Dynamic Thermal Balance in the Leaf‐Eared Mouse

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Dynamic Thermal Balance in the Leaf‐Eared Mouse 396 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 Ecologı´a y Biodiversidad, Departamento de Ecologı´a, 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 de- mands. 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.
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