The Tradeoff Between Torpor Use and Reproduction in Little Brown Bats (Myotis Lucifugus)

J Comp Physiol B DOI 10.1007/s00360-012-0705-4

ORIGINAL PAPER

The tradeoff between torpor use and reproduction in little brown bats (Myotis lucifugus)

Yvonne A. Dzal • R. Mark Brigham

Received: 10 May 2012 / Revised: 17 August 2012 / Accepted: 24 August 2012 Ó Springer-Verlag 2012

Abstract In mammals, reproduction, especially for bats did not vary with reproductive condition, suggesting females is energetically demanding. Therefore, during the that even short, shallow bouts of torpor produce substantial reproductive period females could potentially adjust pat- energy savings, likely obviating the need to spend more terns of thermoregulation and foraging in concert to min- time foraging. Our data clearly show that torpor use and imise the energetic constraints associated with pregnancy reproduction are not mutually exclusive and that torpor use and lactation. We assessed the inﬂuence of pregnancy, (no matter how short or shallow) is an important means of lactation, and post-lactation on torpor use and foraging balancing the costs of reproduction for M. lucifugus. behaviour by female little brown bats, Myotis lucifugus. We measured thermoregulation by recording skin temper- Keywords Torpor Reproduction Bats Myotis ature and foraging by tracking bats which carried temper- lucifugus Foraging Thermoregulation ature-sensitive radio-tags. We found that individuals, regardless of reproductive condition, used torpor, but the Abbreviations patterns of torpor use varied signiﬁcantly between repro- MR Metabolic rate ductive (pregnant and lactating) females and post-lactating Tb Body temperature females. As we predicted, reproductive females entered Ta Ambient temperature torpor for shorter bouts than post-lactating females. Tsk Skin temperature Although all females used torpor frequently, pregnant Troost Roost temperature females spent less time in torpor, and maintained higher LMM Linear mixed model skin temperatures than either lactating or post-lactating ANOVA Analysis of variance females. This result suggests that delayed offspring AIC Akaike information criterion development which has been associated with torpor use AICC Bias-corrected Akaike information criterion during pregnancy, may pose a higher risk to an individual’s reproductive success than reduced milk production during lactation. Conversely, foraging behaviour of radio-tagged Introduction

Torpor is a temporary state of heterothermy defined by a Communicated by H. V. Carey. reduction in metabolic rate (MR) and other physiological processes (i.e. heart rate, breathing rate, body temperature Present Address: (T )) (Geiser and Ruf 1995; Geiser 2004). Although torpor Y. A. Dzal (&) b Department of Zoology, University of British Columbia, use results in a pronounced reduction in daily energy Vancouver, BC V6T 1Z4, Canada expenditure (Geiser 1994, 2004), there are other advanta- e-mail: [email protected]; [email protected] ges to torpor use that are often overlooked, such as accu- mulation of fat, reduction of water requirements, and sperm Y. A. Dzal R. M. Brigham Department of Biology, University of Regina, storage (for a full review see Geiser and Brigham 2012). Regina, SK S4S 0A2, Canada Supporting a high MR, typical of endothermic mammals, 123 J Comp Physiol B requires high levels of energy intake which is accom- 1994, 2004), assessments of torpor use in pregnant and plished through foraging. However, when food abundance lactating individuals are limited to a few mammals (for declines, the cost of maintaining an elevated MR may example, bats: Chruszcz and Barclay 2002; Willis et al. become prohibitively expensive. 2006; dormice: Fietz et al. 2005; dunnarts: Morton 1978; Body size has an important effect on an endothermic Geiser et al. 2005; lemurs: Randrianambinina et al. 2003; animal’s energy demand to maintain normothermy (for a mouse-opossums Bozinovic et al. 2005; mulgaras: Geiser review see McNab 2006). Small endotherms have higher and Pavey 2007; and prairie dogs: Lehmer et al. 2003). mass-specific MRs than larger ones to compensate for the Like most mammals, female Myotis lucifugus (little brown higher rate of heat and water loss in relation to their larger bat) invest substantial amounts of energy in reproduction. surface area (Geiser and Pavey 2007). The large surface Regulating Tb at high levels during the reproductive season area of small animals facilitates heat loss, therefore, is especially challenging for this species because not only maintaining Tbs at euthermic levels during times of low do they primarily eat insects, a food source whose avail- ambient temperatures (Tas) is energetically costly. Low ability is temperature dependent (Racey and Swift 1985; Ta not only increases the energetic costs of maintaining Speakman and Racey 1989; Park et al. 2000), but their euthermic Tbs but typically, it also decreases the abundance small and irregular body shape, and large wing surface area and availability of food. This energetic dilemma can be lead to high levels of heat loss. While this species has been further exacerbated during the reproductive season, the focus of numerous ecological and physiological studies, because in addition to the normal energetic costs of nor- and individuals are known to enter torpor both in the lab- mothermy, reproductive female mammals must dedicate a oratory and field (e.g. Fenton and Barclay 1980; Kurta substantial proportion of their energy budget to support et al. 1989), there are no data on the extent of torpor use by foetal growth, milk production, and nutrient acquisition free-ranging reproductive individuals. Thus, the aim of our (Farmer 2003). study was to assess the thermoregulatory and foraging To manage energetic constraints brought on by repro- strategies of M. lucifugus during the reproductive season. ductive condition or unpredictable weather, it should be We examined whether torpor patterns (frequency, duration, advantageous for endotherms to employ heterothermic and depth) varied among pregnant, lactating, and post- responses. Yet not all small endotherms use torpor when lactating females under natural conditions. Because faced with an energetic imbalance. This could be due to a reproduction is energetically costly, we hypothesised that tradeoff between using torpor for energy savings and the female bats would enter torpor on a regular basis, espe- costs associated with a reduction of nutrient absorption that cially when Ta, and consequently, food abundance coincides with declining Tb (Holloway and Geiser 1995), declined. Given that torpor use has been suggested to delay or the costs associated with daily arousal from torpor which foetal and juvenile development and decrease milk pro- have often been underestimated and may limit energetic duction, we predicted that pregnant and lactating females savings (Ko¨rtner et al. 2008). It has been suggested that would use shorter and shallower torpor bouts than post- torpor and reproduction are functionally incompatible (see lactating females. If pregnant and lactating females use Kenagy 1989), but more recently there has been accumu- torpor for shorter periods than post-lactating females then lating evidence which suggests this is not true. Torpor use they might be expected to make up the energy deficit by by females during the reproductive season has been foraging for longer periods (and presumably eating more) reported for some species from all three mammalian sub- than post-lactating females. By foraging longer, pregnant classes (Morton 1978; Chruszcz and Barclay 2002; Geiser and lactating females are more likely to acquire enough et al. 2005; Willis et al. 2006). However, it appears that energy to support the increased costs associated with when reproductive mammals do use torpor, they often use reproduction, while minimising the costs associated with it less than non-reproductive animals (see Landau and using torpor. Dawe 1960; Audet and Fenton 1988; Csada and Brigham 1994; Lausen and Barclay 2003; Nicol and Andersen 2006). Variation in torpor expression throughout the Methods reproductive stages of female mammals may, at least in some instances, be due to delayed foetal development Study site and species (Racey 1973; Krishna and Dominic 1982; Hoying and Kunz 1998), restricted or reduced milk production (Wilde We radio-tracked a total of 35 adult female M. lucifugus et al. 1999), all of which likely compromise reproductive from three maternity colonies from June to August of 2008 success. and 2009. Each colony roosted in a human-made structure Although torpor in mammals has been well studied located in Upstate New York: Fort Edward (43°090N, during the non-reproductive season (for reviews see Geiser 73°3400W), Greenwich (43°070N, 73°340W), and Willsboro 123 J Comp Physiol B

0 0 (44°21 N, 73°23 W). We captured bats by picking them off Torpor onset 1SE¼ ½ðÞ0:041 ðÞbody mass the walls of roosts, or using mist-nets or a harp trap set in ð1Þ þðÞ0:040 ðÞþðTa 31:083Þ known foraging areas or in proximity to maternity colonies.

All bats caught were banded with a metal split ring (to The Tsk threshold used to differentiate torpor from ensure we did not affix radio-tags to the same bat twice), normothermia ranged from 31.3 to 33.0 °C for different and we recorded reproductive condition and body mass individuals (pregnant 31.8–33.0 °C; lactating 31.3– (±0.1 g). To prevent overlap in our classification of 33.0 °C; post-lactating 31.4–33.0 °C). We classified a bat reproductive condition, we only affixed radio-tags to as being torpid anytime that Tsk fell below the torpor onset pregnant bats that were estimated to be at least 2 weeks temperature. We defined torpor duration as the total time from parturition (beginning of July, Kurta and Kunz 1987), bats spent in single or multiple torpor bouts on any given and only tagged lactating females that expressed milk and, day, while torpor depth was defined as the lowest had noticeably swollen mammary glands and exposed skin Tsk reached during a bout, with lower values of Tsk surrounding the nipples (Racey and Swift 1985). Pregnant representing deeper torpor. bats were captured between 1 and 17 June, lactating bats We recorded roost temperature (Troost) using DS1921G between 4 and 27 July, and post-lactating bats from 16 July Thermochron iButton (±0.5 °C, Dallas Semiconductor to 10 August in both years. Corp., Dallas, TX, USA) temperature data-loggers placed within each roost, and other ambient conditions (wind

Thermoregulatory strategies speed, precipitation, and Ta) recorded at a weather station closest to the roost (Fort Edward: 43°160N, 73°340W; We used temperature-sensitive transmitters to measure the Greenwich: 43°50N, 73°300W; Willsboro: 44°200N, 0 skin temperature (Tsk) of bats which is an indicator of 73°29 W; Weather Underground Inc. 2010), every 10 min. core Tb (Audet and Thomas 1996; Barclay et al. 1996; We collected data on ambient conditions to evaluate the McKechnie et al. 2007). We outfitted each captured bat effect of abiotic factors on thermoregulatory and foraging with a pre-calibrated LB-2NT transmitter (Holohil Sys- strategies of M. lucifugus for each day we tracked bats. tems, Carp, ON, Canada), which had masses of 0.35–0.42 g, and projected battery life of 8–21 days. Foraging strategies Captured bats had body masses ranging from 6.5 to 10.8 g, and thus transmitters represented 3.2–6.3 % of We tracked individuals each night beginning about 1 h body mass. We attached radio transmitters using surgical before sunset and completed tracking between 0100 h and glue (Torbot Bonding Cement, Torbot Group Inc., Cran- sunrise the next day. We defined a bat day as the period ston, RI, USA; or SkinbondÒ, Smith and Nephew United from when a bat returned to the roost after its last foraging Inc., Largo, FL, USA) to the skin between the scapulae bout of the night, until it departed from the roost to forage after trimming the fur with scissors. Once the transmitter the next evening. We tracked tagged bats using two mobile was securely attached (typically about 30 min), we telemetry receivers (AN-ADH 174, Lotek Wireless Inc., released individuals at the site of capture. We tracked bats Newmarket, ON Canada; and F172-3FB, AF Antronics on the day following transmitter attachment and each Inc., Urbana, IL USA) and a stationary telemetry receiver subsequent day they carried a functional transmitter to located at a base station in close proximity to known roosts. locate roosts, monitor Tsk, and measure the duration of The base station consisted of a 6.1 m tall antenna which foraging bouts. Once we located where tagged bats were allowed for the reliable detection of signals even in for- roosting, we deployed a Lotek SRX_400 data-logger/ ested areas. By scanning through the frequencies of all scanner receiver (Lotek Wireless Inc., Newmarket, ON, functioning transmitters, and reviewing the telemetry data- Canada) within their roost area. This device automatically logger output, we were able to ascertain the emergence scanned for tagged bats every 10 min and stored data time of all tagged bats to the nearest minute. After emer- about the transmitter pulse rate of individuals when they gence, we remained in constant contact with as many bats were in range. as possible each night. One observer always remained at We used the manufacturer-derived calibration curves the base station, while the other observers tracked bats to produced for each transmitter to estimate Tsk based on the confirm that bats were foraging. Foraging bats were dif- mean of ten inter-pulse intervals. Using an equation ferentiated from night roosting ones when a signal that developed by Willis (2007) specifically for bats, we were remained in a single area (over a body of water or in a able to assign the torpor onset Tsk threshold differentiating forest) for more than 10 min would intermittently get torpor from normothermia in the absence of direct MR louder and then quieter due to a moving transmitter data. antenna. Signals from night-roosting bats remained in one

123 J Comp Physiol B area for [10 min., but without any change in pulse inten- AIC. For each model, we included individual as a random sity. We determined foraging duration by following bats effect. Weather variables included in the models were through the night and excluded any period of time spent average daily wind speed, cumulative daily precipitation, night-roosting. We measured foraging duration for each bat and minimum daily Troost, or minimum Ta. We used the on a nightly basis until the transmitter ceased to function or bias-corrected version of the AIC (AICc) as a measure of fell off. model fit, because our sample to parameter ratio was less than 40 (Turkenheimer et al. 2003). AICc scores indicate Statistical analyses the amount of information lost in estimating what is occur- ring in the natural population with a model. We compared We used linear mixed models (LMMs) to determine whe- our models using an ANOVA, selecting the model with the ther or not reproductive condition affected torpor use and lowest AICc value as our final model. We used Akaike foraging activity of bats. We chose a LMM to account for weights to summarise the relative support for other com- repeated sampling of the same individual during the period peting models. We used Tukey’s post hoc multiple com- of transmitter attachment. We used multiple data explora- parison tests on each final model to assess how tion tools to determine if our data met the four assumptions thermoregulatory and foraging strategies were affected by of LMM (normality, homogeneity of variances, linearity, reproductive condition and roost site. All statistical analyses and independence; Quinn and Keough 2002; Zuur et al. were performed using R v. 2.15.1 (R Development Core 2009), and to identify variables that were highly correlated. Team 2012), and all results are presented as mean ± SE. Torpor duration and percent of the day spent roosting in torpor were highly correlated (r = 0.97), so we removed percent of roosting day spent in torpor from our analyses. Results

In addition, minimum daily Troost, and minimum daily Ta were highly correlated (r = 0.81). Given that we were Thermoregulatory strategies interested in how roosting conditions may have affected the duration and depth of torpor bouts, minimum daily Troost We monitored thermoregulation and foraging by 10 preg- was used in our analyses of factors related to torpor nant, 15 lactating, and 10 post-lactating M. lucifugus for a duration and torpor depth. Because insect activity is tem- total of 2,184 tracking hours (the sum of the number of perature dependent, and low Ta may indirectly result in hours each bat with a working transmitter was tracked) and reduced bat foraging efficiency, and increased foraging 157 bat days. Females from each reproductive condition duration, we used minimum daily Ta in our analyses of class used torpor; however, the pattern of torpor use varied foraging duration. (Fig. 1). Pregnant females used torpor the least, employing Ambient conditions influence thermoregulatory and thus a heterothermic response 60.6 % of the time (20 out of 33 daily expenditure in endotherms. Therefore, to determine bat days), while lactating females used torpor 90.9 % (50 thermoregulatory and foraging strategies of females that out of 55) and post-lactating females 97.1 % (67 out of 69). differed in reproductive condition we accounted for dif- Torpor duration differed significantly among females in ferences in ambient conditions, and the possible role they different reproductive conditions. The shortest period of may have in explaining our data. For each reproductive time a bat spent torpid was 50 min (a pregnant female) group (pregnant, lactating, and post-lactating), we built while the longest bout was by a post-lactating female models to explain (1) torpor duration; (2) torpor depth (18.2 h). Pregnant females used torpor for significantly

(based on Tsk); and (3) foraging duration. We examined shorter periods (133.1 ± 33.7 min; n = 10, N = 33 where compound symmetry, autoregressive with equal variances, n = individuals and N = bat days) than lactating and autoregressive with heterogeneous variances, as pos- (334.1 ± 50.8 min; z =-3.66, p = 0.0008; n = 15, sible models for covariance structure. We undertook an N = 55) and post-lactating females (510.7 ± 40.0 min; analysis of variance (ANOVA) to compare all models, z =-5.40, p \ 0.0001; n = 10, N = 69; Fig. 2). There selecting the covariance structure that had the lowest were no significant differences in the duration of torpor Akaike Information Criterion (AIC) value (autoregressive bouts between lactating and post-lactating females with heterogeneous variances for torpor duration and torpor (z = 2.18, p = 0.08; Fig. 2). depth, and autoregressive with equal variances for foraging Reproductive condition was also significantly related to duration). We fit four competing models to our data: (1) the depth (minimum Tsk) of torpor events. The lowest Tsk reproductive condition; (2) reproductive condition and we recorded, 12.5 °C, was for a lactating female and was weather variables; (3) reproductive condition and roosting *24 °C below the normothermic Tsk we recorded for site; and (4) reproductive condition, weather variables, and M. lucifugus (36.1 ± 0.02 °C). Pregnant females (25.4 ± roosting site; and then compared their performance using 1.2 °C; n = 10, N = 33) used shallower bouts of torpor 123 J Comp Physiol B

Fig. 1 Thermoregulatory patterns of a (a) pregnant; (b) lactating; and represents skin temperature (°C) of the bat, the solid grey line (c) post-lactating Myotis lucifugus for a single roosting day. Skin and represents the ambient roost temperature (°C), while the dashed grey ambient temperatures were recorded every 10 min on 09 June 2008, line represents the threshold deﬁnition for torpor onset. Black bars on 06 July 2009, and 08 August 2008, respectively. The black line the x axis indicate night

than both lactating (21.2 ± 1.0 °C; z = 2.81, p = 0.013; n = 15, N = 55) and post-lactating females (20.9 ± 0.7 °C; z = 2.84, p = 0.012; n = 10, N = 69; Fig. 3). There was no signiﬁcant difference in torpor depth between lactating and post-lactating females (z = 0.28, p = 0.96; Fig. 3).

Foraging duration

The amount of time spent flying on a nightly basis, which we assume represented foraging duration by individual M. lucifugus, ranged from 1 to 9 h and was not significantly influenced by reproductive condition. Pregnant females 270.8 ± 34.1 min (n = 10; N = 32) foraged for a longer time than lactating females 231.1 ± 24.2 (n = 15; N = 50) and post-lactating females 253.2 ± 57.1 min (n = 10; N = 61; Fig. 4) each night, but this trend was not significant. Fig. 2 Boxplot of the duration of torpor use by pregnant (n = 9, N = 33), lactating (n = 14, N = 55), and post-lactating (n = 10, Weather and roost conditions N = 69) Myotis lucifugus (n = individuals; N = bat days). The top and bottom of each box represent the upper and lower quartile, respectively. The median is represented by the horizontal solid line. Weather conditions (defined on the basis of average daily Open circles represent outliers, while the dashed vertical lines wind speed, cumulative daily precipitation, and minimum represent the maximum and minimum values (excluding outliers). daily T or minimum daily T ) and roosting site affected Different letters represent a significant difference a roost thermoregulation and foraging by M. lucifugus. Of these

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weather variables, torpor duration was signiﬁcantly related to cumulative daily precipitation (p \ 0.0001), while for-

aging duration was affected by minimum daily Ta (p = 0.018) and wind speed (p = 0.006). Minimum daily

Troost was only significantly related to torpor depth (p \ 0.0001). Roost site had no effect on torpor duration, but did have an effect on torpor depth, and foraging duration. Bats from Willsboro used deeper torpor than bats from Fort Edward (z = 2.44, p = 0.039) and Greenwich (z = 4.25, p \ 0.001). There was no significant difference in torpor depth between bats from Fort Edward and Greenwich (z = 2.25, p = 0.064). Bats from Willsboro foraged significantly longer than bats from Fort Edward (z = 2.59, p = 0.026). However, there was no significant difference in foraging duration between bats from Fort Edward and Greenwich (z = 0.53, p = 0.86), nor Greenwich and Willsboro (z = 2.30, p = 0.06). Fig. 3 Boxplot of minimum skin temperature (°C) of pregnant (n = 10, N = 33), lactating (n = 15, N = 55), and post-lactating Model selection with AIC (n = 10, N = 69) Myotis lucifugus. Minimum skin temperature was used to infer torpor depth (n = individuals; N = bat days). The top and bottom of each box represent the upper and lower quartile, Torpor duration was best explained by the model that respectively. The median is represented by the horizontal solid line. included reproductive condition and weather variables Open circles represent outliers, while the dashed vertical lines (Table 1). The best model explaining torpor depth and represent the maximum and minimum values (excluding outliers). Different letters represent a significant difference foraging duration was the model that contained reproductive condition, weather variables, and roost site (Table 1).

Discussion

Our results support the hypothesis that torpor and reproduction are not mutually exclusive processes. We demonstrate that pregnant, lactating, and post-lactating free-ranging M. lucifugus females commonly use torpor. However, the duration and depth of torpor bouts vary signiﬁcantly with reproductive condition. Varying costs associated with different stages of reproduction inﬂuence the manner in which animals use torpor. If there was no

cost of decreasing Tb, than we would expect all females to employ deep and long torpor bouts to maximise energetic savings, even when food is abundant. In addition, we found no evidence that foraging duration was significantly influenced by reproductive condition, or by torpor duration. This insinuates that regardless of a potential cost for offspring development and milk production, short bouts of torpor (and not increased foraging) is a common strategy Fig. 4 Mean foraging duration (min) by pregnant (n = 10, N = 32), lactating (n = 15, N = 50), and post-lactating (n = 10, N = 61) for balancing energy use by female M. lucifugus.We Myotis lucifugus (n = individuals; N = bat days). The top and suggest that ecological effects (weather variables and bottom of each box represent the upper and lower quartile, roosts) must be considered when determining the physio- respectively. The median is represented by the horizontal solid line, logical effects of reproduction on thermoregulatory and while the dashed vertical lines represent the maximum and minimum values (excluding outliers) foraging strategies of bats given that we found insufficient

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Table 1 Results of the AIC models for torpor duration, torpor depth, and foraging duration Response Model K AICc Akaike weight

Torpor duration Fixed effects: reproductive condition 2 1,600.51 0.0044 Random effects: individual Fixed effects: reproductive condition ? weather 5 1,590.03 0.8362 Random effects: individual Fixed effects: reproductive condition ? roost site 5 1,605.16 0.0004 Random effects: individual Fixed effects: reproductive condition ? weather ? roost site 6 1,593.31 0.1589 Random effects: individual Torpor depth Fixed effects: reproductive condition 2 668.41 2.382E-11 Random effects: individual Fixed effects: reproductive condition ? weather 5 629.37 0.0072 Random effects: individual Fixed effects: reproductive condition ? roost site 5 672.67 2.832E-12 Random effects: individual Fixed effects: reproductive condition ? weather ? roost site 6 619.50 0.9929 Random effects: individual Foraging duration Fixed effects: reproductive condition 2 1,466.72 0.0370 Random effects: individual Fixed effects: reproductive condition ? weather 5 1,462.90 0.2530 Random effects: individual Fixed effects: reproductive condition ? roost site 5 1,465.72 0.0613 Random effects: individual Fixed effects: reproductive condition ? weather ? roost site 6 1,461.00 0.6488 Random effects: individual

For each model, fixed and random effects, number of parameters (K), bias-corrected Akaike Information Criterion (AICC), and Akaike weight are given. For each response, models with the best fit are shown in grey evidence to consider reproductive condition alone as a and Barclay 2002; Lausen and Barclay 2003). However, we plausible explanation for torpor duration, torpor depth, and found that pregnant M. lucifugus spent more days normo- foraging duration. thermic, and used shorter and shallower torpor bouts than Despite the perception that the costs of torpor for suc- lactating females. Few studies have reported a higher fre- cessful rearing of young may preclude its use (Racey 1973; quency of torpor use and lower Tb’s among lactating Lewis 1993; Wilde et al. 1999), torpor substantially redu- female bats than pregnant female bats (Studier and ces daily energy expenditure, and its use has been recorded O‘Farrell 1972; Turbill and Geiser 2006). Although torpor during the reproductive season in endothermic animals use has been shown to delay foetal development, increased other than insectivorous bats (monotremes: Geiser and use during a particular period of pregnancy may be bene- Seymour 1989; Geiser 1996; Morrow and Nicol 2009; ficial, as it allows females to save energy, presumably for marsupials: Geiser et al. 2008 for a review; other placental re-allocation to the developing pup. Interestingly, its use mammals: Fowler 1988; Stephenson and Racey 1993; and during energetic shortfalls can also delay neonatal devel- birds: Calder and Booser 1973; Csada and Brigham 1994). opment and extend parturition until conditions are Our results suggest that in the wild, torpor use is energet- favourable for the survival of the mother and her offspring ically favourable and commonly used; however, repro- (Willis et al. 2006). ductive condition influences the frequency of torpor use Because lactation in most small mammals (i.e. M. lu- and the pattern of expression (i.e. depth and duration). cifugus) is more energetically costly than pregnancy (Kurta Generally, torpor patterns vary between reproductive et al. 1989; Farmer 2003), lactating females may benefit periods, with torpor being used more extensively during more from using longer and deeper torpor bouts than pregnancy than lactation (e.g. Studier and O‘Farrell 1972; pregnant females (Studier and O‘Farrell 1972). The energy Audet and Fenton 1988; Geiser and Masters 1994; Ham- saved during torpor can be redirected to milk production ilton and Barclay 1994; Grinevitch et al. 1995; Chruszcz rather than used to regulate Tb at normothermic levels. 123 J Comp Physiol B

However, lactating females face costs associated with lower energetic demands, yet they foraged for the same torpor use that post-lactating females do not. When length of time as pregnant and lactating females. We exposed to similar warm Ta’s, lactating Eptesicus fuscus suggest that post-lactating females consume more energy (big brown bat) use shallower torpor than post-lactating than is needed to meet their short-term energy balance, to females (Lausen and Barclay 2003). This suggests that build fat reserves in preparation for future periods of deep torpor may be particularly costly during lactation for energetic needs (e.g. migration and hibernation, Kunz et al. this bat. Although we found no differences in the depth of 1998). However, pregnant and lactating females may not torpor for lactating and post-lactating bats, lactating increase foraging duration (albeit higher energetic costs of females had signiﬁcantly shorter torpor bouts. While the reproduction; i.e. allocation of energy to offspring devel-

Tsk of lactating females decreased more than that of preg- opment and parental care), due to costs associated with nant females (but not post-lactating females), the deeper foraging itself. Foraging during a certain reproductive stage torpor episodes were employed for shorter periods of time may account for more than half of an individual’s energetic than in post-lactating females. By limiting the depth and balance (Speakman and Racey 1987; Kurta et al. 1989), time spent in torpor, lactating females must presumably be therefore, when foraging flight costs exceed energetic able to produce an adequate supply of milk for pups, while intake bats may reduce foraging duration. Overall, our data still saving a considerable amount of energy that short and suggest that instead of flying for longer and presumably shallow torpor bouts provide (e.g. savings of 11.2 cal/g/h, consuming more food, M. lucifugus rely on saving energy when Tb decreases by just 4° C; Studier 1981). to balance energetic requirements in the wild. Another possible means of reducing the costs associated In summary and in contrast to some previous evidence, with torpor use during the reproductive season may relate we found that torpor use and reproduction are functionally to the patterns of its use. Bats may reduce costs associated compatible and that reproductively active bats use torpor with torpor use during pregnancy or lactation by either regularly. While previous studies have reported examples taking advantage of roosting conditions, through social of torpor use during the reproductive season, there is a lack thermoregulation, or altering torpor patterns (i.e. torpor of consistency as to which reproductive groups use torpor, depth and/or duration). It has often been reported that the depth of torpor use, and when torpor is used among reproductive females cluster with others to produce warmer reproductive females. Therefore, species currently thought roosts, thus minimising thermoregulatory costs (bigger to strictly regulate Tb at high normothermic levels during clusters and warmer roosts are associated with less torpor the reproductive season may in fact employ torpor. We use; Chruszcz and Barclay 2002; Lausen and Barclay suggest that torpor use should be common among most 2003). Although we could not determine cluster size, small endotherms during the reproductive season when roosting site did influence torpor depth and foraging energetic demands are high, and fat reserves are small. duration. Thermal conditions varied in our study, and were Varying costs associated with different reproductive con- important in the models explaining our data. Previous ditions will influence the manner in which animals use laboratory studies have found that under identical thermal torpor. If there is no risk in allowing metabolism and Tb to conditions, thermoregulatory strategies of pregnant and fall, then all females should use deep extended bouts of lactating bats are the same, leading to the conclusion that torpor to maximise energetic savings, even when food is differences in thermoregulatory responses in the wild are abundant. Data on torpor use at different stages of each due to ecological and not physiological reasons (Turbill reproductive condition are needed to test predictions about and Geiser 2006; but see Lausen and Barclay 2003). We thermoregulatory strategies among different individuals suggest that if ecological conditions are not controlled for, and species. Ultimately, we need to understand whether variation of the frequency, duration, and depth of torpor there are physiological differences between individuals that must be assessed in the context of reproductive condition, use torpor and those that maintain a high Tb during the weather conditions, and roost site to determine if thermo- reproductive season and, if so, what selective factors regulatory and foraging strategies of wild animals are favoured this evolution. solely within the physiological realm, ecological, or both. Given that reproduction is energetically costly, females Acknowledgments We are thankful for the comments and insight may either increase energy consumption (to meet higher provided by the anonymous reviewers, as well as B. Fenton, J. Kil- gour, S. Lund, D. Riskin, C. Somers, K. Spadafore and N. Veselka. energetic demands of reproduction), and or decrease We thank C. and D. Bailey, P. Douglass and S. McPheeters for access energy use. Our data suggest that reproductive condition to bat colonies and D. Dahrouj, L. Hooton, T. McClenahan and had no effect on the duration of foraging by female M. lu- N. Veselka for their help in the field. This study was financially cifugus. Counter to our prediction, pregnant and lactating supported by General Electric, Natural Sciences and Engineering Research Council Discovery and Research Tools and Instruments M. lucifugus did not forage for longer periods of time than Grants and the University of Regina Faculty of Graduate Studies and post-lactating females. Post-lactating females should have Research. 123 J Comp Physiol B

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