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Journal of Thermal Biology 28 (2003) 489–495ARTICLE IN PRESS Energy metabolism and thermoregulation in Chinchilla brevicaudata Arturo Cortes ! a , *,

IN PRESS Journal of Thermal Biology 28 (2003) 489–495 Energy metabolism and thermoregulation in Chinchilla

Energy metabolism and thermoregulation in Chinchilla brevicaudata

Arturo Cortes! a, *, Carlos Tirado a , Mario Rosenmann b

a Departamento de Biolog!ıa, Facultad de Ciencias, Universidad de La Serena, Casilla 599, La Serena, Chile

b Departamento de Ciencias Ecologicas,!

Facultad de Ciencias, Universidad de Chile, Casilla 653, Santiago, Chile

Received 6 November 2002; accepted 6 June 2003

Abstract

Chinchilla brevicaudata lives at 3500–5000 m, with high ambient temperatures during the day but cold at night. In this Andean habitat there is also low availability of food and water resources. Physiological attributes that may minimize their energetic cost as well as the water requirements are: (1) Low values of basal metabolic rate (67.2%) and thermal conductance (51.0%) compared to predicted values. (2) The aerobic metabolic expansivity was 5.1, while the calculated theoretical critical lethal temperature was extremely low ( 67.8 C). (3) The energetic cost for maintenance of water balance was 85.3% of the predicted value for xeric rodents of similar size. r 2003 Elsevier Ltd. All rights reserved.

Keywords: Chinchilla brevicaudata; Basal metabolism; Maximum metabolism; Thermal conductance; Evaporative water loss

1. Introduction

In xeric environments, the ambient temperature (T a ), the photoperiod and the availability of food and water are the main variables that present the largest daily and seasonal variations (Degen, 1997; Kronfeld-Schor et al., 2000). Consequently, organisms that live in these environments should be able to maintain homeostatic conditions, particularly in their water and energy equilibrium. In mammals, one of the most utilized energetic parameters is the basal metabolic rate (BMR), which is the main component of the energy spent under laboratory as well as in natural conditions (Cruz-Neto et al., 2001). For some wild mammals BMR may represent 50% of the daily energy expenditure (Nagy et al., 1999; Speakman, 2000). Variations of BMR among homeotherms have been basically explained by allometric relations of body mass (Kleiber, 1961). More recently the residual variance of

*Corresponding author. E-mail addresses: acortes@userena.cl (A. Cortes),! ma@abello.dic.uchile.cl (M. Rosenmann).

mrosen-

this correlation has been applied at taxonomic level (Hayssen and Lacy, 1985) or in relation to food habits (McNab, 1986), ambient temperature (MacMillen and Garland, 1989), and habitat (McNab and Morrison, 1963; Hulbert and Dawson, 1974; Shkolnik and Schmidt-Nielsen, 1976; Lovegrove, 1986; Lovegrove et al., 1991). In nature most homeotherms keep their body tem- perature (T b ) within certain limits. This condition depends on some physiological characteristics, such as the metabolic rate (MR) and thermal conductance (C). McNab (1979) found that granivorous rodents from xeric habitats have low BMR, avoiding risks of hyperthermia and maintaining their water economy by minimizing evaporative water loss (EWL). This last feature has been greatly neglected in studies in South American mesic and xeric rodents, in spite of the fact that EWL plays an important role in thermoregulation and water balance (Degen, 1997). Afew exceptions are the observations in some Chilean rodents (Rosenmann, 1977; Cortes,! 1985; Cortes! et al., 1988, 1990, 2000a, b; Bozinovic et al., 1995). In rodents, the metabolic water production (MWP) and the EWL are utilized to evaluate the efficiency

0306-4565/03/$ - see front matter r 2003 Elsevier Ltd. All rights reserved.

doi:10.1016/S0306-4565(03)00049-4

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et al. / Journal of Thermal Biology 28 (2003) 489–495

Nomenclature

BMR

basal metabolic rate (ml O 2 /g h)

C

thermal conductance (ml O 2 /g h C)

C He thermal

conductance in He–O 2 atmosphere

(ml O 2 /g h C)

EWL evaporative water loss (mg H 2 O/g h)

m b

MR metabolic rate (ml O 2 /g h) MMR maximum metabolic rate (ml O 2 /g h)

MWP metabolic water production (mg H 2 O/g h)

T a

body mass (g)

ambient temperature ( C)

T a @ ambient temperature ( C), when MWP/

EWL=1

T b body temperature ( C) T ic calculated theoretical lower critical tempera- ture ( C) T LL calculated theoretical lower lethal temperature ( C) MR-WB energetic cost of maintaining the water balance (cal/g h) D T m minimum thermal differential between T b and T ic ( C)

of water regulation by means of the relation T a @ MWP=EWL (MacMillen and Hinds, 1983), where T a @ is the ambient temperature when MWP/EWL=1. If temperature and humidity are kept constant this index is not affected by the animal’s activity (Raab and Schmidt-Nielsen, 1972). The efficiency of water regula- tion has also been expressed considering the energetic cost of maintenance of water balance (MR-WB), taking the value of T a @ that permits the calculation MR-WB from the relation between MR and the species-specific ambient temperature (Cortes! et al., 2000b). Further- more, the value of MR-WB permits the regulatory efficiency between mesic and xeric rodents to be determined (Cortes! et al., 2000b). Chinchilla brevicaudata (Waterhouse, 1848) is an hystri- comorphic nocturnal rodent dwelling between 3500 to 5000 m above sea level in the Andes Range (Mun˜oz and Yan! ˜ez, 2000). Due to the special quality of the fur, the species was intensively hunted and a great part of the Chilean populations was extinguished or significantly diminished (Jimenez,! 1996). Currently its distribution is restricted to Southern Peru,! Northeast Argentina and to the (I–III Region)! of Northern Chile (Redford and Einsenberg, 1989). Conservation problems have been noted and it has been considered in critical danger in Argentina (Garc!ıa et al., 1997) and in risk of extinction in Chile (Glade, 1993; SAG, 2000). Ecophysiological studies in C. brevicaudata are few, but some ecological and conservation aspects have been reported (Jimenez,! 1996). The combined effects of physiological, morphological, behavioral and ecological attributes allow desert rodents to minimize the energetic costs and assure their survival in these harsh environments (Bozinovic and Contreras, 1990; Prakash, 2001). Because of the extreme climatic conditions of the Andean range, we hypothe- sized that C. brevicaudata would present most, if not all of these features. To test this idea we measured oxygen consumption in normal air and under He–O 2 (80–20%) atmosphere. EWL and body temperature (T b ) were also measured at different ambient temperatures (T a ). In addition, two indices T a @ (MWP=EWL), that repre-

sents the efficiency of water regulation, and MR-WB, representing the energetic cost of maintaining the water balance, were estimated.

2. Materials and methods

2.1. Experimental animals

Five individuals of C. brevicaudata (2 ## , 3~~ ) were captured with National traps in the locality of El Morro Negro (25 00 0 S; 69 45 0 W) in the National Park Llul- laillaco (II Region,! South East of Antofagasta, Chile), between 3000 and 5000 m of altitude. This area is characterized by a perarid climate (di Castri and Hajek, 1976), with an annual precipitation of 20–50 mm (Messerli et al., 1993) and a mean annual temperature of 2 C (Luebert, 1998). At the site of capture we found scant vegetation, covering less than 9% of the ground surface. One of us (AC) found the following proportions of shrubs and herbs: Baccharis tola (0.05%), Adesmia eranicea (0.08%), Adesmia caespitosa (0.05%), Cristaria andicola (0.06%), Fabiana bryoides (5.10%) and Stipa chrysophylla (3.55%). The captured animals were transported to the laboratory and maintained under natural photoperiod in individual cages, with water and food (barley and alfalfa) ad libitum. At the laboratory, ambient temperature was 21.0 7 3 C, while relative humidity averaged 60%.

2.2. Energy metabolism

All oxygen consumption measurements were conducted individually with a modified automatic closed-system respirometer, based on the manometric design of Morrison (1951). Animals were in postabsortive state (2–3 h after feeding). Different ambient temperatures (T a ) were main- tained within 70.1 C in a water–glycol bath in which the metabolic chambers were submerged. Average body mass of our five experimental animals was 454.4762.5 g. Body temperature (T b ) was recorded before and after each

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metabolic run with a Cole Parmer, Model 8500-40 copper- constant thermocouple. O 2 consumption was also mea- sured in 80% He–20% O 2 atmosphere, which has been used to obtain the maximum metabolic rate of thermo- regulation (MMR) (Rosenmann and Morrison, 1974; Holloway and Geiser, 2001). For this purpose we used a T a range of 5 C to 7.5 C (Bozinovic and Rosenmann, 1989). Metabolic values were determined from the average of the three minimum periods of 3–5 min of each experimental trial which lasted 1–3 h (Rosenmann and Morrison, 1974). BMR was similarly estimated from the lowest three MR values when independence of T a was

determined. Thermal conductance (C) was calculated from the slope of the regression (MR vs. T a ), below thermo- neutrality. The lower critical temperature (T ic ) was inferred by the intersection of C with BMR. Values of BMR, C; and the endothermic limit were compared with the expected values for mammals of similar size using

(Kleiber, 1961) and C ¼

(McNab and Morrison, 1963). The ratio BMR/

C that indicates the minimum thermal differential (D T m ),

between T b and T ic ; was also calculated: D T m ¼ BMR=C

( C)=3.42m

the relations: BMR=3.42m

1:0m

0:50

b

0:25

b

b

0:25

¼ T b 2T ic (McNab, 1979).

2.3. Evaporative water loss

Values of EWL were obtained gravimetrically (7 0.1 mg) from the average of three minimum 5 min periods during 2–3 h of measurements, following the method of Hainsworth (1968). EWL trials were con- ducted at different T a (5 C, 15 C, 20 C, 25 C, 30 C and 32.5 C), with an air flow of 5 l/min. All measure- ments started after 1 h of thermal equilibrium (Cortes! et al., 1990). Results of minimum EWL were compared with the expected values for mesic (EWL ¼ 7:272m

) of similar size

)

and desert rodents (EWL ¼ 5:968m (Cortes! et al., 2000b).

0:532

b

0:416

b

2.4. Efficiency of water regulation

To evaluate the efficiency of water regulation we utilized two indices: T a @ MWP ¼ EWL (MacMillen and Hinds, 1983) and MR-WB (Cortes,! 2000b). MWP was assessed from MR data vs. T a ; assuming that 1 ml O 2 consumed produce 0.62 mg of water (Schmidt-

Nielsen, 1979) and 4.8 cal (Schmidt-Nielsen, 1990). The magnitude of MR-WB was compared with the expected values for mesic and xeric rodents, using the relations

MR-WB=34.627m

;

respectively (Cortes! et al., 2000b).

0:339

b

and MR-WB=68.132m

b

0:381

2.5. Statistical analyses

Regression equations were calculated using least- squares analyses (Steel and Torrie, 1985). Values are given as means7 SD.

3. Results

3.1. Energy metabolism

Linear regression of MR vs. T a ; gave the equation MR=1.022–0.0239T a (Fig. 1). Extrapolation of MR to 0 gave the theoretical body temperature of 42.8 C, which is 5.2 C higher than the normothermic T b (37.6 C). The slope of the curve was 0.0239 ml O 2 / gh C, and represents the thermal conductance in normal air. This value is equivalent to 51.0% of that expected for its body size (McNab and Morrison, 1963). D T m was 20.8 C. BMR of C. brevicaudata (0.498 7 0.068 ml O 2 /g h) is equivalent to 67.2% of that expected (Kleiber, 1961). The lower critical temperature (T ic ) was 22 C. In a He–O 2 atmosphere the relationship of MR vs. T a was MR (ml O 2 /g h)=2.28–0.0544T a ; whilst the thermal conductance (C He ) reached 0.0544 ml

O 2 /g h C (Fig. 1). When T a was lowered to 7.5 C in this artificial atmosphere, MR fell 16.9% with respect to the MMR of 2.52 7 0.005 ml O 2 /g h, indicating that the thermoregulatory capability was exceeded (Fig. 1). The aerobic metabolic expansivity, calculated as the ratio MMR/BMR, was found to be 5.1. This figure gives an indication of the animal’s thermoregulatory ability under low temperatures. The relation MMR=C ¼ T b 2T LL (Bozinovic and Rosenmann, 1988) gave a theoretical critical lethal temperature (T LL ) for this species of 67.8 C, close to the value of 65.0 C obtained by extrapolating MMR (He–O 2 ) on the regression curve of MR vs. T a in normal air (Rosen- mann, 1977; Rosenmann and Morrison, 1974).

3.2. Evaporative water loss

Minimum values of EWL were found to be 0.4987 0.014 mg H 2 O/g h
Minimum
values
of
EWL
were
found
to
be
0.4987 0.014 mg
H 2 O/g h
within
the
T a
range
of
be 0.4987 0.014 mg H 2 O/g h within the T a range of Fig. 1.

Fig. 1. Relationships between oxygen consumption and ambi- ent temperature in C. brevicaudata under two different atmo- spheres (normal air ( ) and He–O 2 ( )).

Body Temperature (ºC)

Evaporative Heat Loss of heat producti on)(%

Evaporative Water Loss (mg/g h)

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p 20 C (Fig. 2), while the averages of EWL at 25 C, 30 C and 32.5 C were 0.604, 0.820 and 1.105 mg H 2 O/ g h, representing increases of 20%, 65% and 120%, respectively, over the minimum. At the highest experi- mental temperature EWL was equivalent to only 24.6% of the basal rate of heat production (2.39 cal/g h). The low cooling capability was reflected in a T b increase of 1.1 C above the normothermic condition (38.7 C vs. 37.6 C) (Fig. 2).

3.3. Efficiency of water regulation

Fig. 3 shows the relation of Log MWP/EWL vs. T a ; which gave the equation MWP=EWL ¼ 1:705 ð0:951Þ T a : Taking MWP/EWL=1, we obtained a value of 10.6 C, that represents the efficiency index of water regulation for C. brevicaudata (see Hinds and

40

39

38

37

40 39 38 37 40 30 20 10 0 2.0 1.5 1.0 0.5 0.0

40

30

20

10

0

2.0

1.5

1.0

0.5

0.0

Normothermic 37.6 + 0.28ºC.
Normothermic
37.6 + 0.28ºC.
1.5 1.0 0.5 0.0 Normothermic 37.6 + 0.28ºC. 0 5 10 15 20 25 30 35
1.5 1.0 0.5 0.0 Normothermic 37.6 + 0.28ºC. 0 5 10 15 20 25 30 35
1.5 1.0 0.5 0.0 Normothermic 37.6 + 0.28ºC. 0 5 10 15 20 25 30 35
1.5 1.0 0.5 0.0 Normothermic 37.6 + 0.28ºC. 0 5 10 15 20 25 30 35
1.5 1.0 0.5 0.0 Normothermic 37.6 + 0.28ºC. 0 5 10 15 20 25 30 35
1.5 1.0 0.5 0.0 Normothermic 37.6 + 0.28ºC. 0 5 10 15 20 25 30 35
1.5 1.0 0.5 0.0 Normothermic 37.6 + 0.28ºC. 0 5 10 15 20 25 30 35
1.5 1.0 0.5 0.0 Normothermic 37.6 + 0.28ºC. 0 5 10 15 20 25 30 35
1.5 1.0 0.5 0.0 Normothermic 37.6 + 0.28ºC. 0 5 10 15 20 25 30 35

0

5

10

15

20

25

30

35

Ambient Temperature (ºC )

Fig. 2. Relationships between evaporative water loss, evapora- tive heat loss, body temperature and ambient temperature in C. brevicaudata.

MacMillen, 1985). Replacing T a ¼ 10:6 C in the regres- sion equation (MR=1.022–0.0239T a ), we obtained a value of 3.71 cal/g h, that is the energetic cost of maintaining the water balance (MR-WB) (Cortes! et al., 2000b).

4. Discussion

4.1. Energy metabolism

C. brevicaudata showed an average BMR of 0.4987 0.068 ml O 2 /g h, which is equivalent to 67.3% of the predicted value for a mammal of similar size (Kleiber, 1961) and to 34% of the average given for South American octodontid and murid rodents (Rosen- mann, 1977; Bozinovic and Rosenmann, 1988; Bozino- vic, 1992; Bozinovic et al., 1995); but in these comparisons we should consider that our species is twice the body size of the largest octodontid measured. Acomparison with a closer species indicated that BMR in C. brevicaudata reached up to 75% of that reported for Chinchilla lanigera (Cortes! et al., 2000a). Both species are herbivorous (Cortes! et al., 2002), and following the proposition of McNab (1986), their BMR should be somewhat higher than that expected for granivorous heteromyids and murids from North American and Australian deserts (McNab, 1979; Daw- son, 1955; Carpenter, 1966; MacMillen and Lee, 1970), and also higher than some murids from Asian deserts (Shkolink and Borut, 1969). Our data did not confirm McNab’s proposition. Here BMR values were similar to those reported for the other groups of desert rodents. The fact that some species may possess a lower than expected BMR is favorable for the maintenance of energy and water balance, especially for those species inhabiting arid environments with extreme climatic conditions as found in the highlands of Northern Chile

1.4 MWP/EWL = 1.705 (0.951) Ta 1.2 r = - 0.88 (P < 0.01) 1
1.4
MWP/EWL = 1.705 (0.951) Ta
1.2
r = - 0.88 (P < 0.01)
1
0.8
0.6
0.4
T a @ = 10.6ºC
0
5
10
15
20
25
MWP/EWL

Ambient Temperature (ºC)

Fig. 3. Relation between MWP/EWL and ambient temperature in C. brevicaudata.

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where C. brevicaudata dwells. Alow thermal conduc- tance was also found in this species (C ¼ 0:0239 ml O 2 / gh C), equivalent to half of that predicted for body size (McNab and Morrison, 1963). In fact, this is the lowest conductance reported for South American rodents, including murids, octodontids and chinchillids (Rosen- mann, 1977; Bozinovic and Rosenmann, 1988; Bozino- vic, 1992; Bozinovic et al., 1995; Cortes! et al., 2000a). Both the high thermal insulation as well as the low T ic should allow this nocturnal species to maintain a normal T b at low ambient temperatures. We should note that the mean annual T a at the capture site is about 2 C (Luebert, 1998). The high thermal insulation is also reflected by a D T m ¼ 22 C. This figure is 16 C and 6.4 C higher than the minimum and maximum DT m values reported for cricetids from South America (Bozinovic and Rosenmann, 1988), and also higher than the reported for some North American heteromyids (Hinds and MacMillen, 1985). The aerobic metabolic expansivity, (MMR/BMR) in C. breviaudata, was 5.1, somewhat lower than the value of 5.8 reported for

C. lanigera (Cortes! et al., 2000a), and is clearly lower

than 8.2, found in the Andean murid Calomys ducilla (Rosenmann and Morrison, 1974), but is of similar magnitude to the values reported for Microtus oecono- mus (5.1), Uromys caudimaculatus (4.7) (Hinds et al., 1993) and the octodontid Octodon degus (4.9) (Rosen- mann, 1977).

The critical lethal temperature that was calculated for C. brevicaudata (T LL ¼ 67:8 C), was similar to the one for C. lanigera ( 65.5 C) (Cortes! et al., 2000a), but was 51.8 C lower than that (T LL ¼ 16 C) given for

C. ducilla (Rosenmann and Morrison, 1974).

4.2. Evaporative water loss

Minimum EWL in our chinchilla was 0.498 mg H 2 O/ gh (Fig. 2). This value is within that expected for xeric rodents (Cortes! et al., 2000b). It is probable that similar morphological respiratory nasal adaptations occur as reported for other xeric and desert rodents (Cortes! et al., 1990). In any case, the low EWL may have unfavorable consequences at high temperatures where evaporative heat loss is important; for example, at T a ¼ 32:5 C,

C.

metabolic heat production, which was reflected by a T b

increase of 1.1 C. This moderate increase was seen to affect its normal conditions. Similar responses to moderate high temperatures have been reported in O. degus (Rosenmann, 1977) and in C. lanigera (Cortes! et al., 2000a). The low EWL of the chinchilla may appear unfavorable at high temperatures, but this physiological response is valuable for the maintenance of body water, considering that this species inhabits highly xeric environments where the only water source may be found in the few plants that are normally

brevicaudata was able to loose by EWL only 4 of the

1

consumed (e.g., S. chrysophylla, A. eranicea, F. bryoides, C. andicola and B. tola). In the same context, it is quite likely that the high ambient temperatures occurring around noon may not have significant consequences on the animal’s thermoregulation, because of the nocturnal habits described in this chinchilla (Mun˜oz and Yan! ˜ez, 2000). Moreover, one of us (AC) found during several summer days a relatively stable T a range of 20–25 C inside the dens or shelters, which are build under or between large (2–3 m) rocks.

4.3. Efficiency of water regulation

A T a @ of 10.6 C was calculated for C. brevicaudata (Fig. 3). This value may indicate a slightly lower efficiency compared with other Chilean rodents from mesic and xeric habits: Abrothrixs olivaceus (18.6 C), A. andinus (12.5 C), Phyllotis darwini (14 C), P. magister (10.5 C), P. rupestris (12.1 C), Oligoryzomys longicau- datus (12.1 C), C. lanigera (12.7 C) and O. degus (16.6 C) (Cortes! et al., 2000b). Nevertheless, the energetic cost of maintaining the water balance, MR- WB=3.71 cal/g h, was similar or lower than the values reported for the other rodent species. In fact, the energetic cost in our studied chinchilla is the lowest so far described, being only 82% of the predicted value (Cortes! et al., 2000b). Because of the extreme environ- mental conditions endured by C. brevicaudata (low availability of food and water), we found that this physiological feature was not surprising.

Acknowledgements

We thank the Corporacion! Nacional Forestal (CON- AF, II Region,! Chile) for logistic assistance, mainly to the wildlife keepers Rodrigo Araya and Alfonso Tapia (Parque Nacional Llullaillaco). We also thank Dr. Jaime Jimenez! (Universidad de Los Lagos) for his valuable collaboration in the field. This work was financed by the projects FONDECYT 5960017, Programa Sectorial Biomas y Climas del Norte de Chile, Comision! Nacional de Investigacion! Cient!ıfica y Tecnologica! de Chile

(CONICYT), and Project FONDECYT 1981122.

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