Metabolic Physiology of Euthermic and Torpid Lesser Long-Eared Bats, Nyctophilus Geoffroyi (Chiroptera: Vespertilionidae)

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Year: 1999

Metabolic physiology of euthermic and torpid lesser long-eared bats, nyctophilus geoffroyi (Chiroptera: Vespertilionidae)

Hosken, D J ; Withers, P C

Abstract: Thermal and metabolic physiology of the Australian lesser long-eared bat, Nyctophilias geojfroyi, a small (ca. 8 g) gleaning insectivore, was studied using flow-through respirometry. Basal metabolic rate of N. geojfroyi (1.42 ml O2 g−1 h−1) was 70% of that predicted for an 8-g mammal but fell within the range for vespertilionid bats. N. geoffroyi was thermally labile, like other vespertilionid bats from the temperate zone, with clear patterns of euthermy (body temperature >32°C) and torpor. It was torpid at temperatures ฀25°C, and spontaneously aroused from torpor at ambient temperatures ฀5°C. Torpor provided significant savings of energy and water, with substantially reduced rates of oxygen consumption and evaporative water loss. Minimum wet conductance (0.39 ml O2 g−1 h−1 °C−1) of euthermic bats was 108% of predicted, and euthermic dry conductance was 7.2 J g−1 h−1 °C−1 from 5-25°C. Minimum wet and dry conductances of bats that were torpid at an ambient temperature of 15-20°C (0.06 ml O2 g−1 h−1 °C−1 and 0.60 J g−1 h−1 °C−1) were substantially less than euthermic values, but conductance of some torpid bats increased at lower ambient temperatures and approached values for euthermic bats. Metabolic rates of bats torpid at ambient temperatures >10°C and bats euthermic in the thermoneutral zone indicated a metabolic Q10 of 3.9. That high Q10 suggested that there may have been an intrinsic reduction in metabolic rate during torpor, in addition to down-regulation of thermoregulation (which accounted for most of the reduction in metabolic rate) and the normal Q10 effect

DOI: https://doi.org/10.2307/1383206

Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-154457 Journal Article Published Version

Originally published at: Hosken, D J; Withers, P C (1999). Metabolic physiology of euthermic and torpid lesser long-eared bats, nyctophilus geoffroyi (Chiroptera: Vespertilionidae). Journal of Mammalogy, 80(1):42-52. DOI: https://doi.org/10.2307/1383206 METABOLIC PHYSIOLOGY OF EUTHERMIC AND TORPID LESSER LONG-EARED BATS, NYCTOPHILUS GEOFFROYI (CHIROPTERA: VESPERTILIONIDAE)

DAVID J. HOSKEN AND PHILIP C. WITHERS

Zoologisches Museum der Universitiit Zurich-Irchel, Winterthurerstr 190, 8057 Zurich, Switzerland (DJH) Department of Zoology, The University of Western Australia, Nedlands, Western Australia 6907, Australia (peW)

Thermal and metabolic physiology of the Australian lesser long-eared bat, Nyctophilus geoffroyi, a small (ca. 8 g) gleaning insectivore, was studied usingftow-through respiro• metry. Basal metabolic rate of N. geoffroyi (1.42 rn1 O 2 g-I h-I) was 70% of that predicted for an 8-g mammal but fell within the range for vespertilionid bats. N. geoffroyi was thermally labile, like other vespertilionid bats from the temperate zone, with clear patterns of euthermy (body temperature >32°C) and torpor. It was torpid at temperatures :s25°C, and spontaneously aroused from torpor at ambient temperatures :::::5°C. Torpor provided significant savings of energy and water, with substantially reduced rates of oxygen con• sumption and evaporative water loss. Minimum wet conductance (0.39 rn1 O2 g-I h-I °C-I) of euthermic bats was 108% of predicted, and euthermic dry conductance was 7.2 J g-I h-I °C-I from 5-25°C. Minimum wet and dry conductances of bats that were torpid at an ambient temperature of 15-20°C (0.06 rn1 O 2 g-I h-I °C-I and 0.60 J g-l h-1 °C-l) were substantially less than euthermic values, but conductance of some torpid bats increased at lower ambient temperatures and approached values for euthermic bats. Metabolic rates of bats torpid at ambient temperatures > 10°C and bats euthermic in the thermoneutral zone indicated a metabolic Ql0 of 3.9. That high QlO suggested that there may have been an intrinsic reduction in metabolic rate during torpor, in addition to down-regulation of ther• moregulation (which accounted for most of the reduction in metabolic rate) and the normal Ql0 effect.

Key words: Nyctophilus geoffroyi, lesser long-eared bat, torpor, euthermy, metabolism, water loss, conductance, QlO

Energetic costs of endothermy are high ered and often approaches ambient tem• (French, 1992), and endotherms living in perature. Routine reduction in metabolic temperate climates are faced with a two• rate and body temperature in response to fold problem, seasonally cold temperatures decreased ambient temperature and acti vi• and a concurrent reduction in availability ty has been recorded in many bats inhab• of food (McNab, 1982). These problems iting temperate latitudes (e.g., Kurta and are especially relevant for small mammals Kunz, 1988; McNab, 1982; Webb et al., with their high ratio of surface area to vol• 1993). Torpor can reduce metabolic expen• ume and small reserves of fat (French, diture by >90% (Hosken, 1997; Hosken 1985). and Withers, 1997; Morris et aI., 1994; One way to survive periods of decreased Thomas et aI., 1990). Although most stud• productivity and cold is to decrease ener• ies of the metabolic physiology of micro• getic expenditure by daily or seasonal tor• chiropteran bats have investigated species por, during which body temperature is low- from Europe and North America (Findley,

Journal of Mammalogy, 80(1):42-52, 1999 42 1999 HOSKEN AND WITHERS-METABOLISM OF NYCTOPH1LUS 43

1993), there has been recent interest in the measured using flow-through respirometry. Bats physiology of Australian bats, especially were weighed to the nearest 0.1 g before each vespertilionids (Geiser et aI., 1996; Hos• experiment. They had not been fed for 12 h, ken, 1997; Hosken and Withers, 1997; which was sufficient for them to be post-absorp• Morris et aI., 1994). tive (Kovtun and Zhukova, 1994). Each bat was placed in a 0.81 glass chamber fitted with a cone We investigated the thermal and meta• of wire mesh from which the bat could hang. bolic physiology of an Australian vesper• The chamber was placed in a controlled-tem• tilionid, the lesser long-eared bat, Nycto• perature room (±2°C) at ambient temperatures philus geoffroyi in the laboratory. This is (Ta) from 5-40°C at five degree intervals. Am• a small (ca. 8 g) gleaning insectivore (Hos• bient temperature was measured in outflowing ken et aI., 1994), found throughout most air (Model HMP35B probe and HMI36 humidity of mainland Australia (Maddock and Ti• data processor, Vaisala OY, Helsinki, Finland). demann, 1995). Kulzer et ai. (1970) re• Air flow into the chamber (Vi) was controlled at ported that N. geoffroyi maintained a body 100 mlImin using a mass-flow meter (Model temperature ca. 2-4°C above ambient tem• 5871-A, Brooks Instrument B. V., Veenendaal, perature at 24°C when torpid, and Mad• Holland). This rate ensured that excurrent air dock and Tidemann (1995) reported it to had a content of O2 > 20%. Air entered at the base of the chamber and exited at the top, near enter torpor, but there are no detailed stud• the apex of the wire cone and the bat. Time re• ies of its metabolic physiology. We com• quired to reach 90% of a change in O2 concen• pare here rates of oxygen consumption and tration was ca. 5 min, reflecting the unidirec• carbon dioxide production, respiratory ex• tional flow of air and location of the bat near change ratio, rate of evaporative water the outlet of the chamber. loss, and thermal conductance for eutherm• Excurrent air was dried using anhydrous cal• ic or torpid bats over a range of ambient cium sulphate (Drierite) before passing through temperatures. one channel of a paramagnetic oxygen analyzer (Model OA184, Servomex Ltd., Crowborough,

MATERIALS AND METHODS United Kingdom) and an infrared CO2 analyzer Animals.-Body temperature and metabolic (Model Binos C, Hereus-Leybold G. M. B. H., rate were investigated for eight adult N. geof• Hanau, Germany). A GWBASIC program and froyi, two males and six non-pregnant females. Promax XT personal computer recorded the dif• Bats were captured near the Perrup Research ferential output of the O 2 analyzer (ambient air Centre (34°1O'S, 116°50'E), ca. 350 km S of minus excurrent air) and the analog output of the Perth, Western Australia. They were housed in CO2 analyzer via a RS-232 interface with a dig• outdoor flight-cages (5 by 2 by 2.2 m) at the ital multimeter (Model 1905, Thurlby Electron• University of Western Australia, under regimes ics Ltd., Cambridge, United Kingdom). V02 and of natural light and temperature. Bats were fed Vc02, corrected to standard temperature and mealworms (Tenebrio molitor), with occasional pressure for dry air, were calculated using sin• crickets (Teleogrylius) and bushcrickets (Re• gle-point samples taken every 30 s (torpid bats) quena verticalis). Mealworms were dusted with or every 5-30 s (euthermic bats). The faster rate powdered milk, and a vitamin supplement (Pen• of sampling for euthermic bats facilitated deter• tavite, Roche Consumer Health, Dee Why, New mination of steady-state V02 and Vc02 because South Wales, Australia) was added. Fresh water those bats tended to become torpid quickly at was supplied ad lib. Metabolic investigations in lower Ta. Absolute humidity of ambient and ex• autumn and winter 1996, began after animals current air was measured using two humidity had been in captivity for ca. 3 weeks. All bats probes (Model HMP35B probe and HMI36 hu• appeared healthy and maintained a stable body midity data processor, Vaisala OY, Helsinki, Fin• mass between ca. 6-10 g, averaging 8.0 ± 0.1 land), and the rate of evaporative water loss (SE) g. (EWL; mg g-I h-I) was calculated. Laboratory methods.-The rate of oxygen Calculations of steady-state V02, Vc02, and consumption (V02; ml O2 g-I h-I) and carbon EWL are based on principles outlined by With•

dioxide production (Vc02; ml CO2 g-I h-I) were ers (1977): 44 JOURNAL OF MAMMALOGY Vol. 80, No.1

V02 = [(VI' FlO,) - (VE' FEo,)] ·60/M, thermal conductance required conversion of ml O2 and g H20 to a common unit of joules. V co, = (VE . FEco,) ·60/M, and Eight bats were used throughout this investi• gation, and each bat was measured once to ob• EWL = [(VI'XEO,) - (VI'XIO,)] tain euthermic data and once to obtain torpid data at each temperature. However, final sample x 60/(1000· M), sizes varied because some data were excluded, where VE was the flow of dry air out of the due to problems in obtaining euthermic data at chamber (mVmin), FI02 and FIC02 were the frac• low Ta and torpid data at high Ta. SE. tional O 2 and CO2 concentrations of ambient air, Means are given with ± 1 Data were an•

FE02 and FEc02 were the fractional O 2 and CO2 alysed using t-tests, least-squares linear regres• sion and analysis of variance (ANOVA) with the concentrations of air out of the chamber, XI02 Student-Newman-Keuls (SNK) multiple com• and XE02 were the absolute humidity (mg/l) of ambient and excurrent air, and M was the body parison test. We used Bartlett's test for homo• mass of the bat. VE was calculated as VI . (1 - geneity of variance, and only mention in the text where it was significant, indicating heterogene• FI02 - FEc02)/(1 - PE02 - PEco). The O2 and ity of variance. ANOVA is robust even if there CO2 analyzers were calibrated to 0.2095 and 0 respectively using ambient air. is heterogeneity of variance, especially if sample Data for torpid bats were collected during the sizes are nearly equal (Zar, 1984). A significance day, but data for euthermic bats at low Ta were level of 0.05 was used. For regression analyses usually collected at dusk. Bats were kept in the when there were two different relationships of the Y value on X, a critical breakpoint (X value) metabolic chamber until a steady state of V02 , was calculated by dividing the data into two Vc02, and EWL had been reached (ascertained visually from graphs displayed by the comput• sets; those were regressed separately to mini• er). This was ~2 h for torpid bats and ~20 min mize residual sum of squares pooled for two re• for euthermic bats. It was essential to ensure that gressions (Withers, 1980; Yeager and Ultsch, 1989). bats had attained a steady state of V02, Vc02, and EWL, because body temperature (T b) was recorded at the end of each experiment, and it RESULTS was assumed that that represented the actual Tb Bats adjusted well to the experimental when other data were collected. At least 40 min protocol and were typically at rest during of sampling for torpid bats in steady-state V02, experiments, perched in their normal roost• ~1O Vc02 , and EWL, and min of sampling for ing posture at the apex of the wire cone euthermic bats, were used to calculate the V0 , 2 near the outlet. There were no significant Vc02, and EWL. The Tb of each bat was record• differences in T b of torpid or euthermic ed :545 s of removal from the chamber by in• serting a fine thermocouple 1 cm into the ani• male and female bats at any Ta for which mal's rectum. Data were discarded if insertion comparisons were possible. As a result, data of the thermocouple took ~45 s, if the bat had from both sexes were combined in subse• urinated or defecated in the chamber, or if the quent analyses. bat remained active. Body temperature.-Nyctophilus geof• Wet thermal conductance (Cwe,; ml O2 g-I h-I froyi is thermally labile with a clear di• °C-I) was determined as Vo/I1T, where V02 was chotomy in T b of euthermic and torpid bats I measured in ml O2 g-I h- and I1T was (Ta - at low Ta (Fig. la). The distinction between T b)' We retained fundamental units of measure• T b of euthermic and torpid bats is less clear ment of V0 (ml O ) for wet thermal conduc• 2 2 at higher Ta, but Speakman's (1988) crite• tance. Dry conductance (C ; J g-I h-I °C-I), in dry rion of Tb 26°C for torpor separated tor• contrast, was calculated as (MHP - EHL)/I1T, < where MHP was metabolic heat production (J pid and euthermic bats, except for one tor• pid bat with a Tb of 26°C at a Ta of ca. 24°C. g-I h-I; calculated from V02 assuming 20.1 Jlml

O2) and EHL was evaporative heat loss (J g-I There was considerable variation at most T h-I; calculated from EWL assuming a latent heat in Tb of bats that were euthermic (Fig. la)~ of vaporization of 2,300 JIg). Calculation of dry Nevertheless, below a Ta of 29.5°C, the crit- 1999 HOSKEN AND WITHERS-METABOLISM OF NYCTOPH1LUS 45

40 a ture, as well as after >3.5 months. The E ° ~ slope of neither regression line was signif• (I) "© B'; ~ '?fj "- 30 ~ icantly different from zero (r < 0.43, P > ::::s '" ° ra ° ° I 0.11, n = 8). -"- (I) , c. 20 °01 Nyctophilus geoffroyi became torpid at Ta E ., of 24.2°C (Tb = 26.0°C) down to 5.7°C (Tb ~ oe f 8.5°C; Fig. la). Bats were able to rewarm >- 10 '" = "C i 0 spontaneously from the lowest experimen• III tal temperatures. The Tb of torpid bats was 0 significantly related to Ta (r = 0.94; n = euthermic 0 ~ b 0 33 measurements of eight bats): Tb = 4.9 :.c: torpid (Tb-Ta>5 °Cl 0 10 (±0.57) + 0.95 (±0.04) Ta. At all experi• "Cl torpid (Tb-Ta<5 °Cl • ON 0 mental temperatures, the range in T b of tor• 0 . 0 pid bats was high, ca. 5°C, and this varia• 8 0 0 0 I tion was partly mirrored in the data for V0 2 (I) ra 0 (Fig. 1b), for which bats with dT > 5°C 0::- <8 c:: 6 generally have a higher V02• There was no 0 0 :;:; consistent relationship between the pattern c. 0 E of Tb for individual bats when euthermic or ::::s 4 til torpid over the whole range of Ta, i.e., bats c:: 0 0 with the highest T b at one T a may have had U 0 c:: 2 o 0 the lowest Tb at another Ta. (I) 0 Cl '0 0 ~ Metabolic rate.-The V02 varied with Ta >- >< ~ • and also displayed a clear euthermic-torpid 0 0 •• 0 10 20 30 40 dichotomy (Fig. 1b). Data for euthermic Ambient Temperature ee) bats are typical of an endothermic homeo• therm, with a linear increase in V0 2 as Ta FIG. I.-The relationship between a) body decreases below 34°C (the critical point for temperature and ambient temperature and b) the two regressions), with variation in Ta metabolic rate and ambient temperature, of Nyc• accounting for 91 % of the variation (r = tophilus geoffroyi when euthermic, torpid but 0.91; n = 56 measurements of eight bats): thermoregulating (AT > 5°C), and passively tor• VOz = 10.14 (±0.24) - 0.268 (±0.012) Ta. pid (AT < 5°C). The slope of that line, 0.268 ml Oz g-l h-l, was an approximate measure of Cwe! but ical point for separate regressions of T b at should be interpreted with caution because low and high Ta, the T b of euthermic bats of large variation in Tb and non-Newtonian (31.6 ± 0.2°C) was independent of Ta effects (McNab, 1980); for example, the (slope of 0.034 was not significantly differ• line below the critical point intercepts the ent from zero; r = 0.03; n = 40 measure• Y-axis at 37.9°C not the euthermic Tb of ments of eight bats). Tb was elevated at 31.6°C. The V0 2 of euthermic bats signifi• higher Ta of 35°C (Tb = 35.9°C ± 0.3, n = cantly differed between 30°C (2.1 ± 0.2) 8) and 40°C (Tb = 38.7 ± 0.3°C, n = 8). and 35°C (1.4 ± 0.1 ml O2 g-l h-1) and To investigate possible effects of captiv• 30°C and 40°C (1.6 ± 0.1) but not between ity on the ability of euthermic bats to ther• 35 and 40°C (F = 8, dj = 2,21; P < 0.05). moregulate, we used two linear regressions We consider V0 2 at 35°C to be the best es• of d T and time after capture (range = 25- timate of basal metabolic rate (BMR), be• 110 days) at Ta of 30 and 35°C. These am• cause it is the lowest mean value at a Ta bient temperatures were chosen because close to the breakpoint temperature. they included data measured soon after cap- The V02 of torpid bats was always well 46 JOURNAL OF MAMMALOGY Vol. 80, No.1

12 1 :.: • euthennic (T b < T a) h- °C-l. When bats were heat-stressed and "", • euthennic (T b > T a) 010 o torpid • Tb < Ta, VOz tended to increase (by a QIO I effect), so those data were not included in fi 8 , iii: the regression. c 6 • •••• :a0 • • • For torpid bats, V02 was clearly lower E than for euthermic bats at equivalent.iT but ., 4 • • • "C 0 the relationship between V02 and .iT was 0 2 • ..c not significant (F = 3, dj = 1,27; rZ = g: 0 0.05; n = 29): VOz = 0.18 (±0.18) + 0.08 0.. -5 0 5 10 15 20 25 30 Body - Ambient Temperature re) (±0.05) .iT. Nevertheless, the lower slope than for euthermic bats (0.08 versus 0.30) FIG. 2.-The relationship between V02 and was expected because torpid bats had a ~T of euthermic and torpid Nyctophilus geof• lower thermal conductance, and the lower froyi. intercept (0.18 versus 1.25) reflected the in• trinsically lower V02 of torpid bats, because below the corresponding value for eutherm• they had a lower T b than euthermic bats. ic bats (Fig. Ib). There was considerable Respiratory exchange ratio.-Vc02 of variation in the V02 of torpid bats at all T a' bats closely paralleled V02 and, hence, were hence the lack of significance in most com• not shown or analyzed separately. The re• parisons. Although the lowest V02 for tor• spiratory exchange ratio (RER = Vcoi pid bats was at a Ta of 15°C (0.26 ± 0.11 V02) of euthermic bats had a slight, but sig• ml O2 g-l h-', n = 7), this was only sig• nificant, positive linear relationship with Ta nificantly different from VOz at 5°C and (rZ = 0.38; n = 63 measurements of eight 20°C (F = 5, dj = 4,29; P < 0.05; sig• bats), increasing from 0.76 (±0.006) at Ta nificant heterogeneity of variance with B4 = 5°C (with the highest V02) to 0.82 = 11). Bats with a higher .iT tended to (±0.01) at Ta = 40°C. There was no sig• have a higher VOz (Fig. Ib). nificant relationship between RER and Ta Torpor substantially reduced energetic for torpid bats (rZ = 0.08; n = 25 measure• expenditure. On average, the lowest VOz of ments of eight bats); RER was 0.80 ± 0.01. torpid bats was 0.26 ml O2 g-I h-1 at Evaporative water loss.-For euthermic 14.5°C, whereas the greatest absolute sav• bats, a critical Ta of 34°C separated two re• ing of energy was 7.9 ml Oz g-I h-I at 5°C; gressions of EWL on Ta. There was no sig• the greatest proportional saving was 96.5% nificant dependence of EWL on Ta from 5 of euthermic VOz at 15°C. to 34°C (rZ = 0.0004; n = 42 measurements Metabolic rate and (..::1T).-For euthermic of eight bats), with a mean EWL of 2.48 bats, there was a linear relationship between (±0.09) mg HzO g-l h- 1• At Ta > 34°C, VOz and .iT (Fig. 2). For bats with Tb > Ta, EWL increased steeply (Fig. 3a) and, at ca. the relationship was V02 = 1.25 (±0.15) + 40°C, was significantly higher than at all 0.30 (±0.01) .iT, with rZ = 0.94 and n = other T a' Torpid bats usually had a lower 53. The intercept (1.25 ml O2 g-l h-') re• EWL than euthermic bats. The EWL of tor• flected the intrinsic metabolic rate of bats pid bats was slightly but significantly ele• when Tb = Ta, i.e., when there was no ther• vated at 25°C (1.2 mg g-l h- 1; n = 2) com• moregulatory requirement, and that value pared with other torpid values (F = 3.7, d.f. was within the 95% CI of BMR (1.16-1.64 = 4,27). ml Oz g-I h-l). The slope of this relation• Thermal conductance.-Wet thermal ship, 0.30 ml Oz g-l h- 1 °C-I, was another conductance was not calculated for bats at measure of thermal conductance. It closely Ta >30°C (Fig. 3b), because .iT was small corresponded to the value obtained from the at high Ta, and this made accurate deter• regression of V02 and Ta of 0.27 ml O2 g-l mination of conductance difficult. There 1999 HOSKEN AND WITHERS-METABOLISM OF NYCTOPH1LUS 47

~~15,------, a o compared with 10°e. The Cctry of torpid bats euthermic 0 o torpid· o was generally lower than the corresponding o o value for euthermic bats, especially at 15 Do and 20°C (Fig. 3c).~~

DISCUSSION The lesser long-eared bat is thermally la• ii3~ b bile and can be either euthermic or torpid ~ C. 1.2 .. ~:c at low Ta, although there is a high metabolic f=i~m 0,8 'b cost to euthermy at low Ta. This thermola• t;Cc) 0 IP ~~e 0 0 bility is typical of microchiropteran bats in _o.4 '6!l 00 ~ ..031 . temperate areas (e.g., Hosken, 1997; Hos• 0 1 • .. ken and Withers, 1997; Kurta and Kunz, 1§~20 C GUO; 15 ~ 1988; Lyman, 1977; McNab, 1982; Morris .c :;,.&:: 10 ~,,":" ~ ~C '" • et al., 1994; Speakman, 1988; Studier, Q~::2. 0 0 1. 20 2. 30 4' 1981; Webb et al., 1993). The day-to-day Air Temperature ('C) variability in thermal and metabolic data FIG. 3.-The relationship between a) evapo· might be due, in part, to daily variation in rative water loss and ambient temperature, b) reserves of body fat (Audet and Thomas, wet thermal conductance and ambient tempera· 1997). ture, and c) dry thermal conductance and am· Body temperature and metabolic rate.• bient temperature, of euthermic and torpid Nyc· The Tb of N. geoffroyi displayed clear pat• tophilus geoffroyi. terns of euthermy, with Tb ca. 32°C, and torpor, with Tb usually within I-5°C of Ta. were significant differences in Cwe! of eu• Mean euthermic T b is low by eutherian thermic bats from Ta 5 to 30°C (F = 17.3, standards but typical of microchiropteran d.! = 5,38; significant heterogeneity of bats (e.g., Genoud, 1993; Hosken, 1997; variance with Bs = 20), with Cwe! at 30°C Hosken and Withers, 1997). Even slight de• significantly different from that at all other pression of euthermic T b leads to significant Ta, and Cwe! at 25°C greater than at 5 and metabolic savings. For example, Plecotus 100 e. auritus affect an energetic saving of >40% Torpid bats had a significantly higher Cwe! by reducing Tb from 38 to 31°C at a Ta of at 5, 10, and 25°C than at 15 and 20°C, and 25°C (Webb et al., 1993), and such a re• Cwe! was also higher at 25°C than at 5 and duction reflects a trade-off between benefits 10°C (F = 11.3, d.f = 4,24). Mean mini• of remaining active (such as avoiding pred• mum Cwe! at Ta from 15 to 20°C was 0.060 ators) and energetic economy (Studier, (±0.01O) rnl O2 g-t h-t °c-t (n = 13 mea• 1981; Webb et al., 1993). surements of eight bats). Cwe! of torpid bats Torpid N. geoffroyi generally have T b was generally lower than the corresponding within I-5°C of Ta, although the Tb of tor• value for euthermic bats, especially at 15 pid bats was extremely variable (present and 20°C (Fig. 3c). study; Kulzer et a!., 1970). This is typical The Cctry followed the same general pat• of microchiropteran bats (Beer and Rich• tern as Cwe! (Fig. 3c). It did not vary sig• ards, 1956; Bell et al., 1986; Hock, 1951; nificantly for euthermic bats at Ta from 5 to Speakman and Racey, 1989; Studier, 1981). 25°C (7.2 ± 0.2 J g-t h-t °c-t; n = 32), At low Ta (5-1O°C), N. geoffroyi maintain but was significantly elevated at 30°C (12.0 a high T b (ca. 10°C) and correspondingly

± 0.9 J g-t h-t °c-t; n 8). The only sig• , = high "02 similar to other Australian ves• nificant difference in Cctry of torpid bats was pertilionid bats (Hosken, 1997; Hosken and at 15°C (0.60 ± 0.21 J g-I h-t °c-t; n = 7) Withers, 1997; Morris et al., 1994). The rel- 48 JOURNAL OF MAMMALOGY Vol. 80. No.1 atively high Tb and VOz reported for torpid Evaporative water loss.-Evaporative vespertilionids from Australia compared water loss (EWL) of euthermic bats had no with values for bats from the northern thermal dependence from 5 to 30°C, despite hemisphere may be related to differences in the significant positive relationship between experimental conditions, climatic factors, Ta and VOz over the same range of temper• and effects of captivity or reproductive con• ature. This is probably due to the counter• dition. In this study, length of captivity (25- acting effects of Ta on VOz and the gradient 110 days) did not influence thermoregula• in water vapor pressure driving EWL. A tion, but bats may acclimate :53 days of similar result was reported by two other captivity (Artibeus jamaicensis-Studier studies that used the same flow-through and Wilson, 1979). system (Hosken, 1997; Hosken and With• The BMR of N. geoffroyi was ca. 70% ers, 1997). of that predicted for an 8-g mammal (Klei• Daily water loss of euthermic N. geof• ber, 1961) but fell within the range reported froyi was ca. 6% of body mass at T a of 5- for vespertilionid bats, which typically have 30°C and 10% RH, and 25% of body mass a lower BMR than predicted (McNab, at 40°C and 15% relative humidity. This bat 1982). The Ta at which BMR was recorded, occupies roosts with Ta as high as 40°C 35°C, also is similar to that reported else• (Maddock and Tidemann, 1995), but RH of where (Bell et aI., 1986; Hosken and With• their roost is unknown. The EWL of euth• ers, 1997; Morris et aI., 1994; Stones and ermic N. geoffroyi was similar to that of Weibers, 1967), with a lower critical tem• other Australian bats under the same ex• perature of ca. 33.5°C. perimental conditions, 4-7% of body mass Torpor led to significant energetic sav• at 5-30°C and 10% RH, and 20-25% of ings of ca. 96% at all Ta. This is similar to body mass at 40°C and 15% RH, respec• that reported for other Australian bats (Hos• tively (Hosken, 1997; Hosken and Withers, ken, 1997; Hosken and Withers, 1997; Mor• 1997). Webb et al. (1995) reported that bats ris et al., 1994). Minimum VOz during tor• lose :530% of body mass per day at low por was ca. 17% of BMR, which is within RH «20%), a figure similar to that report• the range of reduction reported for hiber• ed here for N. geoffroyi, which inhabits ex• nators and daily heterotherms, although at tremely arid areas of Australia where high the upper end of the former and lower end water loss seems problematic. Daily water of the latter (Geiser and Ruf, 1995). Studier loss of bats is generally high compared with and O'Farrell (1980) reported that the VOz other mammals (Studier and O'Farrell, of euthermic and torpid Myotis lucifugus 1980). Nevertheless, a water loss of 23- and M. thysanodes were indistinguishable 32% of body mass is lethal for some bats at Ta of 20 and 24°C, respectively, and sim• (Studier et aI., 1970). ilarly, P. subflavus cannot enter torpor at Ta Conditions within the roost can reduce above ca. 18°C (McNab, 1974). This is not EWL significantly, with reported water loss the case for N. geoffroyi, which had a sub• in natural roosts of 15-16% of body mass stantial energetic savings through torpor at over 12 h (Studier et aI., 1970). Although Ta up to ca. 25°C. some bats occupy roosts of high RH (Stu• Respiratory exchange ratio.-The posi• dier and Ewing, 1971), they are in negative tive relationship between RER and Ta for water balance at RH less than ca. 99% euthermic N. geoffroyi has been noted for (Thomas and Cloutier, 1992). As a result of other bats (Hosken, 1997; Hosken and high EWL, selection apparently has favored Withers, 1997). RER values for torpid N. renal adaptations for high urinary concen• geoffroyi, which were not related to T a' also tration as a means of conserving water (Ge• are similar to values for other bats (Hosken, luso, 1980). 1997; Hosken and Withers, 1997). In mammals with limited access to water, 1999 HOSKEN AND WITHERS-METABOLISM OF NYCTOPHlLUS 49 low BMR and torpor are sometimes consid• 1994) and other small mammals (Snyder ered a strategy for conservation of water and Nestler, 1990). Although there are di• (Bonaccorso et aI., 1992; MacMillen, urnal differences in C (Aschoff, 1981), and 1972). Torpor reduces EWL of bats to a we measured euthermic and torpid C at dif• fraction of euthermic levels (Carpenter, ferent times during the day, the differences 1969; Hosken and Withers, 1997; Webb et in C of euthermic and torpid N. geoffroyi aI., 1995; this study). For N. geoffroyi, tor• are much greater than the 50% circadian por reduces water loss to ca. 25% of euth• difference reported by Aschoff (1981). The ermic values from 1O-25°C, which is sim• Cwet of torpid bats was ca. 15% of eutherm• ilar to other studies (Morris et aI., 1994). ic Cwet. The Cctry has less diurnal variation Thermal conductance.-For euthermic than Cwet (Aschoff, 1981), but differences N. geoffroyi, both wet and dry conductance for Cctry of euthermic and torpid N. geoffroyi were independent of Ta from 5-25°C. Con• were as apparent as differences for Cwe!" ductance (C) measured over this range of Reasons for differences in C of euthermic temperature (0.39 ml O2 g-I h-I °C-I, 7.2 J and torpid bats are not clear. Postural, re• g-I h-I °C-I) is our best estimate of mini• spiratory, and circulatory changes during mum euthermic conductance. Thermal con• torpor could produce a poorly perfused, hy• ductance (C) is typically constant below the pothermic periphery that acts as additional thermoneutral zone (TNZ) (Aschoff, 1981), insulation and reduces C (cf. Hosken and and the temperature range over which we Withers, 1997; Snyder and Nestler, 1990; reported a constant C is not unusual (Bon• Withers and Jarvis, 1980). The hypothesis accorso et at, 1992). Minimum euthermic that peripheral hypothermic tissue provides Cwet for N. geoffroyi is 108% of that pre• additional insulation is supported by the ob• dicted by Herreid and Kessel (1967) and is servation that C increases for torpid bats typical for bats in general (Bonaccorso et with elevated Tb and V02, presumably be• al., 1992; Genoud et aI., 1990). However, C cause this hypothermic insulative layer is of N. geoffroyi is high compared with some disrupted by the increased respiration and other Australian bats (Hosken, 1997; Hos• circulation required for elevated V0 2 (cf. ken and Withers, 1997). This may be relat• McNab, 1980) or the subcutaneous location ed to the potentially high temperature of of thermogenic brown fat (Dawson and Ol• their roosts (Maddock and Tidemann, son, 1987). The increase in V02 of torpid 1995), because high C facilitates loss of bats at low Ta is not reflected necessarily by heat. Thermal conductance of bats is related a correspondingly substantial increase in to characteristics of their roost (Kurta, AT, because Cctry and especially Cwet also in• 1985), and solitary tree-roosting bats typi• crease. Thus, the thermogenic response of cally have lower C than colonial species these torpid bats at low Ta is not very ef• roosting in more sheltered environments fective. (Shump and Shump, 1980). Interestingly, Metabolic depression during torpor.• N. geoffroyi is generally a solitary tree• Mechanisms responsible for reduced meta• roosting bat (Hosken, 1996; Lumsden, bolic rate of torpid mammals and birds have 1995), yet has high conductance. been debated (Geiser, 1988; Heldmaier and

Torpor not only decreases V0 2 and EWL Ruf, 1992; Snyder and Nestler, 1990). Two but also C. Minimum C wet of torpid bats is major factors contributing to reduced met• only 16% of that predicted for an 8-g mam• abolic rate during torpor are abandonment mal (Herreid and Kessel, 1967), and both of thermoregulation (or more correctly, a Cwet and Cctry were lowest at a Ta of 15°C lowering of the thermoregulatory set-point) for torpid bats. A lower C has been noted and a reduced metabolic rate as a conse• for other bats when torpid (Genoud, 1993; quence of lowered body temperature and a Hosken and Withers, 1997; Morriset aI., concomitant QIO effect (Geiser, 1988; Sny- 50 JOURNAL OF MAMMALOGY Vol. 80. No.1 der and Nestler, 1990; Withers, 1992). Met• 100,------, abolic rate during torpor might be de• euthermic 'CJI 10 non-b~S~ pressed further intrinsically, for example, ($ by changes in acid-base status (Malan, §. thermoregulating 00 0 o 1980, 1986, 1988). .; 1 ~ooQ§lo torpid • BMR It: o 0 • We suggest a major role of down-regu• .2 o • o • lation of the thermoregulatory set-point and :g 0.1 • a QIO effect in reducing metabolic rate of i passive ::IE Q,,= 3.94 f-r-,-~,.c;....,--r-rl~~~-,--b~~~_+____~~__.__.__j N. geoffroyi. The V02 at a Ta of ISoC could 0.01 o 10 20 30 40 immediately decline at the onset of torpor Body Temperature ('C) from ca. 6.0 ml O2 g-I h-I to BMR, a dif• FIG. 4.-Tbe relationship between V02 and ference of 4.6 ml O2 g-I h-I, by down-reg• ulation (Fig. Ib). A consequence of this body temperature of euthermic (BMR and non• basal) and torpid (passive and thermoregulating) down-regulation is that Tb declines, so there Nyctophilus geoffroyi. The regression line for is a further reduction in V02 below BMR V02 of bats when passively torpid and euthermic due to a QIO effect. This Qwrelated reduc• at BMR is equivalent to a QIO of 3.94. tion in V02 is ca. 1.14 ml O2 g-I h-I (from

1.4 to 0.26 ml O2 g-I h-I). At a Ta of ISoC, the relative importance of down-regulation and a QIO effect is about 4:1 (4.6/1.14). At geoffroyi, for which C changes markedly higher T a' the decrease in V02 due to down• during torpor and there is a substantial QIO regulation is less (V02 of euthermic bats is effect. lower), as is the QIO decrease (torpid Tb is Finally, is there evidence for intrinsic higher); at 2SoC, the ratio is 2.4: 1. At lower metabolic depression in torpid N. geoffroyi? Ta, the decrease in V02 due to down-regu• Unfortunately, the precise contributions of lation is greater (V02 of torpid bats increas• down-regulation, the QIO effect, and possi• es but not as much as for euthermic bats), ble intrinsic metabolic depression are diffi• and the QIO decrease is greater (Tb is lower); cult to discern (Snyder and Nestler, 1990), at SoC, the ratio is 3.6: 1. Thus, down-reg• particularly if aT is substantial and thermal ulation of the thermoregulatory set-point conductance decreases during torpor (as for and the consequent QIO effect are both con• N. geoffroyi). We graphically analyzed the tributors to metabolic reduction in torpid N. relationship between V02 and T b for N. geoffroyi over a wide range of T a' although geoffroyi when euthermic and thermoneu• the down-regulation effect is always great• tral, and when torpid and non-thermoregu• er. lating, to estimate the QIO for metabolic re• Heldmaier and Ruf (1992) suggested that duction during torpor (Fig. 4). It should be the metabolic rate of torpid Djungarian valid to calculate a QIO from these data be• hamsters (Phodopus sungorus) was ex• cause V0 of these bats is not elevated for plained solely by down-regulation. Their 2 evidence was an identical linear relation• thermogenesis (unlike V02 of euthermic bats when non-basal and torpid bats when ship between V02 versus aT for euthermic and torpid hamsters (cf. our Fig. 2). The thermoregulating). Our analysis yields a QIO of 3.94, which is higher than values of 2- slope of this relationship is Cwet, which is apparently the same for euthermic and tor• 3 (Withers, 1992) and QIO for endotherms pid hamsters. Absence of a difference in el• within torpor of 2.3-2.6 (Geiser, 1988). evation of V02 for euthermic and torpid Thus, the high QIO of 3.94 for N. geoffroyi hamsters indicates the surprising absence of suggests intrinsic metabolic depression. a QIO effect. Results for Djungarian ham• Metabolic acidosis during torpor may be sters are very different from ours for N. one explanation (Malan, 1980, 1986, 1988). 1999 HOSKEN AND WITHERS-METABOLISM OF NYCTOPH1LUS 51

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