ORIGINAL PAPER

Markus Dietz Æ Elisabeth K.V. Kalko

Seasonal changes in daily torpor patterns of free-ranging femaleand male Daubenton’s bats (Myotis daubentonii )

Received: 26 April 2005 / Revised: 10 June 2005 / Accepted: 27 September 2005� Springer-Verlag 2005

Abstract Daily torpor can provide significant energy andwater savings in bats during cold ambient temperaturesand food scarcity. However, it may reduce rates of foetaland juvenile development. Therefore, reproductive fe-males should optimize development by minimizing timesin torpor. To test this hypothesis, the use of torpor byfemale and male free-ranging Daubenton’s bats (Myotisdaubentonii) during reproduction (gestation, lactation,and post-lactation period) was investigated in 1998 and1999. Temperature-sensitive radio transmitters were at-tached to the bats to measure skin temperature. Simul-taneously, ambient temperature was recorded. Whileboth sexes became torpid during daytime, male batsused daily torpor (>6�C below individual active tem-perature) significantly more often during reproductiveperiod (mean: 78.4 % of day time in May and 43 % inJune) than females. Female bats went into daily torpor,particularly in late summer when juveniles were weaned(mean: 66.6 % of daytime). Lowest skin temperaturesoccurred in a female bat with 21.0�C during post-lacta-tion. Skin temperatures of male bats fluctuated from16.8�C in torpor to 37.2�C during times of activity.There was a significant effect of reproductive period onskin temperature in females whereas mean ambienttemperature had no significant effect. However, meanambient temperature affected mean skin temperatures inmales. Our findings indicate that female Daubenton’sbats adopt their thermoregulatory behaviour in partic-ular to optimize the juvenile development.

Keywords Chiroptera Æ Myotis daubentonii Æ Torpor ÆThermoregulation Æ Skin temperature

Abbreviations DEE: Daily energy expenditure ÆTa: Ambient temperature Æ Ts: Skin temperature ÆPreg: Pregnant Æ Lac: Lactating Æpost-lac: Post-lactating

Introduction

Bats occurring in temperate zones are subject to a strongreproductive periodicity, reflecting seasonal variations infood supply. They hibernate in deep torpor and givebirth in summer when insect availability is highest (e.g.Hickey and Fenton 1996; Racey and Swift 1985; Rydell1992). In most temperate zones, vespertilionid bats matein late summer and early autumn when sperm produc-tion reaches a peak and females are in oestrus (Encar-nacao et al. 2004; Racey and Tam 1974). After mating,sperm is stored in the oviduct throughout the winter(Racey 1973). Pregnancy starts immediately after fertil-isation following hibernation. During pregnancy andlactation, energy demand of females grows continuously(Kurta et al. 1989; McLean and Speakman 2000). This isreflected in higher food consumption by lactating fe-males that increases, for example, by about 45 % inMyotis lucifugus (Anthony and Kunz 1977) and Myotisvelifer (Kunz 1974) from pregnancy to lactation. Foodavailability dictates timing of parturition, as shown byArlettaz et al. (2001) for the insectivorous mouse-earedbat Myotis blythii.

When food availability is low at low-ambient tem-peratures, bats in the temperate zone become torpidduring daytime in summer to reduce daily energyexpenditure (DEE) (Coburn and Geiser 1998; Hosken1997; Kurta 1990). Such torpor patterns as a reaction oflow-ambient temperatures and fluctuating food supplyare also known for other small mammals like lemurs(Schmid et al. 2000; Schmid 2000) and hedgehogs(Fowler 1988), as well as for birds (e.g. Kortner et al.

Communicated by G. Heldmaier

M. Dietz (&) Æ E. K.V. KalkoExperimental Ecology, University of Ulm,Albert-Einstein Allee 11, 89075 Ulm, GermanyE-mail: Markus.Dietz@tieroekologie.comTel.: +49-731-5022660Fax: +49-731-5022683

E. K.V. KalkoSmithsonian Tropical Research Institute,P. O. Box 2072, Balboa, Panama

J Comp Physiol B (2005)DOI 10.1007/s00360-005-0043-x

2001; Prinzinger et al. 1981). However, breeding femalesof mammals face an obvious dilemma, because milkproduction is less during torpor. This may considerablyslow down fetal development and postnatal growth(Eisentraut 1937; Racey and Swift 1981; Wilde et al.1995, 1999). Because of the brief gestation and theparticularly short lactation period at temperate lati-tudes, a delay of the development of juvenile bats re-duces their time to prepare for hibernation. It istherefore crucial that yearlings deposit enough fat re-serves in late summer to survive the winter (Ransome1968; Thomas et al. 1990).

So, we assume that breeding female bats optimiseprogress of reproduction by minimizing use of torporduring pregnancy and lactation. However, currentknowledge about thermoregulatory strategies of free-ranging bats during reproductive season is scarce andlimited to a few Nearctic bats, particularly to Eptesicusfuscus (Audet and Fenton 1988; Grinevitch et al. 1995;Hamilton and Barclay 1994; Lausen and Barclay 2003),Lasiurus cinereus (Hickey and Fenton 1996), and Myotisevotis (Chruszcz and Barclay 2002). Furthermore, skintemperature as a measure of torpor was mainly mea-sured while the bats were in the roost but not duringforaging. The purpose of this study was to investigatethermoregulatory behaviour of female and male Dau-benton’s bats (Myotis daubentonii) during pregnancy,lactation and post-lactation period.

We hypothesized that in order to optimise foetaldevelopment and milk production, females shouldmaintain a constantly high-body temperature duringpregnancy and lactation, as long as possible, while deepdaily torpor would be used predominantly in the post-lactation period. We expected that ambient tempera-tures would affect thermoregulation of reproductiveactive females less than actual reproductive condition. Incontrast, adult male M. daubentonii that are not repro-ductive active during early summer might be expected toreact more strongly to ambient temperatures by reduc-ing body temperature more often, especially at low-ambient temperatures during pregnancy and parturition,because they are not involved in the development andrearing of the young. However, as sperm productionstarts in late summer, thermoregulatory behaviour of themales should change accordingly.

Methods

Study area and animals

We radio-tracked 6 adult females and 5 adult males ofM. daubentonii during 1998 and 1999 (Table 1). Thefemales belonged to a maternity colony in the ‘‘Philos-opher-Forest,’’ a small deciduous forest in the city ofGießen in central Germany. Males and females live inthe same place and both roost in tree holes of Fagussylvatica, Quercus robur and Fraxinus excelsior. Thebats flew to their feeding grounds along a traditional

flight-path. The feeding grounds consisted of two pondsat a distance of a few hundred meters to the roost, andthe river Lahn at a distance of 2.5 km (Dietz and Fitz-enrauter 1996). Population structure and feeding ecol-ogy of the Daubenton’s bats in the ‘‘Philosopher-Forest’’ have been investigated since 1992; therefore,seasonality and habitat use are well known. We caughtbats with mist nets set in their flight-path or at theirroosts to attach radio-transmitters. The age of the batswas determined by evaluating the closure of the epiph-ysis (Anthony 1988) and by subsequent banding. Thereproductive status was classified as pregnant, non-pregnant, lactating and post-lactating according to themethods described by Racey (1988). Pregnancy was as-sessed by palpation of the abdomen directly after theemergence of the bats. A bare patch around the nipplesand milk expression were used as evidence for lactation.The onset and progression of spermatogenesis in maleswas assessed by the size of the testes and the distensionof the epididymis.

Telemetry

We used LB-2T temperature-sensitive radio-transmitters(Holohil Systems, Canada) with a weight of 0.5 g fortagging bats. The bats weighed between 7.1 and 10.7 gso that the transmitter corresponded to 4.6–6.8% oftheir body weight, which was slightly below and in a fewcases slightly above the 5% that is suggested for radio-tracking studies (see Aldridge and Brigham 1988). Alltransmitters were attached between the shoulder bladesof the bats with skin-bond to study skin temperature andtorpor behaviour (Barclay et al. 1996). The transmittersfell off after 3–8 days. During this time we monitored thebats continuously by ‘‘homing-in-on-the-animal’’ (Whiteand Garrott 1990) with the help of 2-element Yagiantennae and Yaesu receivers (FT-290RII) modified byWagener, Cologne (Germany). Pulse repetition rate ofthe transmitters was measured 1 to 4 times per hour, aslong as the transmitter stayed on the bat to determineskin temperature. The pulses for three 1-minute setswere counted, and then the average of the values wasdetermined and finally compared with a calibrationcurve provided by the manufacturer. Usually, we tagged2–3 bats simultaneously and monitored them with 2 or 3observer-groups. For this study, our total sample was1,114 recorded hours distributed over 45.5 bat-days and43 bat-nights. Daily ambient temperature (mean, minand max; resolution 1/10�C) was taken from records of astation of the German Weather Service near the ‘‘Phi-losopher-Forest.’’

The usefulness of temperature-sensitive transmittersfor measuring skin temperatures of bats in the field wasfirst demonstrated by Audet and Thomas (1996). Theyfound that externally attached transmitters accuratelyreflected core temperature. The difference betweenmeasured skin and body temperature was linearly cor-related with ambient temperature (Ta), but they also

found differences as high as 6�C at relatively high Ta

(>21�C). Barclay et al. (1996) confirmed that the read-ings were only slightly affected by Ta. Their study re-vealed that skin temperature was within 2.0�C of rectaltemperature in 35 out of 44 measurements with a max-imum deviation of only 3.3�C. Willis and Brigham(2003) also showed that core body temperature isslightly higher than Ts because external transmitterswere cooled by lower ambient temperatures. In ourstudy, we sometimes measured a decline of 2–3�C in skintemperature for a short time when the bats emergedfrom their roost. This may be the influence of the coolerambient temperature on the sensor when the bats startedto fly. However, overall differences between the last Ts

value measured in the roost before departure and thefirst value after leaving the roost were not significant(Wilcoxon Signed Rank Test, P=0.88).

Definitions

‘‘Active temperature’’ refers to the average skin tem-perature of a bat when it leaves the roost. We based ourvalues of active temperature on temperature measure-ments taken about 15 min before emergence. Definitionof torpor is controversial and many definitions havebeen proposed in different studies (Barclay et al. 2001;Geiser and Ruf 1995). We refer to Hamilton and Barclay(1994) and Grinevitch et al. (1995) for definition of dailytorpor to permit direct comparison of our data withother studies on bats. As recently reviewed by Willis andBrigham (2003), differences as high as 6�C have beenobserved between skin temperature and core bodytemperature influenced by ambient temperatures. So, wedefined that torpor occurs when skin temperature dropsmore than 6�C below active temperature.

We further defined bat day and bat night to comparedifferences in thermoregulation. A ‘‘bat day’’ started at6:00 am and ended at 9:00 pm in early summer duringpregnancy and lactation and at 8:00 pm in late summerwith shorter day length during post-lactation. A ‘‘batnight’’ is defined as the hours between daytimes and

corresponded to the time between astronomical sunsetand sunrise. With reference to the long-term studies inthe research area since 1992, we divided the investigationperiods (Table 1) into pregnancy, lactation and post-lactation periods. Female Daubenton’s bats give birth inthe first week of June and the young become fledged atthe beginning of July.

Statistical analyses

All results are given as mean ± SE. Individual skintemperatures (Ts) of females andmales were calculated asmean of all average values of Ts of the recorded bat days(Table 1). Individual skin temperatures were averaged tocalculate the mean skin temperature of the respectivereproductive period (pregnancy, lactation, post-lacta-tion). Influence of gender, different reproductive periodsof the year and variant ambient temperatures of indi-vidual skin temperatures were tested using General Lin-ear Model analysis (GLM). Backward stepwise selectionwas applied in order to exclude non-significant indepen-dent variables from the model. Active temperature is gi-ven as mean Ts for each individual bat prior to leaving theroost. Using these data, we computed the individualpercentage of daytime in torpor as well as the mean timefor all female and male bats. Kruskal–Wallis non-para-metric one-way ANOVA and Mann–Whitney U-testwere applied to test for significant differences in meantemperature data. The Spearman rank correlations werecalculated to test for significant correlations between skinand ambient temperatures. All statistical analyses wereperformed using statistical software (Statistica 6.0,SigmaStat, San Rsfael, CA, USA).

Results

Thermoregulation

For Daubenton’s bats GLM analysis (Table 2) revealed asignificant effect of gender, reproductive period and the

Table 1 Summary of radio-tracking data of 11 individuals of M. daubentonii sampled in central Germany during 1998 and 1999

Bat (Ring no.) Sex Age Mass (g) Reprod. status Tracking period Recorded bat days Recorded bat nights Hourly recordings

M16067 F ad 10.7 preg 2/V 5 5 120M10625 F ad 11.3 preg 2/V 5 5 120M19502 M ad 7.1 75% 2/V 5 5 120M19545 M ad 8.0 0% 2/V 3 3 81M16067 F ad 10.0 preg 2/V 4 4 112M19520 M ad 8.0 0% 2/VI 5 5 120M11872 F ad 9.5 lac 2/VI 4 4 98M08282 F ad 9.1 post-lac 2/VIII 3 3 72M16021 M ad 9.5 75% 1/VIII 4 4 96M11907 F ad 9.4 post-lac 1/VIII 4 4 96M25084 M ad 8.5 75% 2/VIII 3 3 79Total 45 45 1114

shown are the ring number of the bat, gender (F = female, M = male), age (ad = adult), mass in grams, reproductive status of thefemales (preg = pregnant; lac = lactating; post-lac = post-lactating) and males (epididymal filling in %), tracking period (half ofmonth/month of the year), recorded bat days and nights and hourly recordings of averaged temperature measurements

interaction of the two variables gender · period andperiod · ambient temperature (Ta) on skin temperatures(Ts). If we compare the individual temperature behaviourof the radio tracked bats, it is obvious that the progress indaily Ts does not follow a mechanism influenced byexogenous factors only. The comparison between apregnant female and an adult male during the period ofpregnancy shows that the male was heterothermwhile thefemale remained homeotherm with constant Ts’s (Fig. 1and 2a). Those bats were radio-tracked simultaneouslyunder similar ambient temperatures. The second exampleshows a second pregnant female in comparison to a post-lactating female in late summer. In both radio-trackingperiods, mean ambient temperature varied identicallybetween 14 and 18�C. During daytime, the post-lactatingfemale was regularly in torpor in contrast to the normo-thermic pregnant bat (Fig. 2b).

Time of arousal from daily torpor varied, but bothmale and female raised their temperature from lowvalues to active temperature during the last hour beforeleaving the roost (Fig. 2a,b). Sometimes, spontaneous

arousals during the second and third daytime periodsoccurred (male bat in Fig. 2a).

It seemed obvious to us that the reduction of thebody temperature is an individual behaviour, whichinitiated anew each day and so the daily Ts’s wereindependent of the Ts’s of the day before. Therefore, wedefined the results of individual bat days as independentdata. Figure 3 shows the mean Ts of all bat days of onereproductive period for both sexes, which was recordeddaily in the same time schedule. As hypothesized ther-moregulatory behaviour of the radio tracked Dauben-ton’s bats was different during the reproductive periodsin both sexes (Fig. 3, Kruskal–Wallis ANOVA:H=363.79, df=5, P<0.001). During pregnancy andlactation, reproductive females remained active in theday-roost and maintained their temperature at a highlevel (pregnancy: mean Ts of 34.8�C±0.4 with a rangefrom 30.7 to 39.5�C; lactation: 34.3�C ± 0.6 with arange from 27.9�C up to a maximum of and 36.3�C).Later in the year, when the young were weaned, bodytemperature of females decreased significantly after they

Table 2 Results of a GLM analysis to test the dependence of skin temperature (mean Ts) of Daubenton’s bats regarding gender, dailyambient temperature (mean Ta) and reproductive period

Effect SS dF MS F P

Intercept 1,967.262 1 1,967.262 2,452.272 0.000000Sex 238.185 1 238.185 296.907 0.000002Period 50.781 1 50.781 63.300 0.000210Mean Ta Pooled 0Sex · Period 169.651 1 169.651 211.476 0.000007Sex · mean Ta Pooled 0Period · Ta 12.694 1 12.694 15.824 0.007300Sex · Period · mean Ta Pooled 0Error 4.813 6 0.802

Fig. 1 Mean daily skintemperature (Ts) of all 11 radio-tracked female (F, n=6) andmale (M, n=5) M. daubentoniiduring different reproductiveperiods (preg pregnancy, laclactation, post-lac post-lactation period). Every dotrepresents one bat-day. Valueswere calculated as mean of allhourly recordings of Ts duringthe bat days

had entered the roost (mean Ts 26.2�C ± 0.9; Mann–Whitney U-test, P<0.001) with a minimum Ts of21.1�C.

In comparison, Ts of adult males varied considerablybetween night and day during pregnancy and lactationperiod. During this time, temperature dropped imme-diately after the males had returned to their day roost(pregnancy period: mean Ts 22.6�C ± 1.3; lactationperiod: mean Ts 27.1�C ± 2.1). The Ts fluctuated to amuch larger extent in males than in females, for exam-ple, during pregnancy period between 16.8�C in deeptorpor and 37.2�C when the males were active. However,thermoregulatory behaviour of males changed later inthe year when they maintained high temperatures duringthe first hours after they had entered the roost. Tem-peratures decreased only in the afternoon but they didnot reach the low levels that we had measured in malesduring pregnancy and lactation period. During post-lactation period, mean Ts of males differed significantlyfrom Ts of females and from Ts of males during preg-nancy and lactation period (Mann–Whitney U-test,P<0.001).

Use of torpor

There was a significant difference in the use of dailytorpor by females and males between reproductive andpost-lactation period (Kruskal–Wallis ANOVAH=36.15, df=5, P<0.001 and pairwise multiple

comparison). Tagged pregnant and lactating females didnot reduce their skin temperature more than 6�C belowactive temperature, whereas in the post-lactating period,females were on average torpid for more than half ofdaytime (60.0 and 73.3%, Table 3). Males were torpidduring pregnancy period for about two thirds of daytime(88.0 and 68.9%). Later in the year, males remainedmostly normothermic (Table 3).

Influence of ambient temperature

The relationship between skin temperature and ambienttemperature (Ta) was sex specifically assessed by calcu-lating the Spearman rank correlations between the twovariables. We found no significant influence of meandaily Ta on mean Ts of females (rs=�0.08, P=0.7,n=26) as opposed to male Daubenton’s bats wheremean Ts was positively correlated with mean Ta

(rs=0.67, P<0.01, n=20).We further assessed the difference of mean Ts—mean

Ta and minimum Ta to assess the stability of Ts in taggedfemale Daubenton’s bats in comparison to ambienttemperature by calculating the Spearman rank correla-tions between the two variables. The two variables werenegatively correlated (rs=�0.73, P<0.001, n=26). Incontrast, we found a positive correlation between thetwo variables (rs=0.64, P<0.01, n=20) in male Dau-benton’s bats. This indicates that body temperature ofroosting female Daubenton’s bats was to a large extent,

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aFig. 2 Hourly absolute skintemperatures (�C) of a pregnant(preg) female (F) and a male(M) M. daubentonii duringpregnancy period (a) withcomparison of a secondpregnant female and a post-lactating (post-lac) female (b).Dark bars represent bat nightsbetween dusk and dawn. Filledsquares indicate the time of abat in the day roost and opensquares the time it was in flight

constant and therefore, independent of variations inambient temperature as opposed to roosting maleDaubenton’s bats where body temperature fluctuates toa large degree with ambient temperatures.

Discussion

The purpose of this study was to compare thermoregu-lation behaviour of female and male Daubenton’s batsduring different reproductive periods. It is the first studywhere body temperature of both sexes of a free-rangingand tree-roosting insectivorous bat in the Palaearcticregion has been examined with temperature-sensitivetransmitters throughout roosting and foraging. OnlyAudet (1992) investigated skin temperatures of mouse-eared bats, Myotis myotis (Vespertilionidae) in the field,but measurements were limited to nursery colonies inattics. With our definition of torpor we take into con-sideration that ambient temperature slightly influencestemperature measurements of external transmitters (seeWillis and Brigham 2003). Compared with the possibleinfluence of handling in captivity (e.g. physiologicalstress, disturbance), radio transmitters are less invasivefor free-ranging bats and therefore, provide a betterestimate of the importance of torpor in the daily ther-moregulatory behaviour of small bats (Audet and Fen-ton 1988; Hamilton and Barclay 1994).

The results of our study support the hypothesis thatthere are significant differences between the thermo-

regulatory behaviour of female and male Daubenton’sbats in relation to reproductive status. Female Dau-benton’s bats avoided deep daily torpor during preg-nancy and lactation, whereas males became regularlytorpid for several hours per day with lowest skin tem-perature of 16.8�C. As a consequence, lower energyexpenditure achieved by the use of torpor may result inreduced foraging activities. This has been confirmed forDaubenton’s bats, as foraging times of male bats weresignificantly shorter during pregnancy period than thatof female bats (Dietz et al. submitted). As we did notfind a strict correlation between torpor and ambienttemperature throughout the breeding season, it must beunder active control of the bats in relation to theirreproductive condition.

Torpor in mammals and birds is characterised bylowering the set point for body temperature regulationto achieve a hypo-metabolic state in order to conserveenergy and water (e.g. Wang and Wolowyk 1988). Re-cent studies have demonstrated that the onset of non-seasonal daily torpor by small mammals and birds (e.g.Schmid et al. 2000; Kortner et al. 2001) and especially bybats can be initiated by food deprivation (Audet andThomas 1997; Hickey and Fenton 1996; Racey andSwift 1981) and by low-ambient temperatures (Grinev-itch et al. 1995). However, reproductive females have tobalance energy savings through torpor with costs ofdecreased juvenile development. Juvenile development isdepressed linearly, as the body temperature decreases(McNab 1982).

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Fig. 3 Mean hourly skin temperature (�C) of female (F) and male(M) M. daubentonii during different reproductive periods. Tem-perature values are given as mean ± standard error (SE) repre-senting the variance between the recorded bat-days. Data represent

14 bat days for 3 females and 8 bat days for 2 males duringpregnancy period, 4 and 5 bat days for 1 female and 1 male duringlactation period and 7 bat days each for 2 females and 2 malesduring post-lactation period

Table 3 Individual use of daily torpor in radio-tagged Daubenton’s bats during different reproductive periods represented as percentageof daytime (F = Female; M = Male)

Torpor (% of daytime) Pregnancy Lactation Post-lactation

F1 F2 F3 M1 M2 F4 M3 F5 F6 M4 M5

Mean 0 0 0 88.0 68.9 0 60 60 73.3 18.3 0Range 0 0 0 66.6–100 60–80 0 26.6–80 46.7–73.3 53.3–93.3 0–40 0n bat days 5 5 4 5 3 4 5 3 4 4 3

Assuming that the variance in Ts with drops of 4–5�Cbelow active temperature is not affected by Ta (pregnantfemales in Fig. 2), reproductive female Daubenton’sbats used shallow daily torpor for short periods of time.Even such slight reduction in body temperature can al-ready result in substantial energy savings by bats(Studier 1981; Webb et al. 1993). The same effect is alsodiscussed for larger mammals like ungulates (Arnoldet al. 2003).

Differences in the use of daily torpor by female andmale bats were also described for Nearctic E. fuscuswhere free-living bats of both sexes had been tagged withtemperature-sensitive radio-transmitters, as in ourstudy. Both sexes went regularly into torpor but malesused deeper torpor and were significantly more oftentorpid than reproductive females (Grinevitch et al. 1995;Hamilton and Barclay 1994). Lactating females weretorpid significantly less often than pregnant and non-pregnant females (Audet and Fenton 1988; Chruszczand Barclay 2002). Comparable results are described forpregnant and lactating females of European hedgehogs(Fowler 1988). It is reasonable that lactating femalesreduce time of torpor as much as possible because syn-thesis and secretion of milk is reduced with decreasedbody temperatures (Wilde et al. 1999). In contrast,assimilated energy requirement for lactation is muchhigher than for pregnancy (Kurta and Kunz 1988; Raceyand Speakman 1987).

Besides shallow torpor, another strategy to compen-sate for energy demands during reproductive period is tocluster in nursery colonies (Kurta et al. 1987; Neuweiler1993). Clustered females of M. lucifugus, for example,consumed only 19.9 ml oxygen per hour and per indi-vidual with a high-body temperature of 36.9�C. Incontrast, solitary females needed 32.5 ml oxygen perhour with low-body temperature of only 32.2�C (Kurta1986). In our study, we conclude that thermoregulationthrough sociality is an important factor that contributesto stable and warmer temperatures in the roosts forDaubenton’s bats. We found colonies of 20–40 Dau-bentons females during pregnancy and lactation,whereas the males mostly lived solitarily or in very smallgroups.

Selecting roosts with different qualities duringreproductive season can also support the thermoregu-latory behaviour of female bats. For instance, repro-ductive females of M. evotis and E. fuscus roosting inrock crevices chose roosts that differed in structure andthermal characteristics (Chruszcz and Barclay 2002;Lausen and Barclay 2003). Roosts used during lactationwere more thermally stable and remained warmer atnight compared to the shallow roosts used by pregnantand post-lactating females. Similar results were found inMyotis bechsteinii (Kerth et al. 2001). Females preferredtree roosts on colder nights especially before parturitionand after weaning, whereas they favoured warm roostsin bat-boxes during the post-partum period. It is likelythat the development of the young benefits fromthe warmer roosts. Female Daubenton’s bats in the

‘‘Philosopher-Forest’’ also switched between differentroosts during the breeding season. However, we did notfind obvious differences in the thermal properties of thetree holes used by Daubenton’s bats in our research area(unpublished data).

Thermoregulatory behaviour of female and maleDaubenton’s bats changed significantly during post-lactation period after the juveniles had been weaned.During this time, females in our study used daily torpormore often and for longer time periods than males. Thischange suggests that males prepare for mating andtherefore reduce periods of torpor to avoid the resultingnegative impact on spermatogenesis (Enwistle et al.1998; Jolly and Blackshaw 1987; Kurta and Kunz 1988).In our study area, sperm production started at the end ofthe lactation period. Epididymal filling continuouslyincreased in July and August and reached its peak in thesecond half of September prior to the migration to thehibernacula (Encarnacao et al. 2004).

We suppose that this period corresponds to the mainmating season of Daubenton’s bats. Although copula-tions in Daubenton’s bats have only been observed inwinter roosts (Grimmberger et al. 1987; Roer and Egs-baek 1969), we believe that it is likely that most copu-lation takes place already in late summer when theepididymes of males are fully developed and the animalsare active. We found males with filled epididymes in treeroosts together with adult females at the end of July.Becoming torpid during this time would reduce copu-lation frequencies because adult females that havegained enough weight for hibernation already leave theirbreeding areas at the beginning of September to settle inthe hibernation site (see Haarje 1994).

We conclude from our data on M. daubentonii thatdifferences in reproductive status, in particular of fe-males, explain the use of torpor better than exogenouosfactors like ambient temperature or food deprivationalone. Our results on the female bats correspond well tothose of other studies where the temperature behaviourof the nearctic E. fuscus was investigated (Audet andFenton 1988; Grinevitch et al. 1995; Hamilton andBarclay 1994). As in female Daubenton’s bats, torporwas used to the greatest extent after weaning. But femaleE. fuscus also used daily torpor during pregnancy inresponse to ambient temperatures below 9�C.

We cannot exclude that this difference is partly due tolow-sample size in comparison to studies on E. fuscusthat have been examined in greater numbers. However,in our opinion, it is more probable that different resultsreflect the diverse feeding preferences and foragingstrategies of the bat-species. For example, E. fuscusmainly feeds on Coleoptera, Hemiptera and Lepidopteraby aerial hawking in open spaces (e.g. Furlonger et al.1987; Hamilton and Barclay 1998). For such prey,nightly availability has been shown to vary widely withambient temperature (Kurtze 1974; Lewis and Taylor1964). On colder nights below 10�C prey availabilitydecreased and also the flight activity of bats foraging inopen space (Hickey and Fenton 1996; Racey and Swift

1985). As a result, the energy intake on colder nights islower than on warmer nights and so the use of torporshould be practised by individuals for whom the ratio ofcosts to benefits for thermoregulation was highest. Incontrast to E. fuscus and other species, ambient tem-perature has no significant influence on flight durationand capture attempts of reproductive females of Dau-benton’s bat (Dietz, in preparation). Moreover, taggedpregnant M. daubentonii hunted still at ambient tem-peratures below 5�C. Daubenton’s bats mainly feed onswarming chironomids (Beck 1995; Swift and Racey1983), capturing them close to the water surface (Jonesand Rayner 1988; Kalko and Schnitzler 1989). Appar-ently, insect density above water surfaces is less affectedby short-term low-ambient temperatures because of theheat saving capacity of the water.

Assuming thatM. daubentonii feeds more successfullyduring low-ambient temperatures compared to otherspecies, this may compensate for the loss of energy tomaintain high-body temperature. What is remarkable isthat Reynolds and Kunz (2000) found changes in thegastrointestinal tract of lactating, ecologically similarfemales of the Neartic M. lucifugus, which suggest thatincreased food intake and assimilation are the primaryfactors with which bats compensate for the increasedenergy demand during pregnancy and lactation.

Overall, we conclude that bats in the temperate zoneadapt their thermoregulatory behaviour primarily to theirreproductive status and the influence of ambient temper-ature is specifically different for gender and species.

Acknowledgements The authors gratefully acknowledge the help ofall the people who supported the time intensive field-work. We areparticularly grateful to Dr. Jutta Schmid, Dr. Jorge Encarnacao,Sabine Springer and two anonymous referees, who greatly im-proved the manuscript by valuable comments. Handling of Dau-benton’s bats was done under licence from the nature conservancydepartment of the Regierungsprasidium Gießen.

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