Dynamic Thermal Balance in the Leaf‐Eared Mouse

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Dynamic Thermal Balance in the Leaf-Eared Mouse: The Interplay among Ambient Temperature, Body Size, and Behavior

Diego M. Bustamante At high Ta, flattening appeared to be an equally useful mech- Roberto F. Nespolo anism for heat loss, for both large and small animals. Enrico L. Rezende* Francisco Bozinovic† Centro de Estudios Avanzados en Ecologıá y Biodiversidad, Departamento de Ecologıá, Pontificia Universidad Cato´lica Introduction de Chile, Santiago 6513677, Chile Organisms live in environments where biotic and abiotic factors Accepted 4/18/02 can vary, causing unpredictable daily changes in energy demands. For example, in small endotherms, a sudden cold spell can lead to greatly increased thermoregulatory expenses (Tracy 1977; Veloso and Bozinovic 1993; Merritt 1995; McNeill- ABSTRACT Alexander 1996; Wolf and Walsberg 1996; Taylor 1998). In order Endotherms maintain constant body temperature through to match supply to energy demands, animals must demonstrate physiological and behavioral adjustments. Behavioral thermo- behavioral and physiological flexibility. regulation is an important factor influencing energy balance. Changes in daily and/or seasonal activity patterns, micro- We exposed the leaf-eared mouse, Phyllotis darwini, to tem- habitat selection, huddling, and nest use are widespread among peratures corresponding to its natural thermal range and stud- small mammals, and the effect of these strategies on energy expenditure has been quantified in several studies (Casey 1981; ied two forms of behavioral thermoregulation: diminishing sur- Vogt and Lynch 1982; Vickery and Millar 1984; Stapp et al. face to volume ratio by huddling and heat dissipation by 1991; Stapp 1992; Hayes et al. 1992; Canals et al. 1997; Feld- increasing physical contact with the substrate (flattening). We hamer et al. 1999). Among the behavioral thermoregulatory predicted that at low ambient temperatures (T ) huddling a mechanisms displayed by small mammals, huddling is partic- would be used as a heat conservation mechanism and at high ularly important for decreasing metabolic rate and food con- T flattening would be used for heat loss. We simultaneously a sumption (Fedyk 1971; MacArthur and Aleksiuk 1979; Springer measured oxygen consumption (V˙ o ) and flattening, in re- 2 et al. 1981; Karasov 1983; Contreras 1984; Andrews and Belk- sponse to three independent factors: huddling, T , and body a nap 1986; Bozinovic et al. 1988; Dyck and MacArthur 1993; mass. Each experiment was a 6-h˙ trial where five virgin Vo2 Feldhamer et al. 1999; Merritt et al. 2001) and also for in- females were measured at constant Ta. We performed this pro- creasing survival times at low ambient temperatures (Ta; Sea- tocol for two body mass groups, small (ca. 40 g) and large (ca. lander 1952; Feldhamer et al. 1999). Thus, behavioral ther- 70 g), in a metabolic chamber. Treatments were groups with moregulation can be viewed as a trait that has direct and without the ability to huddle at five different Ta, ranging consequences on fitness. from 5Њ to 35ЊC. A significant interaction between all three Theoretical as well as empirical studies on huddling behavior, factors was found. Huddling and flattening were used as strat- and its relationship with body mass (mb), emphasize the in- egies for conserving or dissipating heat, respectively, and the creased effects of Ta on decreasing mb (McNab 1970; Schmidt- shift between both strategies occurred at the lower limit of Nielsen 1995). Riesenfeld (1981) found that survival time of thermoneutrality. At Ta below thermoneutrality, huddling was two species of rodents maintained at low Ta increased concom- a more effective way of reducing metabolic requirements and itantly with mb, but at Ta above thermoneutrality the opposite was more efficient (HE) in small individuals than large indi- effect was observed. This indicates that behavioral mechanisms viduals. So, by huddling, small individuals save more energy. that minimize heat loss should be substantially more important in smaller species. * Present address: Department of Biology, University of California, Riverside, At the intraspecific level, few studies have analyzed the effect California 92521. of m on energy savings through behavioral thermoregulation †E-mail: [email protected]. b (McCracken et al. 1997; Redman et al. 1999). This mechanism Physiological and Biochemical Zoology 75(4):396–404. 2002. ᭧ 2002 by The would be particularly important for understanding the main- University of Chicago. All rights reserved. 1522-2152/2002/7504-1104$15.00 tenance of euthermy during ontogeny (Webb et al. 1990; Canals

This content downloaded from 146.155.157.160 on May 18, 2018 14:18:55 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). Thermal Balance in the Leaf-Eared Mouse 397 et al. 1998). Recently, Baer and Travis (2000), Dawson et al. captured in Quebrada de la Plata (33Њ29ЈS, 70Њ56ЈW; 500 m (2000), and Tracy and Walsberg (2000) pointed out that phys- above sea level), using Sherman live traps. We used unrelated iological and behavioral strategies that take place at high Ta’s virgin females that were born and maintained in the laboratory Њ עp Њ have been poorly studied. A good example of the consequences (food and water ad lib.,Ta 28 2 C and 12L : 12D pho- of discarding this issue is the common—yet untested— toperiod). Animals were divided into two groups (N p 5 per ע hypothesis that some small mammals are very limited in their group) of contrasting mb: small individuals (41.2 3.8 g p ע upper thermal tolerance (Tracy and Walsberg 2000). Contrarily, [mean SD ], 33.6–49.4 [range],m b 40 g) and large indi- p ע ע the extremely small kangaroo rat can maintain its locomotory viduals (69.8 4.9 g [ mean SD ], 60–79 g [range], m b Њ performance at Ta’s above 42 C (Tracy and Walsberg 2000). 70 g). Both behavioral and metabolic measurements were car- We studied the behavioral thermoregulation of the leaf-eared ried out in a Plexiglas metabolic chamber (50 # 50 # 40 cm). mouse, Phyllotis darwini (Sigmodontidae), as a function of a The chamber was divided into nine equivalent compartments wide range of Ta’s. Phyllotis darwini inhabits the semiarid en- separated by wooden walls, each 20 cm tall and connected by vironments of central Chile and shows a large variability in mb passageways. This setup allowed animals free access to each among adults, ranging from approximately 35 g to 100 g (Lima compartment. The height of the walls was one-half the height et al. 1997). In addition, under cold conditions, P. darwini of the chamber to ensure complete mixing of the air inside. demonstrates an efﬁcient huddling behavior (Canals et al. Individuals were free to move, huddle, or remain separated. 1989), communal nesting (Bozinovic et al. 1988), and changes Animals were placed in the experimental system 24 h before in daily activity patterns (Rezende and Bozinovic 2001) as strat- experimentation and maintained with the same photoperiod egies to economize energy. (12L : 12D) to allow them to get habituated to the experimental

At low Ta’s, endotherms need to elevate oxygen consumption conditions. During this 24 h period, apples were provided ad ˙ (Vo2 ) in order to maintain body temperature (Tb); huddling lib. as a source of food and water; however, before each ex- allows individuals to decrease metabolic requirements and heat perimental trial, animals were postabsorptive for at least 2 h. loss by reducing the surface area to volume ratio. In the op- For the nonhuddling treatment, the same experimental setup posite extreme, Ta’s above thermoneutrality induce an increase and protocol was repeated using the same individuals for each in metabolic rate and eventually provoke hyperthermia (Gor- group (N p 5 ), with the exception that in this treatment phys- don and Rezvani 1995; Tracy and Walsberg 2000). Our prelim- ical contact among individuals was eliminated by closing off inary observations suggested that warm conditions induced an passages between compartments and placing only one individ- increase in physical contact between the individual and the ual in each compartment. Under these conditions, huddling substrate (“flattening”), which is probably employed as a mech- was suppressed. Comparisons were carried out between hud- anism that allows for an increase in heat loss by conduction. dling groups (connected compartments, Hϩ) and solitary in- Such a mechanism may account for observations of individuals dividuals (isolated compartments, HϪ). Њ of P. darwini that survive at Ta’s above 42 C. In all experiments, mb was measured before and after ex- g). The 0.1ע) This study was designed to examine how the energy economy perimental trials, using an electronic balance ˙ and thermoregulatory behavior (i.e., decrease in exposed sur- total mass of each group was used for O2-consumption (Vo2 ) face area) of P. darwini varied with body mass, thermoregu- analyses. The metabolic chamber was kept in an incubator, Њ ע latory costs (Ta), and huddling. We assessed the interplay where Ta was maintained constant ( 0.5 C) for five Ta’s be- Њ Њ among these three fixed factors on metabolic rate (energy ex- tween 5 and 35 C. Each Ta (i.e., temperature treatment) was penditure) and exposed surface to substrate (flattening behav- randomly assigned, and individuals were exposed to the Ta ior). We predict that flattening and energy expenditure are corresponding to their acclimation period. The complete ex- determined by the significant interaction of these three factors. perimental procedure lasted 120 h (6 h # 2 huddling condi- # # Specifically, we predicted that at a low Ta, huddling would be tions 2 mb 5 Ta’s; see below). Each trial produced six or used as a heat conservation mechanism, whereas at a warmer seven photographs of exposed surface (see below), along with ˙ Ta, flattening would be used for heat loss. To provide a mech- the correspondingVo2 recordings. Following this procedure, ˙ anistic foundation for the behavioral responses of small mam- we obtained at least 120 photographs andVo2 recordings ˙ # # mals, we also attempted to analyze the behavioral responses at (6 photographs/Vo2 5 temperatures 2 huddling condi- # p ˙ low and high Ta’s. tions 2 body masses 120Vo2 and exposed surface area records). Material and Methods Animals and Experimental Procedures Rate of Metabolism Animals were obtained from a laboratory-reared colony started Oxygen consumption was measured in a computerized (Da- from wild individuals one generation before experiments. In- tacan V) open-flow respirometer (Sable Systems, Henderson, dividuals from the parental generation (35 individuals) were Nev.). The metabolic chamber received dried air at a rate of

1,000 mL/min from a mass-flow controller (Sierra Instruments, F values using the “Rt Manly” software (http://www.west- Monterey, Calif.), which was enough to ensure adequate mixing inc.com; Manly 1998). This procedure performs a traditional in the chamber. Air passed through CO2-absorbent granules of ANOVA with F computations for each factor and interaction, Baralyme and Drierite before and after passing through the followed by the random allocation of each observation to the chamber and was sampled every 5 s by an Applied Electro- design factors. This reallocation was repeated 5,000 times; thus, chemistry O2 analyzer, model S-3A/I (Ametek, Pittsburgh). after each randomization we obtained a different F value for Since the volume of the chamber was 100 L, the time for each factor and interaction. An F distribution was built from equilibration ranged from 30 min (at 35ЊC) to 3 h (at 5ЊC). these values, and we declare our observed F to be significantly We used measurements obtained at least 1 h after the equili- large at the100(a Ϫ 1)% for F values from randomization. The ˙ bration period for analyses.Vo2 group values were calculated advantages of randomizations arise from the fact that we test using equation (4a) from Withers (1977, p. 122), where total significance using an F distribution obtained from our observed ˙ mass was the group total (i.e., an averageVo2 measurement data and not from a theoretical distribution. Homogeneity of for the group was obtained for each separate treatment). All variance is the unique assumption of randomized ANOVA metabolic trials were performed between 1400 and 1700 hours, (Manly 1998), which was accomplished by our data (P 1 0.05 , corresponding to the resting period of this species (Rezende Levene test). When all ANOVA assumptions are met, both ran- and Bozinovic 2001). Recording began 20 min after the partial domization and ANOVA results are similar (Manly 1998, p. pressure of O2 inside the metabolic chamber remained stable. 145). Here, we present significance levels for the original ANOVA as well as for the randomization procedure. In addition, a Mann-Whitney U-test was used to determine differences Exposed Surface Area Measurements (“Flattening”) in efficiency (HE) and energy saving between body size groups. ע ˙ DuringVo2 measurements, the surface area of the animal in All results are shown asmeans SD (Statistica 1997). contact with the bottom surface of the metabolic chamber (i.e., floor) was quantified through photographic records. A camera Results and Discussion (Canon, model EOS 500N) was placed approximately 80 cm below the metabolic chamber inside the incubator, in such a Metabolic rate and flattening revealed similar patterns for both manner that all the transparent floor of the chamber was in- groups (i.e., large and small individuals). Metabolism decreased ˙ cluded in the field of view. DuringVo2 measurements, pho- linearly as Ta increased, reaching low values together with the tographs were taken every 30 min with an automatic shooter highest exposed surface area observed for both groups at 30ЊC # located outside the incubator, so as not to disturb the animals (Fig. 1). In this context, the interaction term (mb huddling # ˙ during shooting. Surface area was estimated gravimetrically by Ta) significantly affected bothVo2 and exposed surface area p ! p ! weighing the total surface occupied by the five animals in the (ANOVA:F4,11820.26 ,P 0.01 andF 4,118 3.41 ,P 0.01 , re- photograph and comparing this weight to the weight of the spectively; Tables 1, 2). chamber floor area. Thus, during each trial we obtained six or In both small and large individuals, the effects of huddling seven values corresponding to the proportion of surface area behavior became more conspicuous as Ta decreased, although of the animals exposed to chamber floor, with their respective huddling appeared to be more important (in terms of metabolic ˙ values ofVo2 . rate) for small individuals at higher Ta’s (Fig. 2). Nevertheless, metabolic rate in large individuals was independent of huddling at both 30Њ and 35ЊC, which was not the case for small indi- Statistics viduals (Fig. 2). ˙ To test for the effects of mb, Ta, and huddling onVo2 and The amount of surface area exposed to the floor showed a exposed surface, we performed fixed-factor ANOVA (model 1) proportional relationship with Ta for both large and small in- for each dependent variable separately. Body mass and huddling dividuals. Temperatures below thermoneutrality decreased the each had two levels (40 g and 70 g, Hϩ and HϪ, respectively), amount of surface exposed to the substrate. In contrast, warmer Њ Њ Њ Њ Њ while Ta had five levels (5 ,10,20,30, and 35 C). We stan- Ta’s (above thermoneutrality) increased exposure to the sub- dardized exposed surface area for each mb to avoid effects of strate (see Figs. 1, 3). Table 3 shows the mean number of mb (Schmidt-Nielsen 1995). We compared the relative pro- individuals per huddling group for each Ta and mb. Both body Њ portion of exposed surface areas between groups (i.e., exposed size groups were to be totally grouped at cool Ta’s (5 and Њ 1 Њ surface per observation divided by maximum surface observed 10 C). Warmer Ta’s ( 20 C) prompted individuals to remain Њ in photographs, for each treatment). These values were log10 separated. This pattern is clear for large individuals at 20 C, transformed to satisfy the assumption of homogeneity of var- while for small individuals, separation occurs only at 35ЊC. ˙ ! iances. OurVo2 data were not normally distributed (P 0.05 , Apparently, animals minimize the amount of exposed surface

Kolmogorov-Smirnov test), but variances were homogeneous area at Ta’s slightly below their lower limit of thermoneutrality (P 1 0.2 , Levene test). We performed 5,000 randomizations on (Fig. 3). This pattern becomes clear when we analyze the ratio

(in warm conditions). Although many studies have demon-

strated the importance of mb, Ta, and huddling on endothermic thermoregulation (Sealander 1952; Tracy 1977; MacArthur and Aleksiuk 1979; Bozinovic et al. 1988; Dyck and MacArthur 1993; Stewart et al. 1993), the interplay among these factors have been less frequently discussed. Our study suggests that these variables exhibit strong interactions inﬂuencing the thermal balance of individuals. Under cold conditions, huddling was more effective in small individuals rather than in large ˙ ϩ ones. The maximum difference inVo2 between (H ) and (HϪ) animals was observed at 10ЊC (Figs. 1, 3; see also Boz- inovic et al. 1988). For small animals, this difference corre-

-mL O2/g/h, whereas in large individ 0.15 ע sponded to1.88

;mL O2/g/h (Fig. 1 0.09 ע uals, this difference was0.85 Mann-Whitney U-test:Z p 3.1304 ,P p 0.0017 ). At the same Њ ˙ Ta (10 C), the reduction inVo2 for the total group mass was

/mL O2 28.88 ע higher in small than large individuals (375.39

-mL O2/h, respectively; Mann-Whitney U 29.45 ע h vs.304.00 p p ˙ test:Z 3.0027 ,P 0.0027 ). Under warm conditions, Vo2 is a measure of thermal stress (i.e., organisms storing heat increase their metabolism; see Gordon and Rezvani 1995; Tracy and ˙ Walsberg 2000). Thus, given that at high Ta, bothVo2 and relative exposed surface area were similar for small and large individuals (Fig. 1), we conclude that small and large individuals do not differ in their flattening effectiveness (Figs. 2, 3). Figure 1. Metabolic rate and exposed surface area of five large Phyllotis darwini (upper panel) and five small individuals (lower panel). Open However, because of technical limitations, we were unable to circles indicate animals not allowed to huddle (HϪ), and closed circles measure body temperature. For this reason, we cannot be cer- indicate individuals allowed to huddle (Hϩ). tain that animals were actually storing heat at warm temperatures. However, when data for Hϩ and HϪ individuals were Ϫ ϩ ˙ Њ of exposed surfaces between H and H (Fig. 4). Differences pooled together, the increment inVo2 at 35 C (compared with Њ Њ Њ ˙ Њ were practically identical for individuals at 5 ,10, and 20 C, Vo2 at 30 C) was significantly greater for large animals (Wil- contrasting with the gradual change in “slopes” observed in coxon matched paired test:Z p 3.2958 ,P p 0.00098 ; see Fig. Figure 1. 1) but not for small animals (Wilcoxon matched paired test: Results indicate that huddling is an important mechanism Z p 0.0314,P p 0.9749 ; see Fig. 1). This increment in metab- of heat conservation and energy economy (in cold conditions), olism of large animals appears to be a sign of hyperthermia. whereas flattening appears to be a heat dissipation mechanism According to Canals et al. (1998), the efficiency of huddling

˙ Table 1: Randomization ANOVA results for Vo2 Sum of Mean Randomization df Squares Square FPValue P Value ! ! mb 1 .045 .045 360.83 .001 .001 Huddling 1 .001 .001 886.34 !.001 !.001 ! ! Ta 4 .006 .001 1,127.01 .001 .001 # ! ! mb huddling 1 .012 .012 93.91 .001 .001 # ! ! mb Ta 4 .039 .983 78.97 .001 .001 # ! ! Huddling Ta 4 .001 .026 211.02 .001 .001 # # ! ! mb huddling Ta 4 .011 .287 23.05 .001 .001 Error 100 .012 .012

Note. Factors were body mass (mb) with two levels, huddling with two levels, and ambient temperature (Ta) with ﬁve levels.

Table 2: Randomization ANOVA results for exposed surface area (log10 transformed) Sum of Mean Randomization df Squares Square FPValue P Value ! ! mb 1 .086 .086 79.69 .001 .001 Huddling 1 .398 .398 368.34 !.001 !.001 ! ! Ta 4 .012 .300 .38 .001 .001 # mb huddling 1 .004 .004 277.16 .539 .537 # ! ! mb Ta 4 .056 .014 12.86 .001 .001 # ! ! Huddling Ta 4 .152 .038 35.14 .001 .001 # # mb huddling Ta 4 .017 .004 3.98 .005 .0038 Error 100 .1081 .011 Note. Levels as in Table 1.

˙ (deﬁned by these authors as the maximum energy saving during (Vo2 of huddling and nonhuddling individuals becomes sim- huddling; HE) can be calculated as ilar; see Figs. 1, 2; Vickery and Millar 1984), and the individuals

tend to be separated (Fig. 3), consequently increasing Mm and p Ϫ HEm1 M ,(1)causing HE to become negative (Fig. 4a). In terms of efficiency, our results reveal significant differences ˙ where Mm is the ratio betweenVo2 (mass specific) of huddling/ in this variable between body masses. Huddling was more ef- nonhuddling animals. When huddling is highly efficient ficient in small than in large individuals (Mann-Whitney U- ! Њ p p (),M m 1 HE becomes positive; this occurs at Ta below 20 C test:Z 2.8719 ,P 0.0041 ). Specifically, at Ta below ther- Њ (Fig. 4a). Above thermoneutrality, huddling is clearly ineffective moneutrality (10 C), where the Mm value was highest for each

Figure 2. Multiway plot showing metabolic rate as a function of temperature and huddling for large (70 g, continuous line, closed circles) and small (40 g, dotted line, open circles) Phyllotis darwini (N p 5 for each size).

Figure 3. Multiway plot showing the logarithm of relative exposed surface area (total exposed surface area/maximum exposed surface area) as a function of temperature and huddling for large (70 g, continuous line) and small (40 g, dotted line) Phyllotis darwini (N p 5 for each size).

-Mann ; 0.05 ע and small individ- in comparison with large individuals (f p 0.47 ( 0.02 ע group, the efficiency of large (0.29 was significantly different (Mann-Whitney Whitney U-test:Z p 2.9866 ,P p 0.0028 ). These differences in ( 0.03 ע uals (0.45 p p ˙ U-test:Z 3.1304 ,P 0.0017 ). f are in agreement with the observed differences inVo2 and Following the theoretical formulations of Canals et al. (1997), huddling efficiency between both body size groups at 10ЊC. a realistic expression of Mm is Above thermoneutrality, f becomes negative; this reflects the fact that individuals in the huddling treatment group are no 0.735 longer losing surface area relative to the nonhuddling treatment f M p ,(2)(i.e., individuals are completely separated in both groups; Fig. m 5 ϩ (1 Ϫ f) [] 3). The ratio between exposed surface area of huddling/non- where f is a unitless quantity that represents twice the relative huddling individuals is shown in Fig. 4b. Values below unity area lost per individual due to huddling (see also Canals et al. 1998). The equivalent expression Table 3: Mean number of SD) per huddlingע) Ϫ M 1.3605 individuals 1 f p m (3) 0.8 group for each ambient temperature by body mass could be used as an alternative of H and M to visualize the Њ E m Ta ( C) 40 g 70 g changes in huddling effectiveness and efficiency with T .At 0. ע 5 0. עa 55 temperatures well below thermoneutrality (5Њ and 10ЊC; 0. ע 5 0. ע 5 10 whereas at , 0.11 ע see Fig. 4a),f p 0.54 ;0.08 ע M p 0.66 99. ע 3.10 0. ע m 20 5 -In . 0.15 ע Fig. 4a),f p 0.33 ; 0.10 ע T p 20ЊC (M p 0.80 52. ע 2.50 0. ע am 30 5 deed, at T below thermoneutrality, the reduction in exposed 98. ע 57. 1.25 ע a 35 1.29 was higher ( 0.1 ע surface area per small individual (f p 0.60

it is assumed that their thermal avoidance habits do not entail physiological and/or short-term behavioral strategies (e.g., noc- turnal behavior, refuge use). Nevertheless, several small mammals are regularly faced with hyperthermia risks (Caviedes- Vidal et al. 1987; Vispo and Bakken 1993; Tracy and Walsberg 2000). In these organisms, heat loss is increased by high evaporative water loss (Caviedes-Vidal et al. 1987; Hayes et al. 1998), high respiratory frequency (Gordon and Rezvani 1995), increase in peripheral blood ﬂow (Gordon and Rezvani 1995), or simply elevated thermal tolerance (Tracy and Walsberg 2000). Nevertheless, according to Gordon (1994), physiological changes are energetically expensive and, theoretically, may be used when behavioral strategies are no longer available. Such behavioral strategies used to cope with increased temperatures include postural changes, adjustments of daily activity (Vispo and Bakken 1993), and selection of cool microhabitats (Gordon 1994). The use of substrate to increment thermal loss by conductance is less studied and appears to be an important mechanism of thermoregulation in laboratory mice (Gordon et al. 2000). Although our study does not address the extent of heat lost by this behavior and does not demonstrate that ﬂattening is important for survival under warm conditions, results do

strongly suggest that at Ta above thermoneutrality flattening could be used as a heat dissipation strategy. Furthermore, our results support the idea that huddling reduces energy expen- ˙ diture (i.e.,Vo2 economy and efficiency of huddling) through lessening body-exposed body surface area (f). Decreasing exposed body surface area implies a reduction in the area to Figure 4. A, Metabolic ratio (V˙˙o of huddling individuals/Vo of non- 22volume ratio, which acts as an efficient mechanism for heat huddling individuals) as a function of Ta. B, Surface ratio (exposed surface of grouped individuals/exposed surface of ungrouped individ- conservation and energy economy. We suggest that further uals) as a function of Ta. Since the same trends were detected at studies aimed at testing the importance of flattening in ther- different mb for both variables (see Figs. 3, 4), body masses were pooled. ˙ moregulation should measure bothVo2 and body (rectal) tem- See “Results and Discussion” for details. perature in animals free to flatten and in individuals prevented from flattening, along a thermal gradient. suggest that huddled individuals reduce their contact with the substrate, as well as physical contact with other individuals, probably to minimize heat losses by conductance. At about Њ Њ 25 –28 C, there is a shift from a heat conserving strategy to a Acknowledgments heat dissipating strategy, and the surface area ratio is higher than unity (Fig. 4b). This temperature range is in close agree- We thank L. Bacigalupe and A. Mangione for a critical revision ment with the lower limit of thermoneutrality for this species of the manuscript. J. C. Opazo, M. Soto-Gamboa, and L. A. (Bozinovic et al. 1988). Ebensperger helped with captures in the field and with labo- Reported adaptive strategies for thermoregulation in cold ratory maintenance of animals. R.F.N. thanks a Comisioń Na- environments, such as nest use (Casey 1981; Redman et al. 1999), fur insulation (Conley and Porter 1986), changes in cional de Investigacioń Cientifica y Tecnolo´gica doctoral fel- thermogenic capacities (Bozinovic et al. 1990), and facultative lowship. The Universidad de Chile kindly allowed us to use heterothermia (Tracy 1977) are well documented in the liter- facilities at Rinconada de Maipu´ . This work was funded by ature. Heat dissipation strategies, however, are not often re- Fondo Nacional de Desarrollo Cientifico y Tecnolo´gico 2000002 ported, although large mammals (11 kg) have received some to R.F.N. and Fondo de Investigacioń Avanzada en A´ reas Prior- attention (Schmidt-Nielsen 1995; Dawson et al. 2000). Small itarias Centro de Estudios Avanzados en Ecologıá y Biodiver- mammals, however, are not usually studied, probably because sidad 1501-001 (program 1) to F.B.

Literature Cited havioral determination of the preferred foot pad temperature of the mouse. J Therm Biol 25:211–219. Andrews R.V. and R.W. Belknap. 1986. Bioenergetic benefits of Gordon C.J. and A.H. Rezvani. 1995. The role of temperature huddling by deer mice (Peromyscus maniculatus). Comp on neurotoxicity. Pp. 1049–1067 in L.W. Chang and R.S. Dyer, Biochem Physiol 85A:775–778. eds. Handbook of Neurotoxicology. Dekker, New York. Baer C.F. and J. Travis. 2000. Direct and correlated responses Hayes J.P., C.A. Bible, and J.D. Boone. 1998. Repeatability of to artificial selection on acute thermal stress tolerance in a mammalian physiology: evaporative water loss and oxygen livebearing fish. Evolution 54:238–244. consumption of Dipodomys merriami. J Mammal 79: Bozinovic F., F.F. Novoa, and C. Veloso. 1990. Seasonal changes 475–485. in energy expenditure and digestive tract of Abrothrix an- Hayes J.P., J.R. Speakman, and P.A. Racey. 1992. The contri- dinus (Cricetidae) in the Andes Range. Physiol Zool 63: butions of local heating and reducing exposed surface area 1216–1231. to the energetic benefits of huddling by short-tailed field Bozinovic F., M. Rosenmann, and C. Veloso. 1988. Termor- voles (Microtus agrestis). Physiol Zool 65:742–762. regulacioń conductual en Phyllotis darwini (Rodentia: Cri- Karasov W.H. 1983. Wintertime energy conservation by hud- cetidae): efecto de la temperatura ambiente, uso de nidos y dling in antelope ground squirrel (Ammospermophilus leu- agrupamiento social sobre el gasto de energıá. Rev Chil Hist curus). J Mammal 64:341–345. Nat 61:81–86. Lima M., F. Bozinovic, and F.M. Jaksic. 1997. Body mass dy- Canals M., M. Rosenmann, and F. Bozinovic. 1989. Energetics namics and growth patterns in the leaf-eared mice (Phyllotis and geometry of huddling in small mammals. J Theor Biol darwini) inhabiting a semi-arid region of Chile. Acta Theriol 141:181–189. 42:14–24. ———. 1997. Geometrical aspects of the energetic effectiveness MacArthur R.A. and M. Aleksiuk. 1979. Seasonal microenvi- of huddling in small mammals. Acta Theriol 42:321–328. ronment of the muskrat (Ondata zibethicus) in a northern Canals M., M. Rosenmann, F.F. Novoa, and F. Bozinovic. 1998. marsh. J Mammal 60:146–154. Modulating factors of the energetic effectiveness of huddling Manly B.F. 1998. Randomization, Bootstrap and Monte Carlo in small mammals. Acta Theriol 43:337–348. Methods in Biology. Chapman & Hall, London. Casey T.M. 1981. Nest insulation: energy saving to brown lem- McCracken K.G., A.D. Afton, and R.T. Alisauskas. 1997. Nest mings using a winter nest. Oecologia 50:199–204. morphology and body size of Ross and lesser snow geese. Caviedes-Vidal E., F. Bozinovic, and M. Rosenmann. 1987. Auk 114:610–618. Thermal freedom of Graomys griseoflavus in a seasonal en- McNab B.K. 1970. Body weight and the energetics of temper- vironment. Comp Biochem Physiol 87A:257–259. ature regulation. J Exp Biol 74:329–348. Conley K.E. and W.P. Porter. 1986. Heat loss from deer mice McNeill-Alexander R. 1996. Biophysical problems of small size (Peromyscus): evaluation of seasonal limits to thermoregu- in vertebrates. Pp. 3–14 in P.J. Miller, ed. Miniature Verte- lation. J Exp Biol 126:149–269. brates: The Implications of Small Body Size. Clarendon, Contreras L.C. 1984. Bioenergetics of huddling: test of a Oxford. psycho-physiological hypothesis. J Mammal 65:256–262. Merritt J.F. 1995. Seasonal thermogenesis and changes in body Dawson T.J., C.E. Blaney, A.J. Munn, A. Krockenberger, and mass of masked shrews, Sorex cinereus. J Mammal 76: S.K. Maloney. 2000. Thermoregulation by kangaroos from 1020–1035. mesic and arid habitats: influence of temperature on routes Merritt J.F., D.A. Zegers, and L.R. Rose. 2001. Seasonal ther- of heat loss in eastern grey kangaroos (Macropus giganteus) mogenesis of southern flying squirrels. J Mammal 82:51–64. and red kangaroos (Macropus rufus). Physiol Biochem Zool Redman P., C. Selman, and J.R. Speakman. 1999. Male short- 73:374–381. tailed field voles (Microtus agrestis) build better insulated Dyck A.P. and R.A. MacArthur. 1993. Seasonal variation in the nests than females. J Comp Physiol B 169:581–587. microclimate and gas composition of beaver lodges in a bo- Rezende E.L. and F. Bozinovic. 2001. Patterns of daily activity real environment. J Mammal 74:180–188. in the leaf-eared mouse (Phyllotis darwini). J Arid Environ Fedyk A. 1971. Social thermoregulation in Apodemus ilavicollis 47:95–100. (Melchior, 1834). Acta Theriol 16:221–229. Riesenfeld A. 1981. The role of body mass in thermoregulation. Feldhamer G.A., L.C. Drickamer, S.H. Vessey, and J.F. Mer- Am J Phys Anthropol 55:95–99. ritt. 1999. Mammalogy: Adaptation, Diversity and Ecology. Schmidt-Nielsen K. 1995. Scaling: Why Is Animal Size So Im- McGraw-Hill, Boston. portant? Cambridge University Press, Cambridge. Gordon C.J. 1994. 24 hour control of body temperature in rats: Sealander J.A. 1952. The relationship of nest protection and integration of behavioral and autonomic effectors. Am J huddling to survival of Peromyscus at low temperature. Ecol- Physiol 267:R71–R77. ogy 33:63–71. Gordon C.J., P. Becker, P. Killough, and B. Padnos. 2000. Be- Springer S.D., P.A. Gregory, and W. Barrett. 1981. Importance

of social grouping on bioenergetics of the golden mouse, Veloso C. and F. Bozinovic. 1993. Dietary and digestive con- Ochrotomys nuttalli. J Mammal 62:628–630. straints on basal energy metabolism in a small herbivorous Stapp P. 1992. Energetic influences on the life history of Glau- rodent. Ecology 74:2003–2010. comys volans. J Mammal 73:914–920. Vickery W.L. and J.S. Millar. 1984. The energetics of huddling Stapp P., P.J. Pekins, and W.W. Mautz. 1991. Winter energy by endotherms. Oikos 43:88–93. expenditure and the distribution of southern flying squirrels. Vispo C.R. and G.S. Bakken. 1993. The influence of thermal Can J Zool 69:2548–2555. conditions on the surface activity of thirteen-lined ground Statistica. 1997. Statistical Release 5 (Quick Reference) for the squirrels. Ecology 74:377–389. Windows 95 Operating System. 3d ed. Statsoft, Tulsa, Okla. Vogt D.F. and G.R. Lynch. 1982. Influence of ambient tem- Stewart W.E., S. Budaraju, W.P. Porter, and J. Jaeger. 1993. perature, nest availability, huddling and daily torpor on en- Prediction of forced ventilation in animal fur under ideal ergy expenditure in the white-footed mouse Peromyscus leu- pressure distribution. Funct Ecol 7:487–492. copus. Physiol Zool 55:56–63. Taylor J.R.E. 1998. Evolution of energetic strategies in shrews. Webb D.R., J.L. Fullemwider, P.A. McClure, L. Profeta, and J. Pp. 309–346 in J.M. Wojcik and M. Wolsan, eds. Evolution Long. 1990. Geometry of maternal offspring contact in two of Shrews. Mammal Research Institute, Polish Academy of Science, Warsaw. rodents. Physiol Zool 63:821–844. ˙ Tracy C.R. 1977. Minimum size of mammalian homeotherms: Withers P.C. 1977. Measurements of metabolic rate,Vco2 , and role of the thermal environment. Science 198:1034–1035. evaporative water loss with a flow through mask. J Appl Tracy C.R. and G.E. Walsberg. 2000. Unappreciated tolerance Physiol 42:120–123. to high ambient temperature in a widely distributed desert Wolf B.A. and G.E. Walsberg. 1996. Thermal effects of radiation rodent, Dipodomys merriami. Physiol Biochem Zool 73: and wind on a small bird and implications for microsite 809–818. selection. Ecology 77:2228–2236.

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