Energetic advantages of slight drops in body temperature in little brown bats, Myotis lucifugus

C<JIIIP_ Blo<hrm. Phwol. Vol. 7OA. pp 537 to 540. 1981 0300-9629 XI 120537-04302.00 0 Printed ,n Great Br,taln. 411 rights rexned Copyright 0 198 I Pergamon Press Ltd ENERGETIC ADVANTAGES OF SLIGHT DROPS IN BODY TEMPERATURE IN LITTLE BROWN BATS, MYOTIS LUCIFUGUS EUGENE H. STUDIER Department of Biology, University of Michigan-Flint, Flint, MI 48503. U.S.A Abstract-l. At constant ambient temperatures (c) below their thermal neutral zone (TNZ), little brown bats, Myotis lucifuyus, maintain a wide range of steady-state body temperatures (&). 2. The relationship between oxygen consumption and T&-T, differential at constant T,s below the TNZ is curvihnear. 3. Small drops in & from high & levels result in sigmfirantly greater energy savings than subsequent & reductions of equal increments. INTRODUCTION Deep body temperature (G) and oxygen consumption (OC) as functions of ambient temperature (T,) have been determined for a wide variety of mammals. Assuming that the organisms under consideration do not significantly utilize anaerobic energy producing metabolic pathways and Tb is constant during the period of measurement, the rate of OC is directly related, with little error, to metabolic heat production. Possible interrelationships between G, OC, and T, have often been discussed and debated (Scholander et al.. 1950; Kleiber, 1961; King, 1964; Tucker, 1965; Porter & Gates, 1969; McNab, 1970; Strunk, 1971; Kleiber, 1972; Calder, 1972; Calder & King, 1972; Strunk rt cd., 1973; McNab, 1980). Of particular interest is the relationship of OC and the T,-T, differential (T-T,) in endotherms at T,s below the thermal neutral zone (TNZ). In mammals in which steady-state G is constant and independent of T,, i.e. in homeothermic endotherms, T,T, differential can be obtained only by varying T,. It is, therefore, impossible to analyze the relation of OC to T,-T, at constant T, in such species. Among heterothermic endotherms, however, some data are available (Studier & O’Farrell, 1972, 1976) for OC at a wide range of steady-state Ths at constant T,. This paper reports the relationships between OC and T,T, at constant T,s below the TNZ in a heterothermic endotherm, the little brown bat, M~,oti.s luc~&~us, and comments on the energetic advantages of this thermoregulatory strategy. MATERIALS AND METHODS Data analyzed for the present study are taken from Studier & O’Farrell (1972). Details of materials and methods used appear in that paper and will be summarized here. Adult, female little brown bats of varying reproductive conditions (pregnant, lactating, post-lactating) collected throughout the summer from a maternity colony were studied. All laboratory studies were performed on the day of capture. Steady-state OC and Tb were recorded at T,s of 1640°C at 4°C intervals. Laboratory controlled T,s were programmed to coincide with T,s in the natural roost. RESULTS AND DISCUSSIONS Steady-state T,,s of little brown bats at various controlled T,s (shown in Fig. 1) indicate the heterothermic pattern of thermoregulation exhibited by these bats when tested on the day of capture. Much of the variability in level of regulated Tb is a function of stage of pregnancy, stage of reproductive cycle, etc. (Studier & O’Farrell, 1972). Data on OC and T,-T, at various controlled T,s from 1632°C were analyzed by both stepwise polynomial regression and by least squares regression analysis of eleven possible power, root, and reciprocal transformations of both OC and T,-T, together and independently to determine the best statistical descriptions of the relationships between these variables. Regression coefficients for the independent variable (T,T,) as a squared term or squared transformation were invariably significant, except at a T, of 32°C. Based on comparing coefficients of determination (r’) for maximal values, the best uniform regression analysis, except at 32”C, were curvilinear equations of the form _V = b.? + u, where J is OC in cc/g per hr and x is T,-T, in ‘C. Equations are given in Table 1 and illustrated in Fig. 2. The relationship of OC to Th-T, becomes progressively less curved as T, rises until at a T, of 32 ‘C. which is the thermal neutral temperature for this species (Stones & Wiebers, 1965), the relationship is linear. Since thermal conductance (McNab, 1980) is represented by the slopes of the lines in Fig. 2, at T,s below the TNZ, thermal conductance is not a constant. Linear regression analysis of these variables (OC and G-T,) will, therefore, underestimate actual thermal conductance when T,-T, is large and overestimate thermal conductance when T,-T, is small. As stated earlier, in homeothermic endotherms, the only method of obtaining T,-T, is by modifying T,. For such species, thermal conductance is characteristically estimated by analyzing the slope of the relationship of OC to T, at T,s below the TNZ. Since Tb is constant in such species, the abscissa is related to T,-T, and resultant figures show a negative slope since T,-T, decreases as T, rises. Such graphic representations are, EUGENE H. STUDIER 40361 I I 4 4 2 320 k t 2 / I 28- ' 2 u D I en 24- , 202 I I I 3 3 2 2 4 5" 5 3 3 7 2 : : 4 f 2 2 2 2 : I I I 2 I I 4 4 / 6 4 /I II 5 3 4 2 5" I $0 : 7 13 1 4 IO ?I I : 2 : 16 ' , I 1 I I t 16 20 24 28 32 36 40 Fig. 1. Steady-state body temperatures (T,) of adult female Myotis Iueijiiyus of varying reproductive condition at constant ambient temperatures (T,). Numbers indicate the number of data points at that position. therefore, inverted left to right in comparison to Fig. 2. Inspection of some published figures depicting OC as a function of T, in homeothermic endotherms Table 1. Reduced statistical data for the relationship of oxygen consumption (y, in cc/g per hr) to body temperature to ambient temperature differential (x, in “C) at various ambient temperatures (7J in Myotis hAjiigus. Regression coefficients are for equations of the form 1’ = hx’ + a. P < 0.0005 in all cases. Values in parentheses are standard errors. Regression coefficients r, (‘C) b a F d.f. r* 16 0.0192 0.268 203.4 1,29 0.875 (0.0013) (0.154) 20 0.0194 0.149 182.8 t,23 0.888 (0.0014) (0.120) 24 0.0263 0.558 166.8 1,33 0.835 (0.0020) (0.077) 28 0.0430 0.480 48.6 1,29 0.627 (0.0062) (0.096) 32* 0.441 0.271 29.4 I,32 0.487 (0.081) (0.158) * Regression coefficients are for the linear equation: !’ = bx + a. shows relationships which appear to be curvilinear although they are often analyzed in rectilinear fashion (e.g. Banholzer, 1976; Grant & Dawson, 1978; Kamau et al., 1979; Degabriele & Dawson, 1979: Riibsamen & Kettembeil, 1980). The rectilinearity of this relationship has been questioned previously (Tracy, 1972). Furthermore, when thermal conductance is calculated on individual measurements of Th and OC, it is apparent for many species that thermal conductance is not constant (McNab, 1980). Since methods are available for curvilinear (polynomial) regression analysis, such analysis should be performed to determine the best descriptive statistics of data such as OC as a function of T, in homeothermic endotherms. Such analysis would yield more accurate estimates of minimal standard metabolism and thermal neutral temperature (Studier rr al., 1975). The curvilinearity of the relationship of OC to G-x at constant T,s in M. ~~c~u~u.s (Fig. 2) would not appear to be related to changes in the bats’ physical environment but probably reflects some animalregulated property. Possibilities include animal regulated differences in metabolic heat production and/or in heat Row through changes in conductivities of the shell (King & Farner, 1961) or in peripheral blood flow, etc. The relatively linear, upper portions of the OC to T,T, relations (Fig. 2) may well be parallel Energy savings due to lowered K in bats 539 80 - 70 - 2 6.0 _ E P s 50s ; f 4.0 _ 5 % 30E 0 16 disproportionately less energy than a very high Y&, set point. Acknowledym~enrs-I thank Drs Bruce Wunder and William A. Calder for many useful comments on an earlier version of this manuscript and Dr Richard W. Dapson for his criticisms throughout the development of this manuscript. Tb - T0 , ‘C Fig. 2. Regression equations at various ambient temperatures for the relationship of oxygen consumption to body temperature to ambient temperature differential (T,-T,) in M~0ti.s /uc~~fi~gu.s. and indicate uniform energetic responses at various T,s when T,-T, differential exceed a critical level. The lowering of rz values as T, increases indicates that G-T, differential explains progressively less of the variability in OC. While a statistically significant rectilinear relationship exists between OC and T,-T, at all T,s analyzed, the relationship is best described by a curvilinear equation except at a T, of 32°C. Use of a rectilinear equation predicts equal reductions in OC for any incremental reduction in Tb whereas the curvilinear equations show larger reductions in OC when Tb is reduced in equal increments from a high set point. As an example, at a T, of 2O’C a drop in Th from 37°C (5.76 cc/g per hr) to 33’C (3.43 cc/g per hr) results in a reduction of OC of 2.33 cc/g per hr. Using 4.8 Cal/cc of oxygen as an energy equivalent, this is a savings of 11.2 Cal/g per hr. A further drop in T from 33°C to 29°C (1.72 cc/g per hr) results in a considerably reduced energy savings of only 8.2 Cal/g per hr. It is also useful to consider energy requirements for raising Tb. 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