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Energy metabolism and thermoregulation in Chinchilla brevicaudata
ARTICLE IN PRESS
Journal of Thermal Biology 28 (2003) 489–495
Energy metabolism and thermoregulation in Chinchilla brevicaudata Arturo Corte! sa,*, Carlos Tiradoa, Mario Rosenmannb b
a Departamento de Biolog!ıa, Facultad de Ciencias, Universidad de La Serena, Casilla 599, La Serena, Chile ! 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 (Ta ), 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: [email protected] (A. Cort!es), [email protected] (M. Rosenmann).
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 temperature (Tb ) 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). A few exceptions are the observations in some Chilean rodents (Rosenmann, 1977; Cort!es, 1985; Cort!es 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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Nomenclature BMR C C He EWL mb MR MMR MWP Ta
basal metabolic rate (ml O2/g h) thermal conductance (ml O2/g h C) thermal conductance in He–O2 atmosphere (ml O2/g h C) evaporative water loss (mg H2O/g h) body mass (g) metabolic rate (ml O2 /g h) maximum metabolic rate (ml O2/g h) metabolic water production (mg H2O/g h) ambient temperature ( C)
of water regulation by means of the relation Ta @ MWP=EWL (MacMillen and Hinds, 1983), where Ta @ 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 regulation has also been expressed considering the energetic cost of maintenance of water balance (MR-WB), taking the value of Ta @ that permits the calculation MR-WB from the relation between MR and the species-specific ambient temperature (Corte! s et al., 2000b). Furthermore, the value of MR-WB permits the regulatory efficiency between mesic and xeric rodents to be determined (Corte! s et al., 2000b). Chinchilla brevicaudata (Waterhouse, 1848) is an hystricomorphic nocturnal rodent dwelling between 3500 to 5000 m above sea level in the Andes Range (Mun˜oz and Y!an˜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 (Jime! nez, 1996). Currently its distribution is restricted to Southern Per!u, Northeast Argentina and to the (I–III Regi!on) 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 (Jim!enez, 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 hypothesized 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–O2 (80–20%) atmosphere. EWL and body temperature (Tb ) were also measured at different ambient temperatures (Ta ). In addition, two indices Ta @ (MWP=EWL), that repre-
ambient temperature ( C), when MWP/ EWL=1 Tb body temperature ( C) Tic calculated theoretical lower critical temperature ( C) TLL calculated theoretical lower lethal temperature ( C) MR-WB energetic cost of maintaining the water balance (cal/g h) DTm minimum thermal differential between Tb and Tic ( C) Ta @
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 (25 000 S; 69 450 W) in the National Park Llul! South East of Antofagasta, Chile), laillaco (II Region, 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 21.073 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 (Ta ) were maintained 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 (Tb ) was recorded before and after each
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metabolic run with a Cole Parmer, Model 8500-40 copperconstant thermocouple. O2 consumption was also measured in 80% He–20% O2 atmosphere, which has been used to obtain the maximum metabolic rate of thermoregulation (MMR) (Rosenmann and Morrison, 1974; Holloway and Geiser, 2001). For this purpose we used a Ta 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 Ta was determined. Thermal conductance (C) was calculated from the slope of the regression (MR vs. Ta ), below thermoneutrality. The lower critical temperature (Tic ) 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 the relations: BMR=3.42m0:25 (Kleiber, 1961) and C ¼ b 1:0m0:50 (McNab and Morrison, 1963). The ratio BMR/ b C that indicates the minimum thermal differential (DTm ), between Tb and Tic ; was also calculated: DTm ¼ BMR=C ¼ Tb 2Tic (McNab, 1979). ( C)=3.42m0:25 b 2.3. Evaporative water loss Values of EWL were obtained gravimetrically (70.1 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 conducted at different Ta (5 C, 15 C, 20 C, 25 C, 30 C and 32.5 C), with an air flow of 5 l/min. All measurements started after 1 h of thermal equilibrium (Cort!es et al., 1990). Results of minimum EWL were compared with the expected values for mesic (EWL ¼ 7:272m0:532 ) b and desert rodents (EWL ¼ 5:968mb0:416 ) of similar size (Cort!es et al., 2000b).
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3. Results 3.1. Energy metabolism Linear regression of MR vs. Ta ; gave the equation MR=1.022–0.0239Ta (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 Tb (37.6 C). The slope of the curve was 0.0239 ml O2/ g h 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). DTm was 20.8 C. BMR of C. brevicaudata (0.49870.068 ml O2/g h) is equivalent to 67.2% of that expected (Kleiber, 1961). The lower critical temperature (Tic ) was 22 C. In a He–O2 atmosphere the relationship of MR vs. Ta was MR (ml O2/g h)=2.28–0.0544Ta ; whilst the thermal conductance (C He ) reached 0.0544 ml O2/g h C (Fig. 1). When Ta was lowered to 7.5 C in this artificial atmosphere, MR fell 16.9% with respect to the MMR of 2.5270.005 ml O2/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 Tb 2TLL (Bozinovic and Rosenmann, 1988) gave a theoretical critical lethal temperature (TLL ) for this species of 67.8 C, close to the value of 65.0 C obtained by extrapolating MMR (He–O2) on the regression curve of MR vs. Ta in normal air (Rosenmann, 1977; Rosenmann and Morrison, 1974). 3.2. Evaporative water loss Minimum values of EWL were found to be 0.49870.014 mg H2O/g h within the Ta range of
2.4. Efficiency of water regulation To evaluate the efficiency of water regulation we utilized two indices: Ta @ MWP ¼ EWL (MacMillen and Hinds, 1983) and MR-WB (Cort!es, 2000b). MWP was assessed from MR data vs. Ta ; assuming that 1 ml O2 consumed produce 0.62 mg of water (SchmidtNielsen, 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=34.627m0:339 and MR-WB=68.132m0:381 ; b b respectively (Cort!es et al., 2000b). 2.5. Statistical analyses Regression equations were calculated using leastsquares analyses (Steel and Torrie, 1985). Values are given as means7SD.
Fig. 1. Relationships between oxygen consumption and ambient temperature in C. brevicaudata under two different atmospheres (normal air () and He–O2 (’)).
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p20 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 H2O/ g h, representing increases of 20%, 65% and 120%, respectively, over the minimum. At the highest experimental 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 Tb increase of 1.1 C above the normothermic condition (38.7 C vs. 37.6 C) (Fig. 2).
MacMillen, 1985). Replacing Ta ¼ 10:6 C in the regression equation (MR=1.022–0.0239Ta ), we obtained a value of 3.71 cal/g h, that is the energetic cost of maintaining the water balance (MR-WB) (Cort!es et al., 2000b).
3.3. Efficiency of water regulation
C. brevicaudata showed an average BMR of 0.49870.068 ml O2/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 (Rosenmann, 1977; Bozinovic and Rosenmann, 1988; Bozinovic, 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. A comparison with a closer species indicated that BMR in C. brevicaudata reached up to 75% of that reported for Chinchilla lanigera (Corte! s et al., 2000a). Both species are herbivorous (Cort!es 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; Dawson, 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
Fig. 3 shows the relation of Log MWP/EWL vs. Ta ; which gave the equation MWP=EWL ¼ 1:705 ð0:951ÞTa : 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
Body Temperature (ºC)
40
39
38
Normothermic 37.6 + 0.28ºC.
37
Evaporative Heat Loss (% of heat production)
40
30
20
10
4. Discussion 4.1. Energy metabolism
0 1.4 MWP/EWL = 1.705 (0.951)Ta r = - 0.88 (P < 0.01)
1.2 1
1.5
MWP/EWL
Evaporative Water Loss (mg/g h)
2.0
1.0
0.5
0.8
0.6
0.4
0.0
Ta @ = 10.6ºC
0
5
10
15
20
25
30
35
Ambient Temperature (ºC ) Fig. 2. Relationships between evaporative water loss, evaporative heat loss, body temperature and ambient temperature in C. brevicaudata.
0
5
10
15
20
25
Ambient Temperature (ºC)
Fig. 3. Relation between MWP/EWL and ambient temperature in C. brevicaudata.
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where C. brevicaudata dwells. A low thermal conductance was also found in this species (C ¼ 0:0239 ml O2/ g h 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 (Rosenmann, 1977; Bozinovic and Rosenmann, 1988; Bozinovic, 1992; Bozinovic et al., 1995; Cort!es et al., 2000a). Both the high thermal insulation as well as the low Tic should allow this nocturnal species to maintain a normal Tb at low ambient temperatures. We should note that the mean annual Ta at the capture site is about 2 C (Luebert, 1998). The high thermal insulation is also reflected by a DTm ¼ 22 C. This figure is 16 C and 6.4 C higher than the minimum and maximum DTm 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 (Cort!es 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 oeconomus (5.1), Uromys caudimaculatus (4.7) (Hinds et al., 1993) and the octodontid Octodon degus (4.9) (Rosenmann, 1977). The critical lethal temperature that was calculated for C. brevicaudata (TLL ¼ 67:8 C), was similar to the one for C. lanigera (65.5 C) (Cort!es et al., 2000a), but was 51.8 C lower than that (TLL 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 H2O/ g h (Fig. 2). This value is within that expected for xeric rodents (Corte! s et al., 2000b). It is probable that similar morphological respiratory nasal adaptations occur as reported for other xeric and desert rodents (Cort!es 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 Ta ¼ 32:5 C, C. brevicaudata was able to loose by EWL only 14 of the metabolic heat production, which was reflected by a Tb 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 (Cort!es 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
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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 Ya! n˜ez, 2000). Moreover, one of us (AC) found during several summer days a relatively stable Ta 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 Ta @ 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 longicaudatus (12.1 C), C. lanigera (12.7 C) and O. degus (16.6 C) (Cort!es et al., 2000b). Nevertheless, the energetic cost of maintaining the water balance, MRWB=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 (Cort!es et al., 2000b). Because of the extreme environmental conditions endured by C. brevicaudata (low availability of food and water), we found that this physiological feature was not surprising.
Acknowledgements ! Nacional Forestal (CONWe thank the Corporacion ! Chile) for logistic assistance, mainly to AF, II Region, the wildlife keepers Rodrigo Araya and Alfonso Tapia (Parque Nacional Llullaillaco). We also thank Dr. Jaime Jim!enez (Universidad de Los Lagos) for his valuable collaboration in the field. This work was financed by the projects FONDECYT 5960017, Programa Sectorial ! Nacional Biomas y Climas del Norte de Chile, Comision ! Cient!ıfica y Tecnologica ! de Investigacion de Chile (CONICYT), and Project FONDECYT 1981122.
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Shkolink, A., Borut, A., 1969. Temperature and water relations in two species of spiny mice (Acomys). J. Mammal. 50, 245–255. Shkolnik, A., Schmidt-Nielsen, K., 1976. Temperature regulation in hedgehogs from temperate and desert environment. Physiol. Zool. 49, 54–56. Schmidt-Nielsen, K., 1979. Desert Animals: Physiological Problems of Heat and Water. Dover Publications, Inc., New York, 277pp. Schmidt-Nielsen, K., 1990. Animal Physiology: Adaptation and Environment. Cambridge University Press, Cambridge, 583pp. Speakman, J.R., 2000. The cost of living: field metabolic rates of small mammals. Adv. Ecol. Res. 30, 178–297. Steel, R.G.D., Torrie, J.H., 1985. Bioestad!ıstica: Principios y Aplicaciones. McGraw-Hill, Bogot!a, Colombia, 340pp.
Journal of Thermal Biology 28 (2003) 489–495
Energy metabolism and thermoregulation in Chinchilla brevicaudata Arturo Corte! sa,*, Carlos Tiradoa, Mario Rosenmannb b
a Departamento de Biolog!ıa, Facultad de Ciencias, Universidad de La Serena, Casilla 599, La Serena, Chile ! 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 (Ta ), 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: [email protected] (A. Cort!es), [email protected] (M. Rosenmann).
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 temperature (Tb ) 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). A few exceptions are the observations in some Chilean rodents (Rosenmann, 1977; Cort!es, 1985; Cort!es 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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Nomenclature BMR C C He EWL mb MR MMR MWP Ta
basal metabolic rate (ml O2/g h) thermal conductance (ml O2/g h C) thermal conductance in He–O2 atmosphere (ml O2/g h C) evaporative water loss (mg H2O/g h) body mass (g) metabolic rate (ml O2 /g h) maximum metabolic rate (ml O2/g h) metabolic water production (mg H2O/g h) ambient temperature ( C)
of water regulation by means of the relation Ta @ MWP=EWL (MacMillen and Hinds, 1983), where Ta @ 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 regulation has also been expressed considering the energetic cost of maintenance of water balance (MR-WB), taking the value of Ta @ that permits the calculation MR-WB from the relation between MR and the species-specific ambient temperature (Corte! s et al., 2000b). Furthermore, the value of MR-WB permits the regulatory efficiency between mesic and xeric rodents to be determined (Corte! s et al., 2000b). Chinchilla brevicaudata (Waterhouse, 1848) is an hystricomorphic nocturnal rodent dwelling between 3500 to 5000 m above sea level in the Andes Range (Mun˜oz and Y!an˜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 (Jime! nez, 1996). Currently its distribution is restricted to Southern Per!u, Northeast Argentina and to the (I–III Regi!on) 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 (Jim!enez, 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 hypothesized 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–O2 (80–20%) atmosphere. EWL and body temperature (Tb ) were also measured at different ambient temperatures (Ta ). In addition, two indices Ta @ (MWP=EWL), that repre-
ambient temperature ( C), when MWP/ EWL=1 Tb body temperature ( C) Tic calculated theoretical lower critical temperature ( C) TLL calculated theoretical lower lethal temperature ( C) MR-WB energetic cost of maintaining the water balance (cal/g h) DTm minimum thermal differential between Tb and Tic ( C) Ta @
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 (25 000 S; 69 450 W) in the National Park Llul! South East of Antofagasta, Chile), laillaco (II Region, 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 21.073 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 (Ta ) were maintained 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 (Tb ) was recorded before and after each
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metabolic run with a Cole Parmer, Model 8500-40 copperconstant thermocouple. O2 consumption was also measured in 80% He–20% O2 atmosphere, which has been used to obtain the maximum metabolic rate of thermoregulation (MMR) (Rosenmann and Morrison, 1974; Holloway and Geiser, 2001). For this purpose we used a Ta 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 Ta was determined. Thermal conductance (C) was calculated from the slope of the regression (MR vs. Ta ), below thermoneutrality. The lower critical temperature (Tic ) 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 the relations: BMR=3.42m0:25 (Kleiber, 1961) and C ¼ b 1:0m0:50 (McNab and Morrison, 1963). The ratio BMR/ b C that indicates the minimum thermal differential (DTm ), between Tb and Tic ; was also calculated: DTm ¼ BMR=C ¼ Tb 2Tic (McNab, 1979). ( C)=3.42m0:25 b 2.3. Evaporative water loss Values of EWL were obtained gravimetrically (70.1 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 conducted at different Ta (5 C, 15 C, 20 C, 25 C, 30 C and 32.5 C), with an air flow of 5 l/min. All measurements started after 1 h of thermal equilibrium (Cort!es et al., 1990). Results of minimum EWL were compared with the expected values for mesic (EWL ¼ 7:272m0:532 ) b and desert rodents (EWL ¼ 5:968mb0:416 ) of similar size (Cort!es et al., 2000b).
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3. Results 3.1. Energy metabolism Linear regression of MR vs. Ta ; gave the equation MR=1.022–0.0239Ta (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 Tb (37.6 C). The slope of the curve was 0.0239 ml O2/ g h 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). DTm was 20.8 C. BMR of C. brevicaudata (0.49870.068 ml O2/g h) is equivalent to 67.2% of that expected (Kleiber, 1961). The lower critical temperature (Tic ) was 22 C. In a He–O2 atmosphere the relationship of MR vs. Ta was MR (ml O2/g h)=2.28–0.0544Ta ; whilst the thermal conductance (C He ) reached 0.0544 ml O2/g h C (Fig. 1). When Ta was lowered to 7.5 C in this artificial atmosphere, MR fell 16.9% with respect to the MMR of 2.5270.005 ml O2/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 Tb 2TLL (Bozinovic and Rosenmann, 1988) gave a theoretical critical lethal temperature (TLL ) for this species of 67.8 C, close to the value of 65.0 C obtained by extrapolating MMR (He–O2) on the regression curve of MR vs. Ta in normal air (Rosenmann, 1977; Rosenmann and Morrison, 1974). 3.2. Evaporative water loss Minimum values of EWL were found to be 0.49870.014 mg H2O/g h within the Ta range of
2.4. Efficiency of water regulation To evaluate the efficiency of water regulation we utilized two indices: Ta @ MWP ¼ EWL (MacMillen and Hinds, 1983) and MR-WB (Cort!es, 2000b). MWP was assessed from MR data vs. Ta ; assuming that 1 ml O2 consumed produce 0.62 mg of water (SchmidtNielsen, 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=34.627m0:339 and MR-WB=68.132m0:381 ; b b respectively (Cort!es et al., 2000b). 2.5. Statistical analyses Regression equations were calculated using leastsquares analyses (Steel and Torrie, 1985). Values are given as means7SD.
Fig. 1. Relationships between oxygen consumption and ambient temperature in C. brevicaudata under two different atmospheres (normal air () and He–O2 (’)).
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p20 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 H2O/ g h, representing increases of 20%, 65% and 120%, respectively, over the minimum. At the highest experimental 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 Tb increase of 1.1 C above the normothermic condition (38.7 C vs. 37.6 C) (Fig. 2).
MacMillen, 1985). Replacing Ta ¼ 10:6 C in the regression equation (MR=1.022–0.0239Ta ), we obtained a value of 3.71 cal/g h, that is the energetic cost of maintaining the water balance (MR-WB) (Cort!es et al., 2000b).
3.3. Efficiency of water regulation
C. brevicaudata showed an average BMR of 0.49870.068 ml O2/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 (Rosenmann, 1977; Bozinovic and Rosenmann, 1988; Bozinovic, 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. A comparison with a closer species indicated that BMR in C. brevicaudata reached up to 75% of that reported for Chinchilla lanigera (Corte! s et al., 2000a). Both species are herbivorous (Cort!es 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; Dawson, 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
Fig. 3 shows the relation of Log MWP/EWL vs. Ta ; which gave the equation MWP=EWL ¼ 1:705 ð0:951ÞTa : 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
Body Temperature (ºC)
40
39
38
Normothermic 37.6 + 0.28ºC.
37
Evaporative Heat Loss (% of heat production)
40
30
20
10
4. Discussion 4.1. Energy metabolism
0 1.4 MWP/EWL = 1.705 (0.951)Ta r = - 0.88 (P < 0.01)
1.2 1
1.5
MWP/EWL
Evaporative Water Loss (mg/g h)
2.0
1.0
0.5
0.8
0.6
0.4
0.0
Ta @ = 10.6ºC
0
5
10
15
20
25
30
35
Ambient Temperature (ºC ) Fig. 2. Relationships between evaporative water loss, evaporative heat loss, body temperature and ambient temperature in C. brevicaudata.
0
5
10
15
20
25
Ambient Temperature (ºC)
Fig. 3. Relation between MWP/EWL and ambient temperature in C. brevicaudata.
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where C. brevicaudata dwells. A low thermal conductance was also found in this species (C ¼ 0:0239 ml O2/ g h 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 (Rosenmann, 1977; Bozinovic and Rosenmann, 1988; Bozinovic, 1992; Bozinovic et al., 1995; Cort!es et al., 2000a). Both the high thermal insulation as well as the low Tic should allow this nocturnal species to maintain a normal Tb at low ambient temperatures. We should note that the mean annual Ta at the capture site is about 2 C (Luebert, 1998). The high thermal insulation is also reflected by a DTm ¼ 22 C. This figure is 16 C and 6.4 C higher than the minimum and maximum DTm 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 (Cort!es 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 oeconomus (5.1), Uromys caudimaculatus (4.7) (Hinds et al., 1993) and the octodontid Octodon degus (4.9) (Rosenmann, 1977). The critical lethal temperature that was calculated for C. brevicaudata (TLL ¼ 67:8 C), was similar to the one for C. lanigera (65.5 C) (Cort!es et al., 2000a), but was 51.8 C lower than that (TLL 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 H2O/ g h (Fig. 2). This value is within that expected for xeric rodents (Corte! s et al., 2000b). It is probable that similar morphological respiratory nasal adaptations occur as reported for other xeric and desert rodents (Cort!es 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 Ta ¼ 32:5 C, C. brevicaudata was able to loose by EWL only 14 of the metabolic heat production, which was reflected by a Tb 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 (Cort!es 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
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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 Ya! n˜ez, 2000). Moreover, one of us (AC) found during several summer days a relatively stable Ta 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 Ta @ 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 longicaudatus (12.1 C), C. lanigera (12.7 C) and O. degus (16.6 C) (Cort!es et al., 2000b). Nevertheless, the energetic cost of maintaining the water balance, MRWB=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 (Cort!es et al., 2000b). Because of the extreme environmental conditions endured by C. brevicaudata (low availability of food and water), we found that this physiological feature was not surprising.
Acknowledgements ! Nacional Forestal (CONWe thank the Corporacion ! Chile) for logistic assistance, mainly to AF, II Region, the wildlife keepers Rodrigo Araya and Alfonso Tapia (Parque Nacional Llullaillaco). We also thank Dr. Jaime Jim!enez (Universidad de Los Lagos) for his valuable collaboration in the field. This work was financed by the projects FONDECYT 5960017, Programa Sectorial ! Nacional Biomas y Climas del Norte de Chile, Comision ! Cient!ıfica y Tecnologica ! de Investigacion de Chile (CONICYT), and Project FONDECYT 1981122.
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