to estimate relationships


between correlated variables that co-varied linearly. In two cases (prehibernation body masspredicted by Julian d, and minimum skin temperature during torpor predicted by soiltemperature), these relationships were descriptive but were not evaluated statisticallybecause cases were not independent (all squirrels experienced multiple torpor bouts andsome were weighed multiple times). All differences were considered significant at P , 0.05.

RESULTS

All thirteen-lined ground squirrels collared in this study were juveniles in 2007 withanimals weighing 91–137 g at first capture (22 Aug.–12 Oct. 2007). Males and females firstcaptured 22–27 Aug. did not differ in body mass at initial capture (males: x 5 108 g, SD 5

13.2, n 5 9; females: x 5 101 g, SD 5 12.4, n 5 4; P . 0.4). Animals that survived tohibernation gained an average of 0.53 g/d during late summer and early fall (Fig. 1A; notevaluated for significance because cases were not independent). Animals with relatively lowbody mass at first capture tended to gain mass progressively (e.g., collared males 1 and 14,female 15); animals with average or greater-than-average body mass at first capture initiallygained mass but subsequently maintained, or even lost, body mass (e.g., collared male 6,females 3 and 4b; Fig. 1A). Three animals last captured within 5 d of entering theheterothermal period weighed 132–144 g at last capture (Fig. 1A).

Eight of nine ground squirrels (5 males and 3 females) recaptured in spring hadfunctional data loggers with overwinter skin-temperature records. Six of these eight squirrelswere last sighted aboveground 2–5 d before onset of torpor, three on the last day the colonywas observed before they became torpid. Two squirrels (male with collar 12, female withcollar 15) were last sighted 9 and 15 d, respectively, before onset of torpor, and they werenot seen during 2 and 5 observation days, respectively, between last sighting and onset ofheterothermy.

FIG. 1.—(A) Summer and fall body mass against capture date with individual growth trajectoriesindicated; linear regression predicts body mass from Julian date. (B) Body mass at spring captureagainst day after final arousal


In spring, five of eight squirrels with functional data loggers were first sightedaboveground 1–4 d after terminal arousal. The remaining three squirrels, all males (collars1, 6, and 14), were not seen aboveground for 8–16 d (3–6 observation days) after terminalarousal. Two of these males (collars 1 and 6) were seen sporadically over the first 1–2 wkafter first sighting (on 1 of 4 observation days for collar 1; on 2 of 10 observation days forcollar 6) before they were observed consistently aboveground.

All squirrels with functional data loggers in spring displayed a characteristic skin-temperature profile during the heterothermal period: a series of 11–22 torpor boutspunctuated by brief arousal bouts (Fig. 2). Male squirrels spent significantly less time in theheterothermal period than did females: they entered the first torpor bout later (not

FIG. 2.—Skin temperature versus time for individual Ictidomys tridecemlineatus and regional minimumdaily soil temperature at ,10-cm below ground surface beneath sod (measured 74 km SW of study site).Dates of entry into and termination of the heterothermal period are indicated by closed triangles, lastfall and first spring sightings by open triangles. The dotted line marks an episode of warm soiltemperature in early Jan. Number of days indicated at low but euthermic body temperatureafter hibernation


statistically significant), initiated final arousal significantly earlier and exhibited fewertorpor bouts (approached significance: P , 0.10) than did females (Table 1). Males andfemales did not differ in lowest skin temperature during hibernation, durations of torporand arousal bouts or proportion of the heterothermal period spent in torpor (Table 1).

Torpor bouts obtained in this study averaged 0–1.5 h shorter than bouts delimited withthe 30 C threshold (available for 5 squirrels). The difference was significant for collaredanimal 15 (paired t 5 23.5, DF 5 16, P , 0.01) but not for other squirrels (collar 4: t 5 0.0,DF 5 21, P 5 1.0; collar 6: t 5 21.1, DF 5 10, P 5 0.3; collar 13: t 5 21.4, DF 5 12, P 5 0.2;collar 14: t 5 20.2, DF 5 16, P 5 0.8).

Averaged by month, torpor-bout depth (Fig. 3A) and duration (Fig. 3B) varied sys-tematically and significantly through the heterothermal period (Kruskal-Wallis test statistic 5

44.4 and 41.2, respectively; P , 0.001, DF 5 6 for both variables): from shallow, short bouts inOct. to deep, long bouts in Feb. Average arousal-bout duration (Fig. 3C) showed no trendacross the heterothermal period (Kruskall-Wallis test statistic 5 6.0, P . 0.40, DF 5 6). In Mar.,average torpor bouts were always deep (Fig. 3A); but both average torpor and arousal boutsvaried markedly in duration (Figs. 3B–C). In Apr., torpor bouts were shallower and shorter(Figs. 3A–B). Males and females did not differ in torpor-bout depth or duration, or in arousal-bout duration, during any month [standardized Mann-Whitney test statistic by month andvariable (torpor-bout depth, torpor-bout duration, arousal-bout duration): Oct. (20.58,21.16, 20.58), Nov. (0.45, 21.34, 1.04), Dec. (20.15, 21.64, 0.30), Jan. (20.15, 20.45, 1.51),Feb. (20.74, 0.60, 0.77), Mar. (1.34, 21.04, 21.64), Apr. (21.34, 0.45, —); P . 0.10 in allcomparisons], even during Mar. when three males showed markedly shorter average torporbouts and longer average arousal bouts (Figs. 3B–C).

Across individual torpor bouts, regional minimum soil temperatures measured at 10 cmbelow ground surface accounted for 96% of variation in minimum skin temperatures pertorpor bout (R2 5 0.96, y 5 1.2 3 + 2.9; not evaluated statistically because cases are notindependent), a pattern also evident across monthly average values (Fig. 3A). An episode ofabrupt soil warming from 8–11 Jan. 2008 corresponded to an increase in torpid skin

TABLE 1.—Comparison of male (n 5 5) and female (n 5 3) juvenile Ictidomys tridecemlineatus onvarious attributes of the heterothermal period during hibernation

Male Female

Mann-Whitney U{x SD x SD

Date of first torpor 31 Oct. 12.9 10 Oct. 10.2 1.64Date of final arousal 28 Mar. 9.2 21 Apr. 1.5 22.24*Duration of heterothermal

period [first torpor to lastarousal (d)] 149.5 21.6 193.5 11.8 22.24*

Number of torpor bouts 14.8 2.7 20.0 2.6 21.99Minimum skin temperature

during hibernation (C) 1.4 .3 1.7 .1 21.65Torpor-bout duration (d)e 9.6 0.8 9.2 0.8 0.45Arousal-bout duration (h)e 15.8 3.5 12.9 1.1 1.04Proportion of heterothermal

period in torpor (%) 94.0 1.3 94.7 0.7 20.75

{ Standardized test statistic* P , 0.05e Based on mean value across the heterothermal period for each squirrel


temperature, or to arousal, in all individuals (Fig. 2). Duration of torpor scaled inversely withboth soil (not shown) and skin temperature, although the relationship was not linear (Fig. 4).

Three males (collars 1, 6, and 13) differed from other squirrels in multiple attributes ofthe heterothermal period. They initiated the first torpor bout late, terminated theheterothermal period early, exhibited 1–3 short torpor bouts (relative to skin temperature)in Nov. and experienced short torpor bouts (both absolute and relative to skintemperature) and long arousal bouts in Mar. (Figs. 2–4).

Two females captured within 5 d after final arousal weighed 80–81 g whereas one malecaptured 6 d after final arousal weighed 95 g (Fig. 1B). One female was weighed within 5 dof entering and terminating the heterothermal period (collar 4b), and she lost 39% of body

FIG. 3.—Seasonal trends (average per individual per month) in (A) mean minimum skin temperatureper torpor bout, (B) mean torpor-bout duration (d) and (C) mean arousal-bout duration (h). Notedifference in scale between (B) and (C). Mean regional minimum soil temperature (averaged across alldays during which individuals attained minimum skin temperatures) given for comparison in (A).Labeled data points in (B) and (C) indicate three collared males with short average torpor bouts and longaverage arousal bouts in Mar. Average monthly values across all males and females connected by lines


mass during hibernation. On average, ground squirrels gained ,1.5 g/d after final arousalalthough one male (collar 13b) probably gained weight more rapidly (Fig. 1B).

Immediately following termination of the heterothermal period in spring, four malesdisplayed relatively low skin temperatures for 2–13 d, followed by return to normal activeskin temperatures (Fig. 2). Two of these individuals were seen aboveground during thisinterval.

DISCUSSION

Free-ranging thirteen-lined ground squirrels alternated bouts of torpor with short boutsof arousal throughout the heterothermal period (Fig. 2) with average monthly durationand depth of torpor-bouts generally increasing from onset of the heterothermal period toFeb. and decreasing thereafter (Fig. 3). A similar pattern characterizes other obligatehibernators within Marmotini for which overwinter body temperatures have been obtainedunder field conditions (Wang, 1973, 1979; Young, 1990; Michener, 1992; Barnes and Buck,2000; Florant et al., 2000; Hut et al., 2002; Humphries et al., 2003; Zervanos and Salsbury,2003; Lehmer and Biggins, 2005; Buck et al., 2008; Frank et al., 2008; Lee et al., 2009;Zervanos et al., 2010). Duration of torpor varied inversely with minimum skin temperatureduring torpor (Fig. 4) and ambient temperature through most of hibernation. This isconsistent with previous studies of hibernation in captivity (Twente and Twente, 1965;Pivorun, 1976, 1977; Twente et al., 1977; French, 1982; Geiser and Kenagy, 1988; Geiser etal., 1990; Barnes and Buck, 2000; Buck and Barnes, 2000; Strijkstra et al., 2008) and the field(Michener, 1992; Barnes and Buck, 2000) at ambient soil temperatures .0 C, below whichanimals typically defend body temperature and decrease duration of torpor (Pivorun, 1976;Geiser and Kenagy, 1988; Buck and Barnes, 2000). Some species of Urocitellus tolerate skintemperatures [Richardson’s ground squirrels (Urocitellus richardsonii)–Michener, 1992] or

FIG. 4.—Torpor-bout duration versus minimum skin temperature during torpor. Relatively shorttorpor bouts of three collared males during Nov. and after 15 Mar. are indicated


even core temperatures below 0 C during torpor (arctic ground squirrels–Barnes, 1989), butwe have no evidence for this in thirteen-lined ground squirrels (lowest skin temperaturerecorded was 1.0 C).

The inverse relationship between duration of torpor and skin temperature broke downfor three of five male ground squirrels late in hibernation (Fig. 3B) when their torpor boutswere substantially shorter than expected based on skin temperatures (Fig. 4), a patternoften displayed by both male and female Columbian (Urocitellus columbianus) andRichardson’s ground squirrels (Young, 1990; Michener, 1992). Also, these three malesexhibited exceptionally long late-hibernation arousal bouts (Fig. 3C) as is common for free-ranging arctic ground squirrels (Buck et al., 2008) and woodchucks (Marmota monax–Zervanos and Salbury, 2003). Decrease in duration of torpor or increase in duration ofarousal late in hibernation appear to be endogenously controlled and may allow squirrels toassess environmental conditions more frequently in preparation for final arousal(Michener, 1992). We do not know why only three of five males, and no females, displayedthese patterns in thirteen-lined ground squirrels.

Skin temperatures closely tracked soil temperatures, measured regionally (but not locally)at 10-cm depth, throughout hibernation (Fig. 3A). A short episode of abrupt soil warmingin early Jan. reached the depth of hibernacula and elicited transient increases in torpid skintemperatures, or arousal, in all individuals (Fig. 2). Thus, hibernacula remained sensitive totransient but abrupt increases in winter temperature even though thirteen-lined groundsquirrels reportedly excavate their burrows to just below winter frost line and plug themwhen entering hibernation (Rongstad, 1965; Desha, 1966).

All thirteen-lined ground squirrels captured in our study were juveniles; apparently mostor all adults had entered hibernation before commencement of our study in late Aug.Adults of this species commonly cease aboveground activity by Aug. or Sept. with juvenilespersisting as late as early Nov. (McCarley, 1966; Clark, 1971), consistent with our findingthat juveniles commenced the heterothermal period in Oct. and early Nov. Adults typicallyenter hibernation before juveniles in marmotine hibernators (Michener, 1984) althoughlate persistence of adult males has been reported for arctic ground squirrels (McLean andTowns, 1981; Buck et al., 2008) and one population of thirteen-lined ground squirrels(Rongstad, 1965). Late entry of juvenile males into the heterothermal period [on average,3 wk later than juvenile females in our study (Table 1)] has been observed for Richardson’sground squirrels and may allow juvenile males to gain sufficient body mass to compete withadult males for breeding rights the following spring (Michener, 1992). We have insufficientdata to rigorously test this hypothesis, but the three squirrels with largest body masses at lastfall capture were all males (Fig. 1A).

Despite late onset of the heterothermal period in fall, juvenile male thirteen-lined groundsquirrels terminated heterothermy, on average, 3.5 wk before juvenile females in spring, andthey thus spent, on average, about 6.5 wk less time in the heterothermal period (149.5 dversus 193.5 d, respectively–Table 1). Richardson’s ground squirrels display a similarpattern: juvenile males terminate heterothermy, on average, several weeks before juvenilefemales and spend substantially less time in the heterothermal period (114 d versus 181 d,respectively, in one study season–Michener, 1992). Early spring arousal is common foryoung male ground squirrels that are reproductive after their first winter (reviewed inMichener, 1984), thus juvenile males in our study probably were reproductively mature inspring. In contrast, young males that remain nonreproductive after their first wintertypically end hibernation later in their first spring and thus spend substantially more time inthe heterothermal period [e.g., Columbian (Murie and Harris, 1982; Young, 1990) and


arctic ground squirrels (Buck and Barnes, 1999; Buck et al., 2008)]. Early spring arousalallows reproductive males to mature, establish territories and monitor the area for emergingfemales so that mating occurs soon after female emergence (Michener, 1984).

The majority of ground squirrels in our study (6 of 8) showed little lag between lastaboveground sighting in fall and the onset of torpor (#5 d), or between terminal arousaland first spring sighting (5 of 8; #4 d), but other individuals exhibited substantial lags [14–15 d in fall (a male and female), 8–16 d in spring (3 males)]. We are not confident thatthese lags indicate extended sequestration before or after the heterothermal period becauseseveral squirrels were not observed for 2–3 consecutive observation days prehibernation,and two of three males with substantial lags between final arousal and first abovegroundsighting posthibernation were observed infrequently for 1–2 wk after first observation. Earlyarousing males appear to have been relatively inactive before 1 Apr. although we did notquantify h/d spent on the colony early in the active season.

Perhaps consistent with low levels of aboveground activity early in spring, four of five malesexhibited relatively low skin temperatures for 2–13 d after terminating the heterothermalperiod (Fig. 2). We initially hypothesized this to represent male sequestration undergroundbetween termination of torpor and emergence from hibernation, a behavior reported forseveral species of Urocitellus (Columbian ground squirrels–Young, 1990; Richardson’s groundsquirrels–Michener, 1992; arctic ground squirrels–Barnes and Ritter, 1993). In these species,males, but not females, eat cached food for several days before emerging (Michener, 1992).This hypothesis was contradicted by our observation that two of these individuals wereaboveground during their episodes of low skin temperatures.

Alternatively, low skin temperatures after hibernation may reflect inadequate skin-collarcontact due to hibernation weight loss, but it is not clear why this would differentially affectmales. Variable skin-collar contact may cause skin temperatures to underestimate bodytemperatures by 0–8 C in active mammals, although skin temperatures more closely trackbody temperatures (62 C) in mammals curled up to conserve heat during torpor(Humphries et al., 2003). This may explain why skin temperatures sometimes did not reach30 C during arousal bouts within hibernation (Fig. 2).

Juvenile thirteen-lined ground squirrels in our study gained body mass, on average, lessrapidly late in the active season (,0.5 g/d from late Aug. to early Nov.; Fig. 1A) thanpreviously reported early in the season from Minnesota (,1.4–1.9 g/d, depending on year,between Jun. and late Aug.; Hohn and Marshall, 1966). Growth trajectories varied amongindividuals: mass tended to increase throughout fall for animals with below-average bodymass at first capture but tended to stabilize, or even decrease, late in the season for animalswith average or above-average body mass at first capture (Fig. 1A). The latter pattern iscommon for ground squirrels as they approach hibernation (Davis, 1976).

Overwinter weight loss estimated for one juvenile female thirteen-lined ground squirrel(39% of prehibernation body mass) was similar to weight loss reported for juvenile females ofRichardson’s ground squirrels [40–48% depending on season (Michener and Locklear, 1990;Michener, 1992)]. Animals captured within 10 d after final arousal all weighed ,100 g atcapture, but squirrels gained weight rapidly over the first 1.5 mo of the active season (Fig. 1B).

In summary, this paper incorporated an additional marmotine genus–Ictidomys–intocomparative studies of overwinter body temperatures among free-ranging hibernators.Thirteen-lined ground squirrels exhibited several universal features of hibernation:alternating bouts of prolonged torpor and brief arousal, with torpor depth and durationvarying systematically through the heterothermal period and inversely with groundtemperature. All study animals were juveniles; most adults probably immerged into


hibernation before our study commenced in late Aug. Compared to females, males enteredthe heterothermal period later, terminated heterothermy earlier, and spent significantly lesstime in the heterothermal period. Some males, but no females, exhibited exceptionallyshort torpor bouts and long arousal bouts late in the heterothermal period. We alsopresented preliminary data on body-mass changes before, during and after hibernation inthirteen-lined ground squirrels.

Acknowledgments.—Andrews University supported this research with a Faculty Research Grant (toHTG) that included a graduate research stipend (for BK). Wayne Spletzer and his crew allowed us touse the Rosehill Cemetery grounds as our study site. Shaun Kisser assisted with animal capture,collaring, and observation throughout this project. Two anonymous reviewers provided helpful, criticalfeedback on an earlier draft of this paper.

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SUBMITTED 9 FEBRUARY 2010 ACCEPTED 4 NOVEMBER 2011


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