183BASAL METABOLIC RATE OF MARSUPIALSRevista Chilena de Historia Natural78: 183-198, 2005

Uniformity in the basal metabolic rate of marsupials:its causes and consequences

Uniformidad en la tasa metabólica basal de marsupiales: sus causas y consecuencias

BRIAN K. MCNAB

Department of Zoology, University of Florida, Gainesville, Florida 32611, USA;e-mail: bkm@zoo.ufl.edu

ABSTRACT

Most of the variation (98.8 %) in basal rate of metabolism (BMR) in 70 species of marsupials is correlatedwith body mass, although lowland species have higher basal rates than highland species and burrowers havelower basal rates than non-burrowers. These factors collectively account for 99.2 % of the variation inmarsupial BMR. Marsupials differ in BMR from eutherians by having no species with a high basal rate bygeneral mammalian standards, even when consuming vertebrates or grass, food habits that are associated withvery high basal rates in eutherians. The absence of high basal rates in marsupials reflects the absence of acorrelation of rate of reproduction with basal rate, a correlation present in eutherians. These differences havetwo consequences: (1) marsupials are less tolerant of cold environments than eutherians, and (2) marsupialscoexist with eutherians only when both have food habits associated with low basal rates and therefore wheneutherians have reduced rates of reproduction. In Australia and South America marsupial carnivoresdiversified in the absence of eutherian equivalents. The importation to mainland Australia of dingos byhumans appears to have been the immediate cause for the extinction of thylacines, Tasmanian devils, andeastern quolls. Carnivorous marsupials in South America were replaced by eutherians with the completion ofthe Panamanian land bridge. Macropods, which have lower basal rates than eutherian grazers, survive incentral Australia probably because of their adjustment to xeric environments, whereas introduced domesticstock require the provision of water by humans.

Key words: coexistence, competitive exclusion, eutherians, marsupials, reproduction.

RESUMEN

Gran parte de la variación (98,5 %) en la tasa metabólica basal de 70 especies de marsupiales se correlacionacon la masa corporal, aunque las especies de tierras bajas tienen tasas basales mayores que las de tierras altas,y las especies subterráneas tienes BMR’s menores que las no subterráneas. Colectivamente, estos factores dancuenta de un 99,2 % en la variación de la BMR de los marsupiales. Los marsupiales difieren de los euteriospor no tener especies con altas BMR’s, esto según los estándares generales para mamíferos. Esto ocurre,incluso a pesar de consumir vertebrados o pastos, estos últimos, hábitos tróficos asociados con altas BMR enmamíferos euterios. La ausencia de altas tasas basales en marsupiales refleja la ausencia de correlación entrela tasa de producción con BMR, una correlación que sí está presente en euterios. Estas diferencias tienen dosconsecuencias: (1) los marsupiales son menos tolerantes a ambientes fríos que los euterios, y (2) losmarsupiales coexisten con los euterios solo cuando sus hábitos alimentarios están asociados a BMR’s bajos yademás cuando los euterios poseen tasas de reproducción bajas. En Australia y Sudamérica los marsupialescarnívoros se diversificaron en ausencia de euterios equivalentes. La importación de los dingos Australianospor los humanos, parece ser la causa inmediata de la extinción de los tilacinos y del demonio de Tasmania.Cuando se terminó de formar el puente de Panamá los carnívoros de Sudamérica fueron reemplazados poreuterios. Los macrópodos, que poseen BMRs más bajas que los pastoreadores euterios, sobreviven enAustralia central pues probablemente son capaces de tolerar ambientes xéricos, mientras que los herbívorosdomésticos requieres de la provisión humana de agua.

Palabras clave: coexistencia, exclusión competitiva, euterios, marsupiales, reproducción.

184 MCNAB

INTRODUCTION1

The basal rate of metabolism (BMR) is astandard measure of energy expenditure inendotherms. It is defined as the minimal rate ofmetabolism measured in the zone ofthermoneutrality, when an endotherm isthermoregulating, post-absorptive, and inactiveduring the period of inactivity (McNab 1997).BMR gives a standard by which to compare theenergetics of different endotherms, which oftenlive in different climates, have differentbehaviors, eat different foods, and arecharacterized by different morphologies. Thatis, differences in standard rate of metabolismreflect differences in the animals studied, notdifferences in the measurements made or in theconditions to which the animals were exposed.Furthermore, many aspects of the life history ofendotherms correlate with BMR independent ofbody size, including maximal rate ofmetabolism (Bozinovic 1992, but see Koteja1987), field energy expenditure (Nagy 1994,Speakman 2000), and reproductive rate(McNab 1980). The study of BMR has giveninsight into some aspects of the comparativebiology of endotherms that could not easilyhave been obtained by other methods.

Many factors have been suggested toinfluence BMR, most importantly body size, asmeasured by body mass. As with most size-dependent biological phenomena, BMR isdescribed as a power function of body mass.Mass then accounted for 95.6 % of thevariation in total BMR, and 77.7 % of mass-specific BMR, in a survey of 320 species ofmammals (McNab 1988a). In this case, thefitted power of body mass was 0.713. Thepower of body mass has attracted the attentionof many observers, some of whom are “truebelievers” in one power or another (McNabsubmitted2), but in such advocacy, they haveuniformly ignored the residual variation aroundthe mean curve. The difficulty with thatdecision is that the fitted power changes, often

significantly, as factors other than mass areincorporated into the analysis (McNabsubmitted3). I find the quest for the factorsinfluencing the residual variation in BMR to bea much more biologically interesting andfeasible goal. The causes for the residualvariation have been and continue to be thesubject of an extended controversy, as havebeen its consequences. Little of residualvariation reflects measurement error.

Factors other than body mass that have beensuggested to influence BMR have includedfood habits, climate, latitude, altitude, acommitment to burrowing or arboreal habits,presence on islands or continents, type ofreproduction, etc. These factors, however, areoften correlated with each other, so that theirindividual effects are difficult to circumscribe.Some observers have argued that the principalfactor influencing the residual variation inBMR is “phylogeny”. Phylogeny then acts as a“collective” for the various interactive factorsother than body mass that influence BMR.

The variability around the mean fittedBMR-mass curve itself varies among groups ofendotherms. For example, within the sample of320 mammals, 272 eutherians showed aresidual variation in total BMR of 4.4 %,identical to that found in the entire sample(McNab 1988a). However, body massaccounted for 98.8 % of the variation in totalBMR in 46 marsupials, i.e., the residualvariation was only 1.2 %, or 27 % of theeutherian value. This difference betweeneutherians and marsupials was also found byHayssen & Lacy (1985) in an earlier, but notidentical, sample of 248 eutherians and 42marsupials. Body mass thus is a more completedeterminant of BMR in marsupials than ineutherians.

Another difference between marsupials andeutherians that has long been known is thatmarsupials have lower basal rates (Martin1902, MacMillen & Nelson 1969, Dawson &Hulbert 1970, McNab 1978, 1986, Hayssen &Lacy 1985). That conclusion, however, ismisleading, reflecting as it does the means ofthe two groups, not the BMR of individualspecies. In fact, the lowest basal rates,

1 This inquiry is a tribute to Mario Rosenmann, who I firstmet in 1959 when I was a graduate student on anexpedition from the University of Wisconsin to study high-altitude adaptation of mammals indigenous to Chile andPerú. Mario and I worked together both in and aroundSantiago. I dedicate this article to Mario with the fondestof memories of days long gone.2 McNAB BK (manuscript) The evolution of energetics inbirds and mammals.

3 McNAB BK & HI ELLIS (manuscript) Flightless railsendemic have lower energy expenditures than flighted railson islands and continents.

185BASAL METABOLIC RATE OF MARSUPIALS

corrected for body mass, found in eutheriansare less than the lowest rates found inmarsupials (Fig. 1). The actual difference thatexists between these groups is that a fewmarsupials have marginally high basal rates bygeneral mammalian standards, whereas manyeutherians have exceedingly high basal ratesthat raise the collective average for eutheriansabove that of marsupials.

Earlier analyses of marsupial basal rateswere limited by the number of species studiedand by the technical tools available at the timefor the analysis of the factors with which BMRwas correlated. With the addition of data andthe use of newer analytical tools, the variationin marsupial BMR can be reconsidered todetermine the extent to which it varies withfactors other than body mass. Such an analysiswill permit me to reexamine whether adifference in BMR exists between marsupials

Fig. 1: Frequency distribution of basal metabolic rate (BMR) in marsupials (see Table 1) andeutherians (from McNab 1988a), expressed as a percentage of the values expected from body massin the general mammal curve derived from McNab (1988a).Distribución de frecuencia de tasa metabólica basal (BMR) en marsupiales (véase Tabla 1) y euterios (de McNab 1988a),expresadas como porcentaje de lso valores esperados para la masa corporal de la curva general de mamíferos de McNab(1988a).

and eutherians, and if so, why. I then shallexamine the consequences of any differences inmetabolism between these groups.

MATERIAL AND METHODS

Data on the BMR and body mass of marsupialswere obtained from the literature (see Table 1),supplemented by unpublished data on fourspecies of cuscuses (Phalanger) that Imeasured in Papua New Guinea. Whereas myearlier analyses (McNab 1978, 1988a) had datafrom 38 and 46 species, respectively, now dataare available from 71 species, including suchdistinctive genera as Dromiciops, Phalanger,Tarsipes, Notoryctes, and Acrobates, from sixof seven orders and 17 of 18 families, i.e., forall groups except the Caenolestidae in thePaucituberculata. These data are combined with

186 MCNAB

the qualitative characteristics of each speciesand the environments in which they live (Table1), including food habits (carnivory,insectivory, frugivory, nectarivory, sap-eating,grazing, folivory, omnivory), substrate use(terrestrial, burrowing, arboreal, aquatic,terrestrial/arboreal), thermal climate(temperate, tropical, montane, temperate/tropical), moisture climate (mesic, xeric), andwhether they enter torpor (yes, no,hibernation).

These data are examined by the analysis ofcovariance (ANCOVA) with the program ofSuperANOVA, Berkeley, California. Thisprogram permits one to regress log10 BMRagainst log10 mass and to examine the maximalextent to which the residual variation isinfluenced by various species’ characteristicsand environmental factors, individually and indiverse combinations. This method also permitsany interactive terms among the factorsinfluencing BMR to be defined, as have beenseen in arvicolid rodents (McNab 1992), NewZealand ducks (McNab 2003a), phyllostomidbats (McNab 2003b), and rails (McNabsubmitted4).

Another potential approach, phylogeneticcontrasts, preferentially describes most (or all)of the residual variation in a character state to“phylogeny,” thereby ignoring the interactionof character states (McNab 2003b). As noted,“phylogeny” at best acts as a collective for thevarious factors influencing the residualvariation in character states. In fact, mostrelatives are physiologically similar becausethey have similar habits and live in similarenvironments, a condition seen in arvicolidrodents (McNab 1992), but when a radicalecological or behavioral diversification occursin a clade, as in the family Phyllostomidae(McNab 2003b), i t is associated with adiversification in physiology, which is what isto be expected. The most interesting questionhere, which will not be addressed in this article(but see McNab, submitted5), is why somegroups show a radical diversification, whereasothers maintain a uniformity in size, behavior,physiology, and the environment occupied.

RESULTS

Basal rate of metabolism in marsupials shows,as expected, a strong correlation with bodymass (Fig. 2). The equation that describes thisrelationship is:

VO2 (mL O2 h-1) = 2.31 g0.746 (1)

where g is body mass in grams. This equationaccounts for 98.8 % of the variation in BMR(F1,68 = 5511.35, P < 0.0001). Data from thehoney ‘possum (Tarsipes rostratus) were notused. This decision was made because the datawere quite variable (see Withers et al. 1990);they represent by far the highest BMR (163 % ofthe general mammalian curve), independent ofbody mass, reported in any marsupial. A similarsituation existed with the yapok (Chironectesminimus), a Neotropical semi-aquatic marsupial.I (McNab 1978) had reported that its BMRequaled 120 % of the value expected frommammals generally, making it by far the highestbasal rate measured in a marsupial at that time.Later, Thompson (1988) reported that the yapokhad a basal rate that was average for a marsupial(97%) and low for a mammal (82%). I do notknow why my measurements were higher thanthose of Thompson, but as long as temperatureregulation occurs, most erroneous measurementsof basal rate are likely to be high, due either toactivity or anxiety. Therefore, I should like tosee a reexamination of the honey ‘possum withspecial attention paid to the zone ofthermoneutrality, which is narrow and difficultto define in a 10-g species, especially if it isprone to activity.

With regard to the remaining 70 species,only 1.2% of the variation in marsupial basalrates is unaccounted for by equation (1), anobservation similar to that seen before.Corrected for body size, the lowest BMR wasfound in the wombat Lasiorhinus latifrons (57% of the mean marsupial curve), whereas thehighest basal rate by marsupial standards(excluding Tarsipes) was found in the brush-tailed rat-kangaroo Bettongia penicillata (131%). The rat-kangaroo thus has a BMR that isonly 2.3 (= 131/57) times that of the wombat,adjusted for the difference in body mass,whereas in eutherians this ratio can be muchlarger. For example, the bighorn sheep (Oviscanadensis) has a basal rate that is 5.6 (= 224/40) t imes that of the giant armadillo

4 McNAB BK (manuscript) Flightless rails endemic toislands have lower energy expenditures than flighted railson continents.5 McNAB BK (manuscript) The evolution of energetics inbirds and mammals.

187BASAL METABOLIC RATE OF MARSUPIALS

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189BASAL METABOLIC RATE OF MARSUPIALSP

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190 MCNAB

(Priodontes maximus) (see McNab 1988a),using eutherian standards, while ignoring theeven higher basal rates found in marineeutherians, like sea otters, seals, and porpoises,which would bring the ratio up to 9.7 (usingdata [388 %] from the sea otter [Enhydralutris])! Again, much more residual variation inBMR is present in eutherians than inmarsupials.

The impact of factors other than body masson BMR in marsupials was examined, although,given the small residual variation, extensivecorrelations would appear to be unlikely.Indeed, Log10 BMR was not correlated with theuse of torpor (F2,66 = 1.15, P = 0.32), foodhabits (F11,57 = 1.25, P = 0.27), order affiliation

(F5,63 = 1.33, P = 0.26), or occurrence inclimates characterized by moisture (F1,67 =3.69, P = 0.059), when individually coupledwith Log10 mass.

Log10 BMR correlated with several factorsin a complicated manner. For example, itcorrelated with substrate (F4,64 = 3.87, P =0.0070), when substrate was represented byfive categories and combined with log10 mass.However, only one category, burrowers,differed (t4,64 = - 3.72, P = 0.0004) from theothers, so when substrate use was divided intoburrowers and non-burrowers, log10 BMRcorrelated with substrate (F1,67 = 15.47, P =0.0002) and log10 mass (F1,67 = 6678.58, P <0.0001; r2 = 0.990). Log10 BMR also correlated

Fig. 2: Log10 basal metabolic rate (BMR) in marsupials as a function of log 10 body mass. The dataare derived from Table 1.Log10 de la tasa metabólica basal (BMR) en marsupiales como función de log10 de la masa corporal. Los datos provienen dela Tabla 1.

191BASAL METABOLIC RATE OF MARSUPIALS

(F3,65 = 3.03, P = 0.036) with the thermalclimate in which marsupials live, when climatewas represented by four categories (temperate,tropical, montane, or temperate/tropical) andcombined with log10 mass. Log10 BMR inmontane species, defined as tolerating altitudes> 2000 m, differed (t4,65 = 2.58, P = 0.012)from that of the other categories, which did notdiffer from each other. So, when thermalclimates other than montane were lumped intoa lowland category, Log10 BMR correlated(F1,67 = 7.27, P = 0.0089) with thermal climate,when coupled with Log10 mass (F1,67 =6022.32, P < 0.0001; r2 = 0.989). When thesefactors were combined, log10 basal rate thencorrelated with thermal climate (F1,66 = 11.30,P = 0.0013), substrate (F1,66 = 19.84, P <0.0001), and log10 mass (F1,66 = 7710.05, P <0.0001; r2 = 0.992). This relationship takes theform of an equation:

VO2 (mL O2 h-1) = 1.86 (A · S) g0.752 (2)

where A is a non-dimensional coefficient foraltitude equaling 1.25 in lowland species and1.00 in montane species, and S is a non-dimensional coefficient for substrate equaling0.66 for burrowing species and 1.00 for non-burrowers (Fig. 3). The coefficient in equation(2) would equal 1.53 (= 1.86 x 1.25 x 0.66) inlowland, burrowing marsupials and 1.86 (=1.86 x 1.00 x 1.00) in highland, non-burrowers.Ambient temperature and substrate, however,collectively accounted for only one-third(0.4%) of the residual variation in equation (1)and leaves the remainder unaccounted for.

Burrowing eutherians are known to havelow basal rates (McNab 1966, Contreras &McNab 1990), so it is not surprising to see thispattern in marsupials. That basal rates inlowland marsupials are higher than in montanespecies is somewhat surprising becausehighland arvicolid rodents (McNab 1992),phyllostomid bats (McNab 2003b), andpteropodid bats (McNab & Bonaccorso 2001)have higher basal rates than lowland species.However, highland tropical pigeons have lowerbasal rates than lowland species (McNab2000a). Among the six montane marsupialsstudied, only Phalanger carmelitae had atypical BMR by marsupial standards (101 %),whereas the remaining five had basal ratesbetween 68 and 94 %.

Residual variation is reduced to 0.4% whenfamilial (F12,47 = 4.17, P = 0.0002) and ordinal(F1,47 = 4.61, P = 0.037) affiliation arecombined with temperature (F3,47 = 7.44, P =0.0004), moisture (F1,47 = 5.76, P = 0.020), andlog10 mass (F1,47 = 3122.35, P < 0.0001; r2 =0.996). Order affiliation appears and disappearsdepending on how the thermal climate iscategorized. Familial affiliation, which appearsconsistently, is a “dummy” variable, probablycoding for substrate, which is always excludedwhen family is included in the analysis, andpossibly for other information. Obviously,factor interaction in the determination ofmarsupial BMR is complex.

DISCUSSION

Four aspects of marsupial basal rates remainthe same: they (1) collectively show littlevariation independent of body mass, (2)average lower than in eutherians, (3) show nocorrelation with food habits, and (4) are nothigh by general mammalian standards.Marsupials fail to show a correlation of BMRwith food habits principally because marsupialcarnivores and grazers, unlike their eutheriancounterparts, do not have higher basal ratesthan marsupials with other food habits.

With regard to the general absence of highbasal rates in marsupials, only six species havemarginally high basal rates by generalmammalian standards (Table 1): Bettongiapenicillata (110%), Petauroides volans (109%),Aepyprymnus rufescens (108 %), B. gaimardi(107 %), Macropus robustus (105 %), andDidelphis marsupialis (105 %). Manyeutherians have much higher basal rates,compared to a general mammalian standard: of272, 112 had basal rates between 100 and 150%, 26 between 150 and 200 %, 11 between 200and 300 %, and three > 300 % (McNab 1988a).The principal difference in the BMR ofmarsupials and eutherians, then, remains thesame: compared to eutherians, marsupials havea truncated distribution of basal rates, correctedfor body mass (Fig. 1).

Causes

These observations raise the question: why doeutherians have a greater diversity in BMR than

192 MCNAB

is found in marsupials? To state that thedifference is due to ‘phylogeny’ obfuscates thetrue factors responsible for this difference. Oneconclusion, however, is obvious: the high basalrates of eutherians are not related to the cost ofendothermy, except possibly in the coldestenvironments and at the smallest masses(Lillegraven et al . 1987): marsupialscollectively are not poorer thermoregulatorsthan eutherians. Although eutherians withunusually low basal rates often show marginalto poor thermoregulation, e.g., Heterocephalusglaber (McNab 1966), the only marsupialknown to have marginal temperature regulationis the mole Notoryctes caurinus (Withers et al.

2000), which combines a low basal rate (50%of the mammalian standard) with a small mass(34 g). Other marsupials that combine a smallmass with a low basal rate enter a regulatedtorpor (Bartholomew & Hudson 1962,Morrison & McNab 1962, Dawson & Wolfers1978, Fleming 1985a, 1985b, Geiser et al.1984, Geiser 1987, 1988, Geiser & Baudinette1987, 1988, Withers et al. 1990), similar to thesituation in white-toothed shrews(Crocidurinae; Genoud 1988). Small eutheriansthat avoid torpor, most notably red-toothedshrews belonging to the subfamily Soricinaeand arvicolid rodents, “overcompensate”metabolism by conforming to the ‘boundary

Fig. 3: Log10 observed basal metabolic rate (BMR) in marsupials as a function of Log10 BMR basedon equation (2), which takes body mass, altitudinal distribution, and burrowing or non-burrowinghabits into consideration.Log10 de la tasa metabólica basal (BMR observada en marsupiales como función de Log10 de BMR basado en la ecuación(2), que considera la masa corporal, la distribución altitudinal y los hábitos subterráneos o no subterráneos

193BASAL METABOLIC RATE OF MARSUPIALS

curve’ for continuous endothermy (McNab1983, 1992). Small dasyurids, burramyids, andamong eutherians crocidurines do not show thisresponse. Consequently, the high basal rates ofeutherians, except at the smallest masses, mustbe related to some factor other than the cost ofendothermy.

What can this factor be? I (1986) suggestedthat it reflected a difference in the energetics ofreproduction: high basal rates of metabolism ineutherians facilitate an increased rate ofreproduction, which partly results from havinga placenta, developed from embryonic(trophoblastic) and maternal tissues, thatpermits an augmented rate of exchangebetween a gravid eutherian and her developingoffspring without an immunological rejectionof the genetically distinct offspring(Lillegraven 1976, Parker 1977, Lillegraven etal. 1987).

In eutherians gestational period decreasesand the post-natal growth rate, fecundity, andthe amplitude of population cycles increasewith an increase in BMR, corrected for bodysize (McNab 1980, Stephenson & Racey 1995,N. Vasey & D.T. Rasmussen personalcommunication). Milk production (Glazier1985, McLean & Speakman 2000) and littersize (Genoud 1988) also increase with BMR ineutherians, but for complications, especially inspecies with low basal rates, see Thompson(1991). Rasmussen & Izard (1988) showed inthe Lorisidae that variation in basal rateaccounted for much of the variation ingestational period, lactational period, and post-natal growth constant. That is, a high BMR ineutherians facilitates an increased reproductiveoutput, which occurs whenever the resources inthe environment permit an increase in rate ofmetabolism, most notably in carnivores andgrazers. External circumstances, such as theuncertain availability or low quality of food,however, may force eutherians to have lowbasal rates with its consequence, a reducedreproductive output, especially in frugivores,folivores, and large terrestrial invertebrate-eaters.

The reproductive rate of marsupials doesnot increase with BMR at least in part becausenutritional and waste exchange cannot beincreased between a pregnant female and herdeveloping young in the absence of atrophoblast without the risk of immunological

rejection. Most of the embryologicaldevelopment in marsupials occurs in thepresence of a shell membrane that isolates theembryos from maternal t issues, therebyprotecting the fetuses from immunologicalrejection, but restricting fetal-maternalexchange. The limited marsupial in uterodevelopment depends on the presence of a largeegg yolk mass, which is nearly absent ineutherians (Parker 1977). The independence ofreproduction from basal rate is responsible forthe restricted range of residual variation inBMR in marsupials (McNab 1986).

Although marsupials cannot augmentnutrient transfer to intrauterine embryos, theytheoretically could facilitate the postpartumgrowth and development of their young throughan increase in rate of metabolism duringlactation. However, at birth marsupial young,compared to eutherians, are sti l l at anembryonic stage of development. Theirpostnatal rate of development is low, whichmay be limited by a restricted uptake andprocessing of milk as a result of the delayeddevelopment of digestive, respiratory, andexcretory systems (Parker 1977). Although theincrease in rate of metabolism in marsupialsduring lactation may be appreciable (Thompson& Nicoll 1986), especially given their generallylow basal rates, it still is less than that found inlactating eutherians with high basal rates (Fig.10.2 of Thompson 1992). This may explainwhy the conceptual-to-weaning periods inmarsupials average 1.5 times those ofeutherians of equal mass (Thompson 1987),most of the difference reflecting the length ofthe lactational period. So, in spite of havingfood habits, such as carnivory and grazing, thatpermit high basal rates in eutherians, marsupialcarnivores and grazers have low to intermediatebasal rates by general mammalian standards.Variation in marsupial BMR is thereforeprincipally associated with the cost ofthermoregulation, which varies with bodymass. Variation in the rate of reproductionoccurs among marsupials (Parker 1977, Russell1982), but it is not correlated with residualvariation in BMR (McNab 1986).

Consequences

The difference in energy expenditure betweenmarsupials and eutherians appears to have at

194 MCNAB

least two ecological consequences: (1) therestricted tolerance of marsupials to coldenvironments and (2) the limited ability ofmarsupials to coexist with eutherians.

Endotherms encounter cold environments inmid-latitudes at high altitudes and seasonally athigh latitudes. The two extended mountainousregions with marsupials are New Guinea andSouth America. In New Guinea severalmarsupials are found near the equator ataltitudes between 3,500 and 4,000 m, includingtwo bandicoots, one macropod, two phalangers,and two pseudocheirids, whereas three rodentsextend to 4,000-4,500 m (Flannery 1995). Intropical South America the only marsupials thatget to 3,500 m or higher are caenolestids,including Lestoros and possibly Caenolestes(Eisenberg 1989, Eisenberg & Redford 1999).Eutherians, in contrast, are found at muchhigher altitudes in South America: eightrodents, the vicuña, and Felis jacobita reach ahigh-altitude limit between 4,500 and 5,000 m,and Felis colocolo , Puma , Akodon, andLagidium occur at altitudes greater than 5,000m (Redford & Eisenberg 1989, Eisenberg &Redford 1999). Marsupials also are lesstolerant than eutherians of cold-temperateenvironments in North America, where onlyone species (Didelphis virginiana) is foundnorth of México (see Brocke 1970), and inSouth America, where only Lestodelphus halli,possibly a hibernator, enters southern Patagonia(McNab 1982, Redford & Eisenberg 1989). Nomarsupial resides on Tierra del Fuego.

The restricted distribution of marsupials incold environments may reflect their response toaltitude in New Guinea, a reduction in BMR.Unfortunately, the basal rates of caenolestidshave not been measured, but C. obscurus has atypically low marsupial body temperature (35.4oC, McNab 1978), which suggests that it too hasa basal rate that is low by mammalian standards.Didephis virginiana, the only marsupial intemperate North America, has a basal rate nearthat expected from general mammalianstandards (98 %), when measured in subtropicalFlorida (McNab 1978), but it appears to belower (52-56 %) at the northern limits ofdistribution in Michigan (Brocke 1970), apattern similar to the reduction in highlandmarsupials in PNG. A low basal rateundoubtedly limits the tolerance of D. virginianato cold temperatures, a response that is

counteracted by its rather large mass, whichfacilitates winter survival in adults throughseasonal fat storage (Brocke 1970). Dromiciopsaustralis, which is limited to temperate Chileand adjacient Argentina, has a basal rate that isonly 66 % of the mammalian level, andThylamys elegans in temperate Chile has a basalrate that is only 51 %. In contrast, cold-temperate and polar eutherians, such as arvicolidrodents, hares, carnivores, and ungulates, arecharacterized by high basal rates.

The coexistence of marsupials witheutherians is l imited. Their apparentcoexistence in the New World is misleading inthat most Neotropical marsupials feedprincipally on fruit, insects, or a mixture offruit and insects. This is a highly restrictedrange of diets compared to that found inAustralian marsupials, which collectively feedon insects, vertebrates, fruit, nectar, sap,leaves, and grass. A mixture of insects andfruits is a diet associated with low basal ratesin eutherians. For example, the kinkajou (Potosflavus), an arboreal eutherian that feeds heavilyon fruit, has a BMR that is 87 % of the valueexpected from mammals, which is similar(89%) to that of a Neotropical marsupial withsimilar habits, Caluromys derbianus. Thesebasal rates reflect their arboreal, frugivoroushabits, as has been seen in other eutherianswith similar habits, such as various viverrids(McNab 1995), when basal rates varied from63-87 % of the mammalian value.

Marsupial carnivores and grazers do notcoexist with eutherians that have these foodhabits. Marsupials with these habits are limited togreater Australia, where the only terrestrialeutherians are bats and murid rodents. The onlypossible marsupial carnivore in the Neotropics isLutreolina crassicaudata, which has beendescribed to prey “…on small vertebrates, fishes,and insects” (Redford & Eisenberg 1989, p. 23);it has a BMR equal to 99 % of the generalmammal curve, which is similar to that found insome omnivorous canids. The Australianmarsupials committed to carnivory have basalrates that varied from 82 to 96 % of the valueexpected from mammals generally (Table 1),whereas nine eutherian, terrestrial carnivoreshave basal rates that vary from 116 to 231 %(McNab 1988a) and recent measurements onseven terrestrial, carnivorous felids reported basalrates between 123 to 151 % (McNab 2000b).

195BASAL METABOLIC RATE OF MARSUPIALS

Marsupial carnivores evolved in the absenceof eutherian carnivores at least twice, once inAustralia/Tasmania/New Guinea, andindependently in island South America. About3,500 years ago, a semi-domesticated form ofthe wolf, the dingo (Canis lupus [dingo]), wasbrought to Australia by seafaring Asians(Corbett 1995). Thereafter, indigenousAustralian marsupial carnivores, including thethylacine (Thylacinus cynocephalus), Tasmaniandevil (Sarcophilus harrisii), and eastern quoll(Dasyurus viverrinus), became extinct onmainland Australia, although they were able tosurvive on Tasmania in the absence of the dingo.The recent reduction in the geographic range onAustralia of the western quoll (D. geoffroii),spotted-tailed quoll (D. maculatus), and kowari(Dasyuroides byrnei) (Strahan 1983) also mayhave resulted from competition with eutheriancarnivores introduced by humans.

The eutherian abili ty to maximizereproductive output through an increase inenergy expenditure may have permitted thedingo to displace marsupial carnivores. It mayalso explain how the canids and felids invadingfrom North America with the establishment ofthe Panamanian land bridge were able todisplace carnivorous marsupials, such asthylacosmilids, indigenous to South America.The Neotropical marsupials that survived theinvasion were those that had habits thatprevented ecologically similar eutherians fromhaving high rates of metabolism and high ratesof reproduction, i.e., fruit- and insect-eating invarious combinations.

The demonstration in Australia thatmarsupial carnivores became extinct or had areduced distribution in association with theintroduction of eutherian carnivores raises thequestion why a similar impact has not beenseen in Australian marsupial grazers with theimportation of cattle and sheep, given that adifference in BMR between marsupial (87 to108 % of mammalian standard, excluding theburrowing wombat) and eutherian grazers (118to 237 %) is similar to that found in carnivores.Large macropods may withstand the presenceof the domesticated grazers as a result of theiradjustments to life in xeric environments,whereas cattle and sheep depend on humans tosupply water in much of central Australia. Animportation of desert ungulates into centralAustralia might represent a greater threat to

macropods. Indeed, the survival of dromedarycamels (Camelus dromedarius) in centralAustralia has been marked (Strahan 1983),although without any clear impact on macropods.

Early investigators, including Huxley (1880)and Martin (1902) suggested that marsupialswere evolutionarily intermediate betweenmonotremes and eutherians, and some recentworkers, including Lillegraven (1976), Pond(1977), Morton et al. (1982), Russell (1982),McNab (1986), and Lillegraven et al. (1987),have pointed out some of the limitations of themarsupial mode of reproduction. This led some(Kirsch 1977a, 1977b, Parker 1977, Low 1978,Hayssen et al. 1985) to defend marsupials asbeing at least equivalent to eutherians, andpossibly their superior in unpredictable,especially xeric, environments (Parker 1977,Low 1978), but see Morton et al. (1982) andThompson (1987). Part of this difference inopinion is based on the tendency to bepreoccupied with the reproduction of macropodsat the expense of other marsupials (Russell1982, Morton et al. 1982).

The analysis given here points out thatmarsupials are the equivalent of eutheriansunder some circumstances, namely in warm-temperate and tropical environments when theyhave food habits that require eutherians toabandon their reproductive advantage.Marsupials, however, have a difficult tasktolerating cold environments under allcircumstances and cannot tolerate the presenceof eutherians even in warm environments whenmarsupials have food habits that permiteutherians to have high rates of metabolism andtherefore high rates of reproduction. Aremarsupials competitively inferior to eutherians?Yes, under some circumstances.

ACKNOWLEDGMENTS

I thank Francisco Bozinovic for the invitationto contribute to this tribute to the life of MarioRosenmann. Charles Woods thoughtfully readan earlier version of this manuscript. I alsoappreciate reading a manuscript by NataliaVasey and D. Tab Rasmussen on the energeticsof reproduction in lorisid primates. PhilipWithers kindly responded to some questionsthat I had on the energy expenditure ofNotoryctes and Tarsipes.

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Associate Editor: Francisco BozinovicReceived December 2, 2004; accepted March 1, 2005