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Torpor Use by Free-Ranging Pallid Bats (Antrozous pallidus) at the Northern Extent of Their Range

Daniela A. Rambaldini, R. Mark Brigham
DOI: http://dx.doi.org/10.1644/08-MAMM-A-029.1 933-941 First published online: 15 August 2008

Abstract

Torpor minimizes energy expenditure and water loss during periods of inclement weather, low prey availability, or both, and appears especially important in harsh environments such as deserts. We investigated use of torpor by free-ranging adult male pallid bats (Antrozous pallidus) at the northern limit of their range in the semiarid Okanagan Valley in British Columbia, Canada. We predicted that males would use torpor frequently during the active season and that ambient temperature (Ta) as well as nutritional condition (body condition index [BCI]) would affect torpor use. We expected roost microclimate to be conducive to daily heterothermy given that roosts had cool morning temperatures that increased in the afternoon. We used temperature-sensitive radiotransmitters to measure skin temperature (Tskin) of 8 bats from June to August 2003. Seven individuals used torpor each day (n = 54 tracking days) but not at night. Torpor duration increased as mean daytime Ta decreased albeit the relationship differed between individuals. There was no significant effect of individual on the relationship between minimum Tskin during torpor and Ta. BCI was significantly and inversely correlated with torpor bout duration. Mean daytime temperatures in rock crevice roosts approached 30°C and fluctuated less than Ta.

Key words
  • ambient temperature
  • arid habitat
  • arousal
  • body condition index
  • Chiroptera
  • heterothermy
  • rewarming
  • roost temperature
  • skin temperature

Torpor is used as an energy- and water-saving strategy, especially during periods of low ambient temperature (Ta), low food availability, or both (Geiser 2004; McKechnie and Lovegrove 2002). One ecological benefit of use of torpor by heterotherms in general, and bats specifically, is that it makes possible the exploitation of habitats where climate conditions are unfavorable and prey abundance may be limited. Thus, use of torpor may be a significant factor determining the limits of a species' geographic distribution, especially for populations inhabiting arid regions (Bozinovic and Marquet 1991; Lovegrove and Raman 1998) or latitudinal extremes of a species' range (Arlettaz et al. 2000; Bell et al. 1986). However, depression of metabolic rate is not without costs. In mammals, heterothermy can negatively affect growth and development of offspring (Hoying and Kunz 1998; Racey 1973; Wilde et al. 1999), inhibit spermatogenesis in males (Fietz et al. 2004; Michener 1992; but see Anand Kumar 1965), hinder digestion (Studier et al. 1976), suppress immune function (Burton and Reichman 1999), increase vulnerability to predation (Kokurewicz 2004; Radzicki et al. 1999), result in possible accumulation of sleep debt (Daan et al. 1991), and reduce synaptic efficacy (Strijkstra et al. 2003). The advantages of torpor vary between individuals of different sex, reproductive condition, nutritional state, and age (Burton and Reichman 1999; Hamilton and Barclay 1994; Racey and Swift 1981). Torpor should confer the greatest metabolic advantage to healthy, nonreproductive adults, especially during periods of inclement weather, low prey availability, limited supply of body fat (energy) reserves, or a combination of these (Geiser 2004).

The pallid bat (Antrozous pallidus, Chiroptera: Vespertilionidae) is a North American desert-adapted species that reaches the northern limit of its range in southern British Columbia, Canada. This species is considered rare and listed as Threatened in Canada (COSEWIC 2002). Little is known about its ecology or behavior in the northern part of its distribution. A. pallidus is known to use torpor under natural conditions as well as in the laboratory (Beasley and Leon 1986; O′Shea and Vaughan 1977; Trune and Slobodchikoff 1976; Vaughan and O′Shea 1976). However, the factors that influence the use of torpor by A. pallidus under natural conditions have not been investigated. We examined use of torpor by free-ranging adult males only because few female pallid bats have been captured in British Columbia (Sarell and Haney 2000). We hypothesized that as a result of inhabiting an arid environment at the northern limit of their distribution, and facing no reproductive costs, adult males would employ torpor frequently during the summer in a manner similar to other free-ranging vespertilionid species (Chruszcz and Barclay 2002; Cry an and Wolf 2003; Grinevitch et al. 1995; Hamilton and Barclay 1994; Lausen and Barclay 2003; Racey et al. 1987).

We predicted that males would use torpor each day and night, especially during wet or cool conditions (Geiser and Drury 2003; Lovegrove et al. 1999; Turbill et al. 2003); bats would use deep torpor (as defined in Hamilton and Barclay [1994]) during periods of low Ta (i.e., day or night Ta below average minima); the nutritional state of a bat, assessed using a body condition index (BCI—Speakman and Racey 1986), would reflect individual proclivity for heterothermy (Audet and Thomas 1997); use of torpor would be more strongly correlated with BCI than with Ta (Lane et al. 2004; Mzilikazi and Lovegrove 2002; Westman and Geiser 2004); and males would select cool day roosts with temperatures (Td_roosts) that rise in the afternoon to facilitate use of torpor and passive arousal, respectively (Hamilton and Barclay 1994).

Materials and Methods

Study area and bat captures.—We conducted our study in the southern Okanagan Valley of British Columbia during the summer of 2003. The Okanagan is a semiarid shrub-steppe ecosystem located between the western Cascade Mountains and eastern Rocky Mountains. We focused our fieldwork on the Nk'Mip (Osoyoos) Indian Band Reserve (49°7′N, 119°30′W). Mean daily maximum Ta from June to August in 2003 was 38.0°C (36.5–39.3°C), mean minimum Ta was 10.2°C (9.5–10.9°C), and average monthly precipitation was 5.6 mm (0.0–15.0 mm—Environment Canada, Osoyoos, British Columbia, Canada). Native vegetation in the study area was dominated by antelope brush (Purskia tridentata), sagebrush (Artemesia tridentata), rabbit brush (Bigelowia graveolens), Ponderosa pine (Pinus ponderosa), Douglas-fir (Pseudotsuga menziesii), prickly pear cactus (Opuntia polyacantha), and a variety of bunchgrasses (predominantly bluebunch wheatgrass [Elymus spicatus] and Idaho fescue [Festuca idahoensis]).

We captured bats using mist nets 10 m high and 6–12 m long, set approximately 0–30 cm above the ground. We affixed BD-2T temperature-sensitive radiotransmitters (Holohil Systems Ltd., Carp, Ontario, Canada) to the interscapular region of each captured male using a small amount of Skin-Bond surgical adhesive (Smith and Nephew United Inc., Largo, Florida). Transmitter mass (1.05 g) represented 3.9–6.2% of body mass. We are confident that individuals in our study were not significantly encumbered by the mass of the transmitter because pallid bats are known to glean large arthropod prey such as Jerusalem crickets, which can have a body mass of up to 4 g—approximately 20% of average body mass (see also Adam et al. 1994; Kalcounis and Brigham 1995). Before affixing transmitters, we clipped the fur from a small area of the interscapular region to expose the skin and to ensure the closest possible contact between the skin and the temperature sensor in the transmitter. All protocols were approved by the University of Regina Animal Care Committee and were in accordance with guidelines of the Canadian Council of Animal Care and the American Society of Mammalogists (Gannon et al. 2007).

Once we located a day roost used by a radiotagged bat, we programmed a Lotek SRX-400 scanning radioreceiver (Lotek Engineering Inc., Newmarket, Ontario, Canada) to record the skin temperature (Tskin) of each tagged male every 5 min while the bat was in the day roost. Data from the receiver were downloaded nightly after bats emerged. Transmitters emitted signals with a pulse rate directly proportional to the Tskin of the bat, and thus we converted the interpulse interval to Tskin based on a calibration curve specific to each transmitter. Transmitters were calibrated to ± 1–2°C by the manufacturer (Holohil Systems Ltd.). We obtained hourly Ta and daily precipitation data from an Environment Canada weather station in the town of Osoyoos, approximately 7 km southeast of the study area.

Definition of terms.—We used the definition of Barclay et al. (2001) for the threshold of torpor; however, we distinguished active skin temperature (Tactive) from emergence skin temperature (Temerg), which we defined as the skin temperature of a bat 15 min before emergence from the roost at night. We defined Tactive as the mean Temerg for the period over which the transmitter remained attached to the bat. Compared to the definition proposed by Barclay et al. (2001), this definition of Tactive delineates a less-conservative threshold for torpor, minimizes the underestimation of slight drops in Tskin (i.e., shallow torpor), and is less prone to the potential error caused by anomalous or unusually low recordings of Temerg. One caveat of our calculation of Tactive is that it is influenced by atypically high values of Temerg, which could occur during active arousal from torpor (Willis and Brigham 2003). Although the threshold Tskin for torpor was unique for each individual in our study, the pooled mean Tactive of bats was 33.6°C ± 0.3°C with a narrow range of 32.4–35.1°C.

A torpor bout was defined as any period during which Tskin remained at least 1°C < Tactive for more than 30 min. Any day during which use of torpor was observed by at least 1 bat was termed a torpor day. We characterized use of torpor by frequency, depth, and duration for each individual on each torpor day. We measured depth of torpor as the difference between Tactive and the minimum Tskin attained during a torpor bout. We measured duration of torpor bouts as the length of time that Tskin was at least 1°C < Tactive, and defined time spent in torpor as the proportion of time that a roosting individual was torpid. We differentiated shallow torpor, which was the period of time that Tskin was <10°C below Tactive, from deep torpor, which was the period of time that Tskin was >10°C below Tactive (Hamilton and Barclay 1994; see also Chruszcz and Barclay 2002; Grinevitch et al. 1995; Lausen and Barclay 2003). We defined the period of arousal from torpor, or period of rewarming, as the interval of time beginning when the Tskin of a torpid bat began to increase for at least 15 min and ending when Tactive was attained. We calculated the rate of arousal, or rate of rewarming (measured in units of °C/min), by dividing (ΔTskin-2 – Tskin-1)/t, where Tskin-1 was the Tskin at the onset of arousal, Tskin-2 was Tskin at the end of arousal, and t was the period of arousal from torpor. We considered morning to be the interval of time between a bat's predawn return to the roost and midday, and afternoon as the interval of time between midday and a bat's emergence from the roost. In contrast, scotophase began at sunset and ended at sunrise.

Skin temperatures and use of torpor.—Skin temperature data were collected from 8 adult males between 4 June and 27 August. Although the average tracking period for each bat was 20 ± 8.5 days (11–32 days), we obtained Tskin data of complete torpor bouts for a mean of 7 ± 3 days (3–12 days) from each individual.

In order to minimize noise, daily Tskin data for each bat were fast Fourier transformed using the single data point smoothing function of Origin 6.0 statistical graphing software (Microcal Software Inc., Northampton, Massachusetts). We then overlaid fast Fourier-transformed data on the original data set and visually evaluated the transformed data to ensure that they remained accurate representations of the original data. This was most often true (n = 52 of 54 torpor days). However, fast Fourier transformation yielded anomalous results in 2 cases, for which we used only the raw data in our analyses. Before conducting statistical analyses, we evaluated the normality of all data using Shapiro-Wilks test. Most data were normally distributed, although some contained 1–3 extreme values. We conducted analyses with and without the extreme values. For all tests, we set α = 0.05 and we report means ± 1 SE (range; n = number of bats or observations) unless otherwise stated. We used SPSS 12.0 Base for Windows and SYSTAT 10 (SPSS Inc., Chicago, Illinois) for all statistical analyses.

Environmental conditions and use of torpor.—To assess patterns of torpor use, we used repeated-measures analysis of variance (ANOVA) to determine the relationship between depth and duration of torpor bouts; to assess the relationship between Ta at the time a bat achieved its lowest Tskin during torpor and the observed variation in the minimum Tskin of the individual; and to investigate the relationship between torpor duration and mean daytime Ta. We used repeated-measures ANOVA because of the pseudoreplication intrinsic to our data. Torpor bouts are not necessarily a series of discrete events that occur over a continuous diel cycle, and our repeated measurements of the same individuals over time and under different conditions preclude the use of regular parametric tests. Homogeneity of variance was analyzed using Levene's test.

Body condition index and use of torpor.—To assess the influence of body condition on use of torpor, we calculated a BCI (mass/forearm length, multiplied by mean forearm to correct for differences in skeletal size) as a relative indicator of the fat reserves of each bat at the time of capture (Speakman and Racey 1986). All but 1 individual was captured either before feeding (i.e., at emergence) or soon after emergence, presumably after a short foraging period; 1 bat was captured approximately 90 min after the mean roost emergence time of the local pallid bats. Most bats were captured between 29 May and 1 July; however, 1 male, captured on 17 August, had an exceptionally high BCI, which was most likely due to his developed scrotal condition (Speakman and Racey 1986) and increased prehibernation body mass (Beasley et al. 1984). We analyzed the data with and without the BCI outlier (Ball 1998). Inclusion of the extreme value affected the outcome of statistical tests, so we report the results of our analysis of both data sets. We calculated Pearson's parametric correlation (r coefficient) to evaluate the relationship between BCI and depth and duration of torpor bouts. We also evaluated the correlation between torpor attributes and mean, maximum, and minimum daytime Ta on the 1st tracking day after the capture of each individual to determine if physiological or environmental parameters were more strongly correlated with use of torpor. To control for individual variation in use of torpor, we standardized our data by evaluating the relationship between torpor attributes and length of forearm (i.e., an index of physical size) for each bat.

Temperatures in roosts and crevices.—We recorded hourly temperatures within roosts (Troost) by inserting Thermochron iButton (Maxim Dallas Semiconductor Corp., Dallas, Texas) temperature loggers within accessible rock-crevice day roosts (d-roost; n = 2 horizontal and 2 vertical) and night roosts (n-roost; n = 1 rock crevice and n =1 tree). We compared these data with daily Ta and with temperatures recorded within randomly selected rock crevices not used as roosts (Tcrevice, n = 1 horizontal and 1 vertical). To minimize disturbance to the bats, we did not insert dataloggers into the actual roosting chamber, which was usually a recess that extended deep into the rock, but inserted dataloggers as deep into the roost entrance as possible (ranging from 15 to 60 cm) when no animals occupied the roost. These data reflect how roost temperatures fluctuated with Ta throughout the diel cycle and how buffered Troost was from Ta, but do not indicate how roost microclimate directly affected the daily thermoregulatory patterns observed in bats. We used ANOVA to compare monthly mean and range in Ta with vertical Td-roost and Tcrevice, horizontal Td-roost and Tcrevice, and Tn-roost, separately. We used Bonferroni post hoc tests to distinguish differences between variables. Data used in our ANOVA were tested for homogeneity of variance using Levene's test. To determine whether the orientation of day roosts was randomly distributed, we employed a V-test, which is a modified version of Rayleigh's test for circular uniformity (Fisher 1993; Zar 1996).

Results

Behavioral ecology of radiotagged bats.—During the day, males roosted in remote rock crevices (mean roost height ± SD = 80 ± 46.3 m; range: 3–150 m; n = 19 day roosts) in high cliff faces. Tagged and untagged A. pallidus appeared to roost alone, in small groups (2–20 bats), or gregariously (>100 individuals). Bats were loyal to roosting areas, but on average switched day roosts every 4 ± 0.6 days (1–13 days). Bats emerged from the day roost 60 ± 2.0 min (38–95 min) after sunset and returned 107 ± 11.3 min (26–325 min) before sunrise (n = 8 bats, 40 nights). Bats had 1 or 2 foraging bouts each night and total mean duration of nocturnal activity periods was 300 ± 114.8 min. Details for each tagged bat are provided in Appendix I.

Skin temperatures and use of torpor.—All bats used torpor (Table 1) during each tracking day (n = 54 days), with the exception of 1 individual. Different males exhibited different Tskin patterns on the same day (Fig. 1), and the same male responded differently on days with the same minimum Ta. Thus, at any given Ta, some bats entered torpor whereas some remained euthermic. There was no “threshold Ta” at which all individuals invariably entered torpor.

Fig. 1

Patterns of skin temperature (Tskin) of 2 adult male pallid bats (Antrozous pallidus) over the same 5-day period. The plot shows Tactive (—, at approximately 34°C), Tskin (•), and Ta (—). The dark bars along the x-axis indicate scotophase. Note in graph A that Temerg < Tactive on 3 nights and torpor duration exceeded 42 h on 1 cool day. Different torpor patterns were exhibited by the same bat over a series of days, but both bats used deep torpor (A, 5 days; B, 4 days).

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Table 1

Descriptive statistics for values defining the use of torpor, patterns of thermoregulation, and time budgets for male pallid bats (Antrozous pallidus) used in our study. T = temperature.

X̄ ± SERangen
Maximum euthermic Tskin (°C)35.6 ± 1.632.0–39.28 bats
Tactive (°C)33.6 ± 0.332.4–35.18 bats
Temerg (°C)34.2 ± 0.228.5–37.454 nights
Total duration of torpor (min)741 ± 50.1170–2520.73 bouts
Duration of 1st torpor bout (min)620 ± 70.135–2,52054 bouts
Duration of 2nd torpor bout (min)125 ± 19.130–28019 bouts
Depth of torpor (ΔTactive – Tskin [°C])7.8 ± 0.51.8–15.073 bouts
Minimum Tskin (°C)26.7 ± 0.518.1–32.754 days
Ta at time of minimum Tskin (°C)21.5 ± 4.812.4–31.854 days
Proportion of time in deep torpor (%)13.7 ± 3.10–73.173 bouts
Rate of arousal, 1st bout (°C/min)0.11 ± 0.010.03–0.454 bouts
Rate of arousal, 2nd bout (°C/min)0.10 ± 0.080.03–0.319 bouts
Time spent in day roost (min)1,149 ± 29.2910–2,52554 days
Proportion of roosting time in torpor (%)61.6 ± 3.0.0–10054 days
Return to day roost to 1st torpor bout (min)119 ± 18.6< 1–50054 days
Total time spent foraging per night (min)300 ± 114.80–52240 nights

Pooled mean torpor duration was 741 ± 50.1 min and mean depth of torpor was Tskin = 7.8°C ± 0.5°C below Tactive. The mean minimum Tskin attained during a torpor bout was 26.7°C ± 0.5°C. Bats spent an average of 1,149 ± 29.2 min in the day roost, approximately 78% of the diel cycle, and spent an average of 61.6% ± 3.0% of total roosting time in torpor. Mean Tactive did not differ significantly between individuals (F = 1.55, df. = 7, 47, P = 0.176) and on some nights (n = 6 bats on 13 [24.1%] of 54 nights), bats emerged from the roost with Tskin below Tactive (i.e., Temerg < Tactive; Fig. 1). The lowest Temerg recorded was 28.5°C, 4.1°C below the Tactive of the bat. Of the 8 bats we tracked to at least 1 night roost (n =40 nights), none used torpor during scotophase. We only recorded torpor in the day roost after the last, predawn foraging bout.

Bats entered either 1 (n = 8 bats) or 2 bouts of torpor (n = 6 bats) per day. The 1st torpor bout in a day was significantly longer than the 2nd (t = 7.20, d.f. = 71,P< 0.001; n = 6 bats) and began in the early morning (X̄ = 323 ±55.1 min after midnight), whereas second bouts most commonly began in late afternoon or early evening (X̄ — 331 ± 40.1 min after noon, range: 30–550 min). Bats entered torpor sooner on cool mornings (r = 0.75, P < 0.001) and the mean difference between Ta at sunrise and Tskin of torpid bats was 21.6°C ± 0.70°C.

Deep torpor was used on 35.2% of torpor days (n = 1 of 8 bats on 19 of 54 torpor days) and it comprised 13.7% ±3.1% of the total time all individuals spent in torpor (n = 8 bats). Deep torpor bouts were significantly longer than shallow bouts and when bats entered deep torpor, Temerg was significantly lower (Table 2). Daytime Ta was significantly higher on days when bats used shallow versus deep torpor, whereas total precipitation over a 24-h period was not. Rates of rewarming did not differ significantly between individuals (F = 1.94, df. = 7, 46, P = 0.09). Rate of arousal from the 1st torpor bout was not significantly different from the rate of arousal from the 2nd bout (t = 1.52, d.f. = 71, P = 0.15). Most early afternoon arousals coincided with rising Ta (i.e., passive arousal, n = 40 bouts) because Tskin increased as Ta increased (Fig. 2), whereas the Tskin of bats arousing from torpor bouts before emergence always increased independently of Ta (i.e., active arousal, n = 19 bouts). Overall, the rate of rewarming did not differ between the arousals we classified as active and those we considered passive (t = 0.24, d.f. = 57, P = 0.81; Fig. 3).

Fig. 2

Duration of torpor bout versus mean daytime ambient temperature (Ta). Repeated-measures ANOVA showed that duration of torpor increased as mean daytime Ta decreased (P < 0.001, r2 = 0.67), even though the relationship differed between individuals (P < 0.001). Individual bats are represented by different symbols and regression lines are shown for each bat.

Fig. 3

Examples of active and passive arousal. A) Active and B) passive arousal were distinguished based on visual evaluation of rising skin temperature (Tskin; ○) in relation to Ta (—, at approximately 34°C); Tactive (—). The dark bars along the x-axis indicate scotophase.

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Table 2

Outcome of paired-sample t-tests for differences in bouts of shallow and deep torpor. Significant differences are shown in bold.

Shallow torpor X̄ ± SEDeep torpor X̄ ± SEtPd.f.
Duration (min)596.2 ± 34.71023.8 ± 104.24.40<0.00151
Temerg (°C)34.1 ± 0.332.7 ± 0.65.19<0.00151
Mean daytime Ta (°C)23.6 ± 0.519.8 ± 0.7−4.600.00051
Ta at minimum
Tskin (°C)23.5 ± 0.717.5 ± 0.8-5.300.00051
Precipitation (mm)0.15 ± 0.10.23 ± 0.20.510.61830

Environmental conditions and use of torpor.—There was a significant effect of individual (F = 2.63, d.f. = 7, 44, P < 0.05) on the direct relationship between duration of torpor bouts and depth (F = 26.98, d.f. = 1, 44, P < 0.001, r2 = 0.64). Duration of torpor increased as mean daytime Ta decreased (F = 57.37, d.f. = 1, 44, P < 0.001, r2 = 0.67; Fig. 2); however, the relationship differed between individuals (i.e., significant difference between regression slopes; F = 4.40, d.f. = 7, 44, P < 0.001). Minimum Tskin during torpor decreased with Ta (F = 32.55, df. = 1, 44, P < 0.001, r2 = 0.67; Fig. 4), independent of individual (F = 1.82, df. = 7, 44, P = 0.11). Bats attained mean minimum Tskin 84.4 ± 26.7 min before midday (n = 54 days).

Fig. 4

Minimum skin temperature (Tskin) during torpor versus Ta. The minimum Tskin for all bats in torpor was lower on cooler days (P < 0.001, r2 = 0.67) and individual regression slopes (shown) are significantly different (P < 0.001). Individual bats are represented by different symbols.

Body condition index and use of torpor.—The mean ± SD body mass of males was 19.9 ± 2.94 g and mean forearm length was 55.7 ± 1.89 mm. The mean ± SD BCI was 19.9 ± 0.98. The mean number of days between the night of capture and the 1st day we collected data on use of torpor from each male was 1 ± 1.5 days (0–4 days). When we excluded the outlier male captured in August, BCI was significantly correlated with the total duration of all torpor bouts a bat employed that day (r = −0.77, P = 0.05), but not with torpor depth (P = 0.83). Environmental variables were not significantly correlated with any torpor attributes. When the outlier was included in the analyses, BCI was significantly correlated with both torpor depth (r = −0.76, P = 0.03) and duration (r =−0.89, P < 0.01), as was mean daytime Ta (depth: r = −0.74, P = 0.03; duration: r = −0.85, P < 0.01). Length of forearm was not significantly correlated with use of torpor for either data set.

Temperatures in roosts and crevices.—In June and July, mean daytime temperatures in a vertical day roost and an unoccupied vertical rock crevice were not significantly different from Ta (Table 3 a) or from each other, whereas both vertical Td-roost and Tcrevice were significantly warmer than Ta at night. Vertical Td-roost and Tcrevice fluctuated less than Ta in June. Mean temperatures in 2 horizontal day roosts were significantly warmer than Ta and an unoccupied horizontal crevice during the day (Table 3b) and at night, and Ta fluctuated more than both horizontal Td-roost and Tcrevice in July and August. The compass orientation of 13 day-roost sites had a significantly nonrandom direction (u13 = —0.26, P < 0.001). Eleven of the 13 roosts faced south. The mean (a) and median aspect angle were 121° and 113°, respectively. Both the tree Tn-roost and rock crevice Tn-roost were significantly warmer than Ta at night (Table 3c) and both Tn-roosts fluctuated concurrently with Ta. At night, both horizontal day roosts were warmer, and fluctuated less, than either night roost.

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Table 3

Analyses of variance showing the degree of thermal insulation of rock crevice day roosts (Td-roost, vertical and horizontal), night roosts (Tn-roost), and unoccupied crevices (Tcrevice), with respect to mean and range of ambient temperatures (Ta). Significant results are shown in bold.

JuneJuly
DayNightDayNight
a) Vertical Td-roost
X̄ TcreviceP = 0.18P = 0.20
X̄ TaF = 1.77, d.f. = 2, 56P = 0.18F = 52.09, d.f = 2, 56P < 0.001F = 1.97, d.f. = 2, 77P = 0.15F = 81.12, d.f. = 2, 77P < 0.001
Range TaF = 25.14, d.f. = 2, 56P < 0.001F = 9.39, df. = 2, 56P < 0.001F = 55.78, d.f = 2, 77P < 0.001F = 26.52, d.f = 2, 11P < 0.001
JulyAugust
DayNightDayNight
b) Horizontal Td-roost
X̄TaF = 48.91, d.f. = 3, 39P < 0.001F = 85.26, d.f. = 3, 39P < 0.001F = 19.20, df. = 3, 115P < 0.001F = 100.79, d.f = 3, 115P < 0.001
Range TaF = 76.74, df. = 3, 39P < 0.001F = 51.79, d.f. = 3, 39P < 0.001F = 131.47, d.f = 3, 111P < 0.001F = 64.95, d.f. = 3, 111P < 0.001
X̄ Tn_roostF = 109.49, df. = 3, 34P < 0.001F = 180.89, d.f. = 3, 59P < 0.001
Range Tn-roostF = 476.48, d.f. = 3, 39P < 0.001F= 13.15, d.f. = 3, 59P < 0.001
JulyAugust
c) Tn-roost X̄TaF = 43.79, d.f. = 2, 32P < 0.001F = 86.42, d.f.= 2, 44P < 0.001
Range TaF = 2.36, df = 2, 32P = 0.11F = 2.09, d.f. = 2, 44P = 0.14

Discussion

Consistent with our predictions, free-ranging adult male A. pallidus at the northern limits of their range used torpor on a daily basis. Despite the small sample of individuals, the consistent pattern of daily use of torpor by all males suggests that this is an important physiological adaptation for this species in British Columbia. Torpor bouts were longer and deeper on cool days, albeit the individual variability in use of torpor suggests that other factors, such as BCI, influenced use of torpor.

Individuals also exhibited substantial variation in skin temperature at the time of emergence, and bats sometimes emerged from the roost with Tskin < Tactive. These results support the logic of defining Tactive as the mean of Temergs, rather than the lowest recorded Temerg. A low Temerg suggests that bats emerged before arousing completely and possibly used heat generated by flight muscles to fully rewarm from torpor (Willis and Brigham 2003).

The Td-roost is known to affect thermoregulatory strategies in bats (Chruszcz and Barclay 2002; Lausen and Barclay 2003; Vaughan and O′Shea 1976). We found that torpid pallid bats regulated body temperature, maintaining Tskin well above ambient, even at low Ta. The day roosts we monitored were warm, with mean daytime Td-roosts approaching 30°C and Td-roost fluctuated less than Ta. Furthermore, the majority of day roosts had a south-facing aspect that would have facilitated warming. By selecting roosts with high, constant temperatures, it appears that male pallid bats reap the energetic benefits of shallow torpor every day and avoid the energetic cost of remaining euthermic.

Roost microclimate could partially explain the relatively low incidence of deep torpor we observed. Kurta and Kunz (1988) found that under laboratory conditions, adult male little brown bats (Myotis lucifugus) did not use torpor more often than lactating females, which suggests that spermatogenesis (which is initiated in late spring in bats inhabiting temperate biomes— Gustafson 1979) may impose constraints on males (Beasley 1986; Entwistle et al. 1998; Mzilikazi and Lovegrove 2002; but see Anand Kumar 1965; Wimsatt 1969). Deep torpor would be most beneficial when Ta and Td-roost are low, when food is scarce or fat reserves are limited, when passive arousal is possible, when reproductive fitness is not compromised, or a combination of these (but see Willis et al. 2006).

We conclude that male pallid bats employ an intermediate thermoregulatory strategy during the summer, exploiting shallow torpor on a daily basis to minimize energy expenditure and evaporative water loss, but avoiding the frequent use of deep torpor to minimize the potentially high energetic cost of arousal or to avoid any potential compromise for reproductive success (see also Hamilton and Barclay 1994). When Ta was particularly low, bats used torpor regardless of physical condition, but the size of fat reserves, time of year, or both appeared to influence how individuals employed torpor to meet their specific energetic demands.

Our study demonstrates that male pallid bats use torpor every day in British Columbia, although the relative importance of this survival strategy remains unclear. Understanding the ecology of torpor use by pallid bats in British Columbia will have implications for the management of this threatened species by providing information about energetics, characteristics of roosts and roosting habitat, and thermoregulation. Assessing use of torpor in reproductive females, determining how use of torpor varies between years and as a function of different roosts, and investigating use of torpor in populations at lower latitudes will help elucidate the importance of heterothermy for A. pallidus at the northern part of its range.

Acknowledgments

We are grateful for the generous financial support from an Natural Sciences and Engineering Research Council Postgraduate Scholarship-A to DAR and a Natural Sciences and Engineering Research Council Discovery grant to RMB, Brink/McLean Grassland Conservation Fund (The Nature Trust of British Columbia), Endangered Species Recovery Fund (World Wildlife Fund of Canada and Environment Canada), Habitat Conservation Trust Fund, Nk' Mip (Osoyoos) Indian Band, Pallid Bat Recovery Team (Canadian Wildlife Service and British Columbia Ministry of Environment), and Public Conservation Trust Fund. For their invaluable assistance we thank S. and R. Bardeck, M. Bracewell, S. Bryson, D. Cerenzie, O. Dyer, S. Falkenberg, M. B. Fenton, L. Friis, J. Hall, K. Hall, R. Hall, B. Hammond, B. Harro wer, M. Holm, S. Hureau, C. Lausen, D. Makortoff, S. Matheson, G. C. McKeown, P. Ord, L. Pica family, G. Rambaldini family, M. Sarell, D. Sharpe, J. Steele, Thomas family, B. White, M. Yao, Nk'Mip Desert and Heritage Centre, Osoyoos Desert Centre, and the Township of Oliver. We also thank G. G. Carter, F. Geiser, D. H. Ireland, M. B. Milam-Dunbar, R. Vinebrooke, T. H. Kunz, and 2 anonymous reviewers for reviewing earlier drafts of this manuscript and providing thoughtful suggestions.

Appendix I

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Details of data for tagged male pallid bats (Antrozous pallidus) used in this study. Abbreviations for the table are: BM, body mass; FA, length of forearm; DF, Douglas-fir; DR, day roost; OT, orchard tree; PP, Ponderosa pine; RC, rock crevice; RD, riparian deciduous. One male (905 L) was recaptured. All bats roosted in rock crevices during the day. Bats captured on 14 June and on 1 July were roosting together in the same crevice. Number of torpor days denotes the number of days for which we obtained skin temperature data of complete torpor bouts.

Bat band no.BM (g)FA (mm)Date of captureTime of capture (h)Site of captureNo. days trackedNo. torpor daysNo. day roosts usedFrequency of switching day roosts (X̄ ± SD, range)Type(s) of night roost used
902 L20.552.929 May2350Foraging habitat, antelope brush13343 ± 2.9, 1–7DR, RC
903 L19.053.014 June2213Emergence from day roost22945 ± 5.3, 1–11DR, RC
904 L18.556.014 June2213Emergence from day roost32375 ± 4.2, 1–12DR, PP, DF, OT
905 L17.055.614 June2213Emergence from day roost32675 ± 4.2, 1–12DR, RC, PP, DF, RD
906 L20.357.814 June2213Emergence from day roost19929 ± 3.5, 7–12DR, RC, PP
911 L18.757.61 July2231Emergence from day roost11910DR, RC
912 L19.355.31 July2157Emergence from day roost131210DR, RC
905 L18.655.31 July2204Emergence from day roost
913 L27.857.317 August2123Foraging habitat, antelope brush15444 ± 3.8, 1–9DR, RC, PP, DF

Footnotes

  • Associate Editor was Craig L. Frank.

Literature Cited

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