metabolic rate, thermoregulation and water balance in lagidium viscacia inhabiting the arid andean...
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Journal of Thermal Biology 32 (2007) 220–226
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Metabolic rate, thermoregulation and water balance inLagidium viscacia inhabiting the arid Andean plateau
Carlos Tiradoa,b, Arturo Cortesa,b, Francisco Bozinovicc,�
aDepartamento de Biologıa, Facultad de Ciencias, Universidad de La Serena, Chile Casilla 599, ChilebCentro de Estudios Avanzados en Zonas Aridas, La Serena, Chile
cCenter for Advanced Studies in Ecology and Biodiversity, Departmento de Ecologıa, Facultad de Ciencias Biologicas,
Pontificia Universidad Catolica de Chile, Santiago 6513677, Chile
Received 20 November 2006; accepted 10 January 2007
Abstract
Lagidium viscacia inhabits where water and food availability is low. We hypothesize that this rodent should minimize metabolic rate
and water loss in order to cope with such extreme environments. We observed that Lagidium viscacia has (1) a comparatively lower basal
metabolic rate (67%) and thermal conductance (78%) of predicted; (2) a higher pulmocutaneous evaporation rate which is 36% (mesic)
and 63% (xeric); and (3) energetic cost of maintaining the water balance similar to that expected for rodents from xeric environments
(2.8 cal/g h). In summary, Lagidium viscacia has physiological traits that favour energy and water economy to cope with such extreme
habitats.
r 2007 Elsevier Ltd. All rights reserved.
Keywords: Basal metabolic rate; Evaporative water loss; Lagidium viscacia; Oxygen consumption; South American rodents; Thermoregulation; Water
deprivation; Water economy
1. Introduction
Rodents from xeric and mesic environments havegenerally physiological specializations and behaviouralstrategies which allow them to minimize energy and watersuch as low metabolic rates, low evaporative water loss(EWL) rates, torpor, nocturnal and/or crepuscular activity(Buffenstein, 1985; Cortes, 1985; Cortes et al., 1988, 1990;Downs and Perrin, 1994, 1996; Prakash, 2001; Bozinovicand Gallardo, 2006).
Rodents and other mammals, regardless of the habitat,keep their body temperature (Tb) between 371 and 381,which implies low energetic cost depending on the thermalload of the habitat (Walsberg, 2000). The minimum energy
e front matter r 2007 Elsevier Ltd. All rights reserved.
erbio.2007.01.003
ing author. Center for Advanced Studies in Ecology and
epartmento de Ecologıa, Facultad de Ciencias Biologicas,
ersidad Catolica de Chile, Santiago 6513677, Chile.
2618; fax: +56 2 686 2621.
esses: [email protected] (A. Cortes),
.puc.cl (F. Bozinovic).
expenditure related to the maintenance of euthermy isknown as basal metabolic rate (BMR). Variations in BMR,at intra- and inter-specific levels, are mostly explained bybody mass (Kleiber, 1961; McNab, 1983), but also by foodhabits (McNab, 1986), climate, and habitat (Lovegrove,1986; Lovegrove et al., 1991; Arends and McNab, 2001)among other factors. On the other hand, Hinds andMacMillen (1985), McNab (1979, 1986) suggested that seedeating rodent species reduce their BMR to balance theirwater budget and to cope with the ephemeral and drynature of seeds as a food resource. Degen (1997) reportedthat EWL is important to maintain thermal and waterbalance, but this fact has been poorly studied in studies ofcomparative physiology of South American rodents(Cortes, 1985; Cortes et al., 1988, 1990, 2000a, b, 2003;Bozinovic et al., 1995; Dıaz and Cortes, 2003).The family Chinchillidae includes a group of hystricognath
rodents, endemic to South America, living along theAndes in low productive environments and extremeclimatic conditions. This family includes the genusChinchilla (chinchillas), Lagidium (mountain vizcachas) and
ARTICLE IN PRESS
Nomenclature
BMR basal metabolic rate (mlO2/g h)C thermal conductance (mlO2/g h 1C)EWL evaporative water loss (mgH2O/g h)mb body mass (g)MR-WB energetic cost of maintaining the water
balance (cal/g h)MR metabolic rate (mlO2/g h)
MWP metabolic water production (mgH2O/g h)Ta ambient temperature (1C)Ta@ ambient temperature (1C), when MWP/
EWL ¼ 1Tb body temperature (1C)Tic calculated lower critical temperature (1C)DTm minimum thermal differential between Tb and
Tic (1C)
C. Tirado et al. / Journal of Thermal Biology 32 (2007) 220–226 221
Lagostomus (pampas vizcachas). Ecophysiological studies onthis family are mainly concentrated in the group Chinchilla,and there are few (or non-existent) studies for other groups.It has been reported that energy metabolism and theefficiency of water conservation ability of Chinchilla laniger
and Chinchilla brevicaudata are similar to the typical desertrodents (Cortes et al., 2000a, b, 2003). Lagidium viscacia onthe other hand, dwells arid Andean highlands at nearly2000–5000m above sea level (Munoz-Pedreros and Yanez,2000), where water and food resources are scarce (Marquetet al., 1998). This rodent presents a wide distribution alongthe Andes, from southern Peru to the south-central Chile andArgentina, occupying rocky areas (Redford and Eisenberg,1989). This species is gregarious, forming colonies and is ageneralist herbivorous rodent, with a diurnal–crepuscularactivity rhythm, and a low reproductive rate (Mann, 1978;Redford and Eisenberg, 1989; Cortes et al., 2002a, b). InChile, Lagidium viscacia is considered an endangered species(SAG, 2003). Because of Lagidium viscacia lives in suchextreme environments, we hypothesize that this rodent hasphysiological traits similar to those described for otherchinchillids, to cope with their habitat physical conditionswhich allow them to minimize the energy cost of euthermyand water balance.
2. Materials and methods
2.1. Experimental animals
Four individuals of Lagidium viscacia (2##, 2~~) werecaptured with National traps in the locality of AlmiranteLatorre (29 1380S, 701570W, at 2.000m of altitude). The sitehas maximum temperatures of 25 1C in summer andminimum temperatures of 1 1C in winter. Relative humidityranges from 40% to 70% (Novoa, pers. comm.). Capturedanimals were transported to the laboratory and kept inindividual cages with water and food (barley, rabbit foodand alfalfa) ad libitum. The average room temperature inthe laboratory was 21.073 1C and the relative humidityaveraged 60%.
2.2. Energy metabolism
The energy variables were estimated from the oxygenconsumption rate (MR), measured at different ambient
temperatures (Ta) in animals in post-absorptive state(4–5 h). Oxygen consumption (ml O2/g h), was measuredwith a computerized automatic closed-system respirometer,based on the manometric design modified by Morrison(1951). Body mass (mb) of the four adult animals was2.056763.5 g. They were placed individually in a metabolicchamber with CO2 and H2O absorbers (Ba(OH)2 andCaCl2, respectively) and submerged into a thermoregulatedbath (water–ethylene glycol) with Ta control (70.01 1C),mb (70.01 g), and the body colonic temperature (Tb) wasrecorded before and after each MR measurement. Tb wasmeasured with a copper-constant thermocouple connectedto a digital thermometer (Cole Parmer, Model 8500-40).MR was obtained from the average value of three
minimum periods of each experimental trial (1–3 h)(Rosenmann and Morrison, 1974). BMR was estimatedfrom the average of MR values, when independence of Ta
was determined. Minimal thermal conductance (C) wascalculated for each measurement at ambient belowthermoneutrality by C ¼MR (mlO2/g h)/DTm (McNab,1980). The lower critical temperature (Tic) was estimatedby the intersection between BMR and C.Values of BMR, C and the endothermic limit were
compared with the expected values for eutherian mammalsof similar mb using the relations: BMR ¼ 3.42mb
�0.25
(Kleiber, 1961) and C ¼ 1.0mb�0.50 (McNab and Morrison,
1963). Furthermore, the ratio between the BMR and C wascalculated, what make possible to indicate the minimumthermal differential—DTm (McNab, 1979).
2.3. Evaporative water loss
EWL rates were measured in the four specimens ofLagidium viscacia; mb ¼ 19937433.8 g). EWL was ob-tained from the averaged value of three minimum periodsof every experimental trial. These values were determinedby gravimetric records (70.1mg) every 5min, during aperiod of 2–3 h, in a system similar to that described byHainsworth (1968). Before measuring, atmospheric aircirculated across the empty chamber, in order to assessmeasurement errors that was 23.872.3mgH2O/h, valuethat was subtracted to EWL measurements of theexperimental animals. All the measurements were carriedout 1 h after thermal balance was reached, and measured todifferent Ta (10, 15, 20, 25, 30 and 32.5 1C), with an air flow
ARTICLE IN PRESS
(ml O
2 /g
h)
0.8
1.0
AirmlO2 /g h = 0.65 - 0.0168Ta
r = - 0.90 (P < 0.001)
C. Tirado et al. / Journal of Thermal Biology 32 (2007) 220–226222
of 5.0 l/min (Cortes et al., 2003). The minimum magnitudeof EWL was compared with the expected values foreutherian mammals of similar mb, by means of the relationsdescribed for rodents from xeric and mesic habitats,proposed by Cortes et al. (2000a).
Ambient Temperature
0 10 20 30 40
Oxy
gen
cons
uptio
n
0.0
0.2
0.4
0.6
Tb = 38.6ºC
Fig. 1. Relationship between metabolic rate and environmental tempera-
ture in Lagidium viscacia, measured in an air atmosphere.
2.4. Resistance to water deprivation
All four individuals of Lagidium viscacia
(mb ¼ 2055763.5 g) were subjected to water deprivationwith two types of dried diets: seeds of barley (11% ofproteins, 68.5% of carbohydrates, 2.0 of fats and 11.6 ofhumidity) and rabbit food (15% of protein, 16.5% of crudefibre, 3% of ethereal extract, and 13% of humidity). Waterdeprivation with barley and pellet (rabbit food) was carriedout during 10 to 8 days respectively, in order to avoid thedeath of the individuals. Body mass was registered every24 h during the experiments.
2.5. Efficiency of water regulation
To evaluate the efficiency of water regulation, twoindices were used: Ta@MWP ¼ EWL, where MWP is themetabolic water production (MacMillen and Hinds, 1983),and energetic cost of maintaining the water balance—MR-WB (Cortes et al., 2000a). MWP was assessed from MRdata versus Ta, assuming that 1ml of O2 produces 0.62mgof water (Schmidt-Nielsen, 1979) and 4.8 calories(Schmidt-Nielsen, 1990). MR-WB was compared with theexpected values for eutherian mammals of similar mb, fromxeric and mesic habitats (Cortes et al., 2000a).
2.6. Statistical analyses
Regression equations were calculated from empiricalvalues, fitting to mathematical equations by the leastsquares method (Zar, 1984). All the graphs valuescorrespond to the average and the standard deviation(7SD). The slopes were compared using the analysis ofcovariance (Zar, 1984).
3. Results
3.1. Energetic metabolism
Linear regression of MR vs. Ta, is represented byMR ¼ 0.65–0.0168Ta (r ¼ �0.90, po0.001, Fig. 1). Extra-polation of MR to 0 gave the estimated value of Tb
(MR ¼ 0; Ta ¼ Tb) of 38.6 1C, which is 0.8 1C higher thanmeasured Tb (37.7 1C). C was 0.017270.00139. The DTm
obtained was 20.2 1C.BMR of Lagidium viscacia was 0.3470.012ml O2/g h
(Fig. 1) and the lower critical temperature (Tic) was 18.4 1C.
3.2. Evaporative water loss
Minimum values of EWL were 0.41870.02mg H2O/g h,obtained within the Ta range of p20 1C (Fig. 2). Theaverage values of EWL at Ta ¼ 25, 30 and 32.5 1C, were0.47, 0.70 and 0.82mg H2O/g h, respectively, values thatwere increased in 14%, 70% and 99% with regard to theminimum EWL. At Ta ¼ 32.5 1C, EWL was equivalent to0.79mg H2O/g h entailing, implying a cooling rate of 29%regarding heat production corresponding to BMR value(2.39 cal/g h); this low cooling capability (thermolyse) wasreflected in a Tb increase of 39.9 1C, which implied anincrease of 2.2 1C above the normothermic condition(Tb ¼ 37.7 1C).
3.3. Resistance to water deprivation
Data obtained from water deprivation in Lagidium
viscacia, presented highly significant regression equations.The values of regression coefficients for barley and rabbitfood diets were r ¼ �0.99 and �0.96, respectively(po0.005). Resulting equations of water deprivation were:with barley: Log % mb ¼ Log1.996–0.0045t, and with rabbitfood: Log % mb ¼ Log1.997–0.0072t. Comparing the slopes(b1 ¼ barley diet and b2 ¼ rabbit food diet) significantdifferences are found (F1,56 ¼ 53.4; Po0.005, Fig. 3).Water deprivation with barley seeds and rabbit food diet
caused on Lagidium viscacia weight losses of 1.94% and2.32% at the first day, respectively. Weight losses were20% higher than that obtained with a less proteindiet (barley). The ratio between both slopes wasb2/b1 ¼ 0.0075/0.0045 ¼ 1.6; which means that it was60% of more body mass loss, when animals were deprivateof water with a diet high in protein.
3.4. Efficiency of water regulation
Ta@ estimated for Lagidium viscacia from the equationindicated in Fig. 4, corresponded to 3.8 1C. It represents the
ARTICLE IN PRESS
Day without water0 10 12
% in
itial
bod
y m
ass
85
90
95
100
105 BarleyRabbit food
8642
Fig. 3. Resistance to water deprivation in Lagidium viscacia (% initial
body mass versus time in days). (barley ¼K, and rabbit food ¼’.)
Day without water0 10 12
Log
% in
itia
l bod
y m
ass
1.92
1.94
1.96
1.98
2.00
2.02 BarleyLog%W = 1.996 - 0.0045tr = - 0.99
Rabbit food Log%W = 1.997 - 0.0072tr = - 0.99
8642
Fig. 4. Resistance to water deprivation in Lagidium viscacia (Log% initial
body mass versus time in days). (Barley ¼K, and rabbit food ¼’.)
Ambient Temperature(ºC)
5 10 15 20 25 30 35
Eva
pora
tive
wat
er lo
ss(m
gH2O
/g h
)
0.0
0.2
0.4
0.6
0.8
1.0
Eva
pora
tive
Hea
t Los
s
(% d
e H
eat P
rodu
ctio
n)
5
10
15
20
25
30
35
Bod
yTem
pera
ture
36
38
40
42
44
Normothermic37.7+0.06ºC.
Fig. 2. Relationships among evaporative water loss rate, evaporative heat
loss, body temperature, and environmental temperature in Lagidium
viscacia.
C. Tirado et al. / Journal of Thermal Biology 32 (2007) 220–226 223
index of water regulation efficiency (MacMillen and Hinds,1983). On the other hand, the index value of MR-WBestimated (Cortes et al., 2000a) was 2.81 cal/g h (Fig. 5).
4. Discussion
4.1. Energy metabolism
Lagidium viscacia showed an average BMR of0.3470.012ml O2/g h, that is equivalent to 66.9% of thatpredicted (Kleiber, 1961). If we compare BMR of Lagidium
viscacia with other chinchillids, it represents 121% (0.28mlO2/g h) of the value reported for Lagostomus maximus
(6784 g) inhabiting temperate climate (Kohl, 1980), 50%(0.68ml O2/g h) for C. laniger (358.8 g) (Cortes et al.,2000b), 68% (0.498ml O2/g h) for C. brevicaudata (454.4 g)(Cortes et al., 2003).
Lagidium viscacia is a herbivorous rodent (Cortes et al.,2002a, b) similar to other chinchillids (Branch et al., 1994),condition that seems to be correlated with high metabolicrates (McNab, 1986). However, this chinchillid has a lowBMR, avoiding risks of hyperthermia and maintainingtheir water economy by minimizing EWL similar physio-logical condition to that described for heteromyids rodents(Dawson, 1955, Carpenter, 1966, McNab, 1979) andmurids from Australia (MacMillen and Lee, 1970) andAsia (Shkolnik and Borut, 1969). Accordingly the lowmass-independent BMR of this specie seems to be animportant mechanism to maintain a positive energy andwater balance (McNab, 1979) in a low productiveenvironment and harsh abiotic conditions (low waterresources and high thermal loads), similar to the environ-ment of this rodent the Andes range.A low thermal conductance value was also found in this
specie (C ¼ 0.0171ml O2/g h 1C), equivalent to 78% of thatpredicted for a eutherian mammals of similar mb (McNaband Morrison, 1963). In fact, this is the lowest conductancereported for other South American rodents, includingmurids, octodontids and chinchillids (Rosenmann, 1977;Kohl, 1980; Bozinovic and Rosenmann, 1988; Bozinovic,1992; Bozinovic et al., 1995; Cortes et al., 2000a, 2003).
ARTICLE IN PRESS
MW
P/E
WL
0.3
0.4
0.50.60.70.80.91.01.21.4 MWP/EWL= 1.182(0.957)Ta
r =- 0.99 (p<0.001)
Ta@ = 3.8ºC
C. Tirado et al. / Journal of Thermal Biology 32 (2007) 220–226224
As BMR and C can be considered as an adaptation ofthis rodent to their habitat, C is consistent with the value ofTic, which allows them to maintain euthermy in a widerange of low temperatures. This is a physiological attributewhich is also reflected in the high DTm ¼ 20.2 1C, whichwas 12.3% lower than predicted for mb (DTm expec-ted ¼ 3.42mb
0.25) and that is 3.6 1C higher than theestimated value for C. laniger and 1.8 1C lower than C.
brevicaudata. This high thermal differential is not expectedfor a rodent with low BMR, but it is explained by its highthermal insulation, similar to that described for otherchinchillids (Cortes et al., 2000b, 2003).
Ambient Temperature (ºC)
0 10 15 20 25 30 350.1
5
Fig. 5. Relationship between MWP/EWL and environmental temperature
in Lagidium viscacia.
4.2. Evaporative water loss
This value of EWL is consistent with the results obtainedin the water deprivation assay. According to this, Lagidium
viscacia does not present a physiological specialization to alow EWL, which contrast with other chinchillids (Cortes etal., 2000a, 2003), condition that makes it depend onexogenous water.
The cooling capacity was only 29% of BMR, withTa ¼ 32.5 1C, condition that is unfavourable for maintain-ing normothermy (Tb ¼ 37.7 1C), which is reflected in the2.2 1C increase of its Tb, which is similar to C. laniger andC. brevicaudata. This is explained by the high thermalinertia of this species, i.e., the bigger the animal, the morethe thermal inertia (Finke, 2003). However, probably theeffects of midday high environmental temperatures are notso influential on thermoregulation, due to the fact thatLagidium viscacia has diurnal–crepuscular habits andexhibit basking behaviour (Mann, 1978).
4.3. Resistance to water deprivation
Lagidium viscacia behaves as a water-dependent spe-cies—i.e., it is unable to maintain its mb when it is waterdeprived and fed with barley seeds and rabbit food, whichindicates that water in the food (barley humidity ¼ 11.6%;rabbit food humidity ¼ 13.0%) plus MWP, is lower thanwater loss ( ¼ EWL+renal+digestive). Losses of mb, afterthe first day of water deprivation with diets of rabbit foodand barley seeds, were 2.32% and 1.94% per day,respectively (Fig. 3). These values suggest that a higherprotein load in the diet (15%) causes a faster dehydration(Fig. 3). However, this information does not reflect thewater behaviour kinetics to water deprivation, because it isnot linear but adjusted to a negative exponential equation(Cortes, 1985; Cortes et al., 1988) (Fig. 4). The ratio b2/b1slopes was 1.6 times higher when protein in the diet washigher, therefore, Lagidium viscacia in spite of occupyingxeric habits, behaves as a species that depends onexogenous water. Hence, Pearson’s (1948) and Mann’s(1978) statements that this species does not drink freewater, are not consistent with our observations, whichshow that this rodent lacks the typical features of desert
rodents; its presence in xeric environments, could be betterexplained on the basis of its behavioural strategies.
4.4. Efficiency and energy cost of water balance
Considering the low value of Ta@ (3.8 1C) showed byLagidium viscacia in comparison with other rodents ofChile from mesic habitat, as Abrothrix olivaceus (18.6 1C),Abrothrix andinus (12.5 1C), Phyllotis darwini (14 1C),Phyllotis magister (10.5 1C), Phyllotis rupestris (12.1 1C),Oligoryzomys longicaudatus (12.1 1C) and from xerichabitat as C. laniger (12.7 1C), C. brevicaudata (10.6 1C)and Octodon degus (16.6 1C) (Cortes et al., 2000a), indicatethat this species is less efficient in regulation andconservation of body water.Nevertheless, the MR-WB index of Lagidium viscacia
was 2.81 cal/g h, which is equivalent to 108% of thepredicted value by allometric equation for rodents fromxeric habitat (Cortes et al., 2000a), similar to the behaviourshowed by C. laniger and C. brevicaudata (Cortes et al.,2000a, 2003).In summary, when analyzed together, however, and with
previous knowledge of the other chinchillid species, ourresults suggest that the distinct components of thephenotypic energetic responses cannot be treated as asingle common factor and that, at least for our studyspecies, the energetic traits seem to be more important thanthe mechanisms associated to tolerance to water depen-dence in setting the level of physiological mechanism tosurvive in the extreme Andean habitat of Lagidium
viscacia.
Acknowledgements
We thank Dr. Julio R. Gutierrez for reviewing a draftversion of this manuscript. This work was financed by theresearch project FONDECYT 1981122 to AC andFONDAP 1501-0001 to FB.
ARTICLE IN PRESSC. Tirado et al. / Journal of Thermal Biology 32 (2007) 220–226 225
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