American Society of Mammalogists

Energetics and the Limits to a Temperate Distribution in Armadillos

Author(s): Brian K. McNab
Reviewed work(s):
Source: Journal of Mammalogy, Vol. 61, No. 4 (Nov., 1980), pp. 606-627
Published by: American Society of Mammalogists
Stable URL: http://www.jstor.org/stable/1380307 .
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 ENERGETICS AND THE LIMITS TO A TEMPERATE
DISTRIBUTION IN ARMADILLOS

BRIANK. MCNAB

ABSTRACT.-Acomparative study of the temperature regulation and rate of metab-

olism of armadillos and armadillo-likemammals(hedgehogs and hedgehog tenrecs) is
reported. Armadillos are characterized by low body temperatures, low basal rates of
metabolism, and high minimal thermal conductances. Strictly temperate species of
armadillos are confined in distribution to South America; they have higher body tem-
peraturesthan tropical species, but these groups show no noticeable difference in basal
rate or in minimal conductance. Armadillos that specialize on termites as food (e.g.,
Tolypeutes and Priodontes) have much lower basal rates and body temperaturesthan
other species. Hedgehogs, hedgehog tentrecs, and marsupialbandicoots also have low
body temperatures, low basal rates of metabolism, and high minimal conductances.
The principal reason why armadillos have low rates of metabolism is to prevent over-
heating in burrows, although termite-eating species may have lower basal rates than
other species due to variations in the spatial and temporal availability of prey. The
high minimal conductances found in these mammals prevent overheating in burrows
and reflect a protective armorof either horny plates (armadillos)or spines (hedgehogs
and hedgehog tenrecs). The interaction of low basal rates and high minimal conduc-
tances results in temperaturedifferentials between the body and environment that are
independent of mass and only about 25% of the values expected in mammals. Studies
of daily energy expenditure in Dasypus novemcinctus show a circadial rhythm of ac-
tivity and indicate that this species responds to a sharp fall in environmental temper-
ature by a reduction in activity and a modest reduction in body temperature. Large
individuals may take as long as 3 or 4 days for normalbody temperatureto be reestab-
lished after such a cold exposure. Armadillos have a limited capacity to invade cold,
temperate environments because food is unavailable at environmental temperatures
below 0?Cand because of their high thermal conductances. Armadillosor other similar
mammals enter cold, temperate environments either by storing enough fat to wait for
foraging to be possible again (D. novemcinctus) or by entering torpor (Zaedyus, Eri-
naceus, Setifer), a response that requires a small body size. Tolerance to starvation
through an increased mass is limited by the necessity to seek refuge in a burrow.
Young-of-the-year,lean individuals, and pregnant females are most susceptible to star-
vation at the geographic and climatic edge of their distribution.

Armadillos are among the most distinctive of Neotropical mammals. They are char-
acterized by moveable, horny bands that cover bony plates on the dorsal and lateral sur-
faces of the thorax and abdomen. They also have a set of plates on the dorsal surface of
the head, and most species have a series of plates encircling the tail. Most armadillos lack
more than a few coarse hairs, the majority of which are on the venter or along the skin
"hinges" between the horny plates. It is not surprising, therefore, that most armadillos
are limited in distribution to the tropics.
Conclusions on the thermal biology of armadillos based either on their morphology
or geographic distribution must be treated with caution. Firstly, there is no reason to
believe that the 20 species and 8 genera of armadillos are ecologically or physiolog-
ically identical. For example, armadillos vary in body mass from about 125 g (Chla-
myphorus) to 60 kg (Priodontes)-a 500-fold range-which in light of the conclusion
that body mass is the most important determinant of energy expenditure (Kleiber,
1932; Hemmingsen, 1960; McNab, 1970), suggests that there may be an appreciable
variation in the energetics of armadillos. It is thus noteworthy that two of the furriest
armadillos are the smallest species. Secondly, more species of armadillos invade the
South Temperate Zone than the North Temperate Zone (e.g., some 14 species are

J. Mamm.,61(4):606-627, 1980 606

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November 1980 McNAB-ARMADILLO ENERGETICS AND DISTRIBUTION 607

known to occur in Argentina). The presence of a single armadillo today in the North
Temperate Zone, then, is as likely due to the geographic isolation of North America
from the sources of armadillos as it is to their physiological incompetence. Some
armadillos are sensitive to arid conditions (Greegor, 1974; Humphrey, 1974), although
others tolerate these conditions; this difference is based on differential physiological
abilities to conserve water (Greegor, 1974, 1975).
Other mammals that are burrowing, soil- and litter-foraging omnivore-insectivores
include hedgehogs (Erinaceidae), which are found in Eurasia and Africa; certain ten-
recs (Tenrecidae), which are found on Madagascar; and to some extent (Keast, 1969)
bandicoots (Peramelidae) in Australia. Hedgehogs and certain tenrecs share with ar-
madillos a dorsal cutaneous shield, presumably as a protection against predators, al-
though in these insectivores it is made of spines. Bandicoots, however, do not have
such a shield, a condition that may represent either a difference in behavior between
bandicoots and the other soil omnivore-insectivores, or the paucity of large predators
in Australia.
The objectives of this paper are (1) to compare the rates of metabolism and tem-
perature regulation of various armadillos in relation to body size, food habits, and
geographic distribution, (2) to compare armadillos with their ecological counterparts
amongst hedgehogs, tenrecs, and bandicoots, and (3) to examine the factors that limit
the distribution of armadillos in temperate environments.

MATERIALS AND METHODS

Most of the animals used in this study were borrowed from zoos (especially the Lincoln Park
Zoo, Chicago; LPZ). The numbers of individuals and the species studied were: 2 hairy armadillos
(Chaetophractus vellerosus, bought froman animal dealer, who imported them from Argentina);
4 three-banded armadillos(Tolypeutes matacus, borrowed fromLPZ and collected in Argentina);
3 pichi (Zaedyus pichiy, LPZ; Argentina); 2 hairy armadillos (Chaetophractus nationi, LPZ;
Bolivia); 7 nine-banded armadillos (Dasypus novemcinctus, collected near Gainesville, Florida);
3 naked-tailed armadillos (Cabassous centralis, LPZ; Panama); 2 six-banded armadillos (Eu-
phractus sexcinctus, LPZ; Brasil); 1 giant armadillo (Priodontes maximus, LPZ; Guyana); 2
African hedgehogs (Erinaceus albiventris, LPZ; Gabon); 1 European hedgehog (Erinaceus eu-
ropaeus, CrandonParkZoo, Miami);2 spiny tenrecs (Setifer setosus, Crandon ParkZoo, Miami;
Madagascar).
Rate of oxygen consumption was measured in an open system employing a Beckman para-
magnetic oxygen analyzer. Carbon dioxide and water were absorbed from the air stream after
the animal chamber and before measuring the flow rate. Rates of metabolism were calculated in
the manner described by McNab (1978b), were corrected to dry STP, and were measured during
the daytime, which generally was the animal'speriod of quiescence. Depending upon body size,
animals were confined for measurement either in a 44-1 chamber, which was submerged in a
water bath for the maintenance of a constant environmental temperature, or in a 329-1 chamber
that had hollow walls through which water from a water bath circulated for temperature control.
The large chamber was covered with a styrofoamlayer to insure thermal stability.
Rectal temperature was measured immediately after each experiment at a given temperature.
An experiment was terminated normally after 2 to 3 hours when the animal was quiescent and
at a time when it was repeating a minimal rate of metabolism that had reoccurred several times.
The rates of metabolism that were used correspond to measurements of body temperature. If an
unusually low rate of metabolism occurred in the middle of an experiment, especially if it
occurred at low environmental temperatures,the measurement was not used because there was
no way of knowing whether it represented inactivity at a normalbody temperatureor a low body
temperature, unless of course the rate was repeated later and the corresponding body temper-
ature was measured. Animals were fed the night before some experiments and starved the night
before others; the resulting data were combined because there was no evidence that feeding
influenced the rate of metabolism or body temperature.
Thermal conductances are calculated from individual measurements of rate of metabolism and
body temperature at ambient temperatures below thermoneutralityusing the equation C = Vo)

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 TABLE 1.-Parameters of energetics of armadillos and armadillo-like ma
Basal rate of metabolism Minimal conductance
Mass (cm3 0/g-h) (cm3 O2/g- hC) Ft Tbt
Species (kg) mean ? SE (N) (%)* mean ? SE (N) (%)** - (?C)
Armadillos(Dasypodidae)
Chaetophractusvellerosus 1.11 0.276 ? 0.015 (10) 47 0.053 + 0.0011 (20) 177 0.27 34.4
Tolypeutesmatacus 1.16 0.181 ? 0.013 (13) 31 0.039 _ 0.0009 (44) 133 0.23 33.0
Zaedyuspichiy 1.74 0.226 + 0.013 (16) 43 0.027 ? 0.0011 (26) 113 0.38 35.2
Chaetophractusnationi 2.15 0.260 ?0.008 (18) 52 0.040 + 0.0009 (39) 185 0.28 35.5
Dasypus novemcinctus 3.32 0.243 + 0.012 (36) 54 0.039 ? 0.0015 (26) 225 0.24 34.5
3.70 0.250 57 0.029 176 0.32 34.5
Cabassouscentralis 3.81 0.213 +0.007 (15) 49 0.033 + 0.0008 (16) 204 0.24 33.6
5.89 0.019 ? 0.0007 (5) 146
Chaetophractusvillosus 4.54 0.178 ? 0.013 (7) 43 0.031 + 0.0014 (20) 209 0.21 35.1
Euphractussexcinctus 8.19 0.151 + 0.006 (31) 42 0.019 ? 0.0006 (36) 172 0.24 34.2
Priodontesmaximus 45.19 0.067 ? 0.004 (12) 29 0.010 + 0.0006 (14) 213 0.14 33.6
Hedgehogs (Erinaceidae)
Hylomys suillus 0.08 36.1
Hemiechinusauritus 0.40 0.38 50 0.083 166 0.30 33.8

Paraechinusaethiopicus 0.45 0.25 34 0.056 166 0.29 34.2

Erinaceus albiventris 0.45 0.326 ? 0.012 (13) 44 0.060 ? 0.0015 (25) 127 0.35 35.2
Echinosorexgymura 0.70 30.2
Erinaceus europaeus 0.75 0.45 69 0.056 153 0.45 34.0

2.00 0.258 + 0.013 (7) 50 0.029 ? 0.0009 (6) 130 0.38 34.5
Tenrecs (Tenrecidae)
Setifer setosus (July) 0.30 0.342 42 31.0
(January) 0.36 0.233 30 32.5
0.53 0.231 ?0.010 (19) 32 0.047 ? 0.0016 (20) 108 0.30 32.2
Tenrececaudatus 2.00 0.222 43 32.5
Bandicoots(Peramelidae)
Echymiperarufescens 0.62 0.49 71 34.6
Peramelesnasuta 0.65 0.49 72 0.057 145 0.50 36.1
Echymiperakalabu 0.70 0.49 74 35.0
Macrotislagotis 1.01 0.35 58 0.047 149 0.39 34.9
Echymiperarufescens 1.28 0.42 73 35.2
Isoodon macrourus 1.55 0.41 75 0.045 177 0.43 35.9
*% of predicted oxygen consumption,where predicted rate is 3.42 g-0.25 (Kleiber, 1932) = 100f,..
** % of expected minimalconductance,where predicted conductance is 1.00 g-0.50 (McNaband Morrison,1963) = 100f,.
t F = (%minimalconductance)= fI/fc.
t Tbat T,.
# AT1 = T0 - Ti.

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November 1980 McNAB-ARMADILLO ENERGETICS AND DISTRIBUTION 609

(Tb - Ta). An average and standard error for conductance were estimated over the range in Ta
where C is independent of Ta (see McNab, 1980). These minimal thermal conductances are
indicated in Figs. 1-4 by the slope of a metabolism curve placed below thermoneutralityin such
a manner as to extrapolate to Tb when Vo2is zero.
Continuous measurements of oxygen consumption in D. novemcinctus were made over 24 or
more h at various ambient temperaturesto obtain (1) the circadian patternof oxygen consumption
and (2) the summed 24-h consumption. The measurements were made in the 329-1 chamber on
two freshly-caught individuals, one 2.9 and the other 4.7 kg. The animals were placed individ-
ually on a 0.58-m2 platform in the chamber, which was large enough to permit appreciable
activity, although presumably less than an animal would have had in the field. The animals were
provided with food, nesting material, and an ambient photoperiod (November). Body tempera-
ture was measured at the beginning and end of a run and at daily intervals, if a run continued
longer than 24 h.
RESULTS
Measured body temperatures and rates of metabolism are plotted in Figs. 1-4 as a
function of ambient temperature for nine species of armadillos, one species of hedge-
hog, and one species of tenrec. Parameters extracted from these data are summarized
in Table 1 along with data taken from the literature. The general patterns found in
the energetics of armadillos and armadillo-like mammals will be examined in the
Discussion; other details of the species included in this study will be noted here.
The three-banded armadillo, Tolypeutes matacus, maintains a low body tempera-
ture (33.0?C) down to an ambient temperature of 5?C (Fig. 1A), a result that conflicts
with the observations of Eisentraut (1932), who found body temperature in this species
to vary with ambient temperature. He found that body temperature fell to 28 at 5?C.
Tolypeutes has a very low basal rate (31% of the basal rate expected in placentals from
mass by the 1932 Kleiber relation) and, in spite of being nearly hairless, has a rather
low thermal conductance (133% of the minimal thermal conductance expected by the
1963 McNab-Morrison relation) for an armadillo.
Chaetophractus vellerosus has a pattern typical of most armadillos (Fig. 1B). It
maintains a low (34.4?C) body temperature independent of ambient temperature at
least down to 5?C. The basal rate of metabolism is low (only 47% of the value expected
from mass) and minimal thermal conductance is high (177%). Consequently, the lower
limit of thermoneutrality is relatively high (30?C) for a mammal having a mass of 1.1
kg.
Unlike other species of armadillos, the pichi, Zaedyus pichiy, has a variable body
temperature with some propensity to enter torpor (Fig. 1C), especially at ambient
temperatures between 5 and 20?C. Eisentraut (1932) also reported a variable body
temperature in the pichi and Hatcher (1903) indicated that this armadillo hibernates.
Zaedyus entered a reversible torpor in the laboratory: body temperature fell to about
16?C at an ambient temperature of 15?C (Roig, 1971). Torpor and hibernation are cor-
related with the extreme austral distribution of the pichi, the southern limit of which
is approximately 50?S in Patagonia. Zaedyus has the lowest thermal conductance of
all armadillos measured (113%), even though it lacks any noticeable fur coat.
Dasypus novemcinctus, the nine-banded armadillo, maintained a body temperature
normal for armadillos (34.5?C) at air temperatures down to 5?C; the lowest body tem-
peratures were measured at ambient temperatures from 19 to 27?C (Fig. 1D). This is
the only species of armadillo to have had its rate of metabolism previously measured:
Johansen's (1961) values for basal rate and minimal conductance are similar to those
reported here (Table 1), but I found a thermoneutral range at least 10?C wide (28 to
38?C), whereas he measured a thermoneutral point near 30?C.
Chaetophractus nationi is somewhat hairier than other species of the genus, as is
to be expected from its high altitude distribution in Bolivia and northern Argentina.
Nevertheless, C. nationi has a thermal conductance indistinguishable from most other

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FIG 1.-Rate of oxygen consumption and body temperature as a function of ambient temperature: A
Chaetophractus vellerosus; C) in three Zaedyus pichiy; D) in five Dasypus novemcinctus.

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FIG. 2.-Rate of oxygen consumption and body temperature as a function of ambient temperature: A
three Cabassous centralis; C) in two Chaetophractus villosus; D) in two Euphractus sexcinctus.

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612 JOURNAL OF MAMMALOGY Vol. 61, No. 4

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FIG. 3.-Rate of oxygen consumption and body temperature as a function of ambient temper-
ature in one Priodontes maximus. The values marked "active" were the first experiments of
each day (see text).

armadillos (175%). This species regulates body temperature with precision at least
down to air temperatures of 5?C (Fig. 2A).
Cabassous centralis, the naked-tailed armadillo, is a strange animal about which we
know very little. For example, Griffiths (1968) stated that Cabassous is a specialized
feeder on termites, but the extent of this behavior is unknown (T. Carter, pers. comm.).
Cabassous is difficult to maintain in the laboratory because of its susceptibility to skin
and respiratory infections. As a result of cold exposures, a large (5.9 kg) female con-
tracted pneumonia and died before I obtained any measurements in thermoneutrality
although there was no evidence that the low rates measured in this individual reflected
illness; they seemed to be related to her large size. Cabassous regulates body tem-
perature rather precisely at warm temperatures, but permits it to fall at ambient tem-
peratures below 15?C (Fig. 2B). Eisentraut (1932) reported somewhat lower body
temperatures in C. unicinctus (28.5 to 33?C) at ambient temperatures between 6 and
16?C.
The large (8.2 kg) six-banded armadillo, Euphractus sexcinctus, like C. nationi and
C. villosus (Fig. 2C), maintains Tb at 34?C with precision between ambient temper-
atures of 10 and 30?C (Fig. 2D). Roig (1969) measured body temperatures in Euphrac-
tus sexcinctus that were similar to those that I measured, but showed a much greater
variation.
Priodontes maximus, the giant armadillo, regulated body temperature at a low level
(33.6?C; Fig. 3). Several measurements were made each day on the one Priodontes
that was available for study. In each case, the first run of the day, which usually started
at about 0700 h, resulted in a higher minimal rate of metabolism than was obtained
at the same temperature measured later on some other day. These higher values,
which are designated "active" in Fig. 3, did not appear to result from gross activity,
but may have reflected a circadian rhythm; they were not produced by handling,
because the animal was handled after every experiment to measure body temperature
and mass. Priodontes is noteworthy for its very low basal rate (29%) and very high
minimal conductance (213%).
Measurements of body temperature and rate of metabolism were also made on two
species of hedgehogs. The small tropical African hedgehog Erinaceus albiventris

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November 1980 McNAB-ARMADILLO ENERGETICS AND DISTRIBUTION 613

' W
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FIG.4.-Rate of oxygen consumption and body temperature as a function of ambient temper-

ature: A) in two Erinaceus albiventris; B) in two Setifer setosus.

maintained body temperature at 35.5?C down to air temperatures as low as 5?C (Fig.
4A). This hedgehog had a low basal rate (44%) and a moderate minimal conductance
(127%). I made only a few measurements on the European hedgehog, E. europaeus,
which are summarized in Table 1: its basal rate (50%) and minimal conductance
(130%) were similar to, but somewhat lower than, those presented by Shkolnik and
Schmidt-Nielsen (1976) (69 and 153%, respectively), possibly because my animal was
obese.
Finally, the spiny tenrec, Setifer setosus, often regulated body temperature be-
tween 31 and 33?C at ambient temperatures down to 11?C; but at other times body
temperature equilibrated between 23 and 29?C under apparently identical conditions
(Fig. 4B). At 5?C the maximal body temperatures fell, presumably reflecting a limited
capacity to maintain a temperature differential with the environment. Setifer had a
very low basal rate of metabolism (32%) and a rather low minimal conductance (108%)
compared to armadillos. Hildwein (1972) measured body temperatures and rates of
metabolism in Setifer similar to those reported here (Table 1).

DISCUSSION
of Armadillos
Climatic Distribution
Armadillos are principally tropical in distribution, but some species are found in,
or even limited to, the South Temperate Zone, and one species is found as far north

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614 JOURNALOF MAMMALOGY Vol. 61, No. 4

FIG. 5.-The approximate distributions of armadillos in Argentina as derived from Yepes

(1929), Minoprio (1945), Cabrera(1957), and Wetzel and Mondolfi (1979). The following abbre-
viations apply: Chvell = C. vellerosus, Chn = C. nationi, Chvill = C. villosus, Z = Z. pichiy, E =
E. sexcinctus, Cl = C. loricatus, Cu = C. unicinctus, P = P. maximus, T = T. matacus, Ds = D.
septemcinctus, Dn = D. novemcinctus, Dh = D. hybridus, Chl = Chlamyphorus truncatus,
Chr = Chlamyphorus retusa.

as the southern part of the North Temperate Zone. Because it is of interest to ask
whether tropical species of armadillos are physiologically different from temperate
species, the climatic distribution of armadillos will be defined here.
The influence of climate on armadillos can best be examined in Argentina, where
all genera and approximately 14 species occur (Fig. 5)-a close examination demon-
strates a bimodal distribution in total numbers of species along a north-south transect
(Fig. 6). Northern "tropical" armadillos reach their southern limits of distribution in
northern to central Argentina, including Priodontes maximus, two species of Cabas-
sous, Chlamyphorus retusa, Euphractus sexcinctus, three species of Dasypus, Chae-
tophractus vellerosus, and Tolypeutes matacus. Southern, "temperate" armadillos
have their northern and southern limits to distribution in Argentina, including Chae-
tophractus villosus, Chlamyphorus truncatus, and Zaedyus pichiy. In addition, Chae-
tophractus nationi has a latitudinal distribution similar to tropical species, but is found
at high elevations in the Andes, and thus, in terms of climate, may best be considered
a temperate species. Dasypus novemcinctus, from this view, is essentially a tropical
species that has expanded into both the South Temperate and North Temperate zones.
It is of further interest that this species has penetrated the North Temperate Zone
(where it is the only armadillo) farther than it has the South Temperate Zone, where
it encounters many other species.

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November 1980 McNAB-ARMADILLO ENERGETICS AND DISTRIBUTION 615

A TRMOPICALSPECIES

L. < TEMPERATE
o SPECIES
(0
w

0
30 40 50
LATITUDE(?S)

15 lo0 5

JULYMEAN ISOTHERM(*C)
FIG. 6.-Number of species of armadillos found along a north-south transect (A-A') in Argen-
tina (see Fig. 5). Armadillos that have a latitudinal range completely enclosed within Argentina
are designated as "temperate" species; those that only reach their southern limits in Argentina
are designated as "tropical"species (for exception, see text).

There are few clear morphological correlates of climatic distribution in armadillos.

The largest armadillos (Priodontes, Euphractus, Cabassous) are strictly tropical. Even
within the genus Dasypus, the southern limit of distribution of the smaller D. hybri-
dus is about 10? south of the southern limit of the larger D. novemcinctus in Argentina.
Within the genus Chaetophractus, however, the larger species are found on the pam-
pas (C. villosus) or in the Andes (C. nationi), whereas the small C. vellerosus is found

? 36- X (<=5r A DISTRIBUTION

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ioog Ikg 10 100
BODY MASS
FIG. 7.-Body temperature as a function of body mass in armadillos and armadillo-like mam-
mals. Independent values for a species are linked together. Data are from Table 1.

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616 JOURNALOF MAMMALOGY Vol. 61, No. 4

-0.2 -

I0.4- -0.4-

03) -0.6- Z

l02lJ N - ^^/ ^. 100

IL 0.05'- - X HEDGEHOGS
- -1E2V- + TENRECS A I -
O1) o BANDICOOTS

-1.4 + TN
-1.0 0.0 1.0 2.0
LOG10M

0.1 0.5 1.0 5 10 50 100

BODY MASS (kg)

FIG. 8.-Basal rate of metabolism as a function of body mass in armadillos and armadillo-like
mammals. Parallel lines represent percentages of the Kleiber (1932) relation for mammals. All
other symbols are as in Fig. 7. Data are from Table 1.

in the warmer Chaco-Mendoza region. Furthermore, there does not appear to be any
marked tendency for armadillos having a temperate distribution to be more heavily
furred than tropical armadillos. The question remains whether temperate and tropical
species are physiologically distinct.
Body Temperature
Temperate armadillos and bandicoots regulate body temperature at higher levels
than tropical species, although bandicoots have higher temperatures than armadillos
living in the same thermal climate (Fig. 7). The five species of tropical armadillos
studied have body temperatures between 33 and 34.5?C, the highest value being
found in D. novemcinctus, which behaves like a temperate species in North America.
Body temperature in hedgehogs does not appear climatically variable, although the
lowest body temperature reported for an erinaceid, 30.2?C, is found in the moon-rat,
Echinosorex, from Southeast Asia (Rudd, 1966). The tenrec Setifer has a very low
body temperature (ca. 32?C).
Basal Rate of Metabolism
All mammals included in this study have low basal rates of metabolism: most ar-
madillos have basal rates between 40 and 60% of the values expected from mass (=
100f , fm being a coefficient that measures the degree to which the basal rate conforms
to Kleiber's relation); most hedgehogs have basal rates 40 to 65% of the expected

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November 1980 McNAB-ARMADILLO ENERGETICS AND DISTRIBUTION 617

j0.10O- -I.0-
0 - 100% 150 200 300

E - x
I-L
W - .TEMPERATE ARMADILLOS
z
0
0- -O \

0
m m.A 7. D
X HEDGEHOGS a

o ~ -i.-LOGoM

undependable in space and

_e time. Clearly, this is case in temperate environments,

BODY MASS (kg)

Some species have unusually low basal rates. These include two armadillos, T.
matacus (31%) and P. maximus (29%); both species are termite-eaters (Eisentraut,
1952; Kiihlhorn, 1952; G. G. Montgomery, pers. comm.). The desert hedgehog, Par-
aechinus aethiopicus, has a lower basal rate (34%) than more mesically distributed
hedgehogs (Shkolnik and Schmidt-Nielsen, 1976). Similarly, the long-eared bandicoot,
Macrotis lagotis, which also lives in a desert, has a lower basal rate (58%) than other
bandicoots (Hulbert and Dawson, 1974). Tenrecs have low rates of metabolism, but
it appears that hedgehog tenrecs may have relatively lower rates (ca. 30 to 40%) than
other tenrecs
other tenrecs (e.g.,
(e.g., Tenrec, ca. 43S;
Tenrec, ca. 43%; Hildwein,
Hildwein, 1970).
1970).
Mammals with the habits of armadillos clearly have low basal rates of metabolism.
Several correlates of low basal rates in mammals have been shown: fossorial and
burrowing habits (McNab, 1966, 1979b), seasonal food supplies (McNab, 1969, 1979a),
and, possibly, the chemical composition of food (McNab, 1978b).
The low basal rates of armadillos, hedgehogs, and bandicoots issue principally from
coupling burrowing habits with a large mass, in part because the tendency to overheat in
burrows increases with body mass (McNab, 1979b). Another factor that may contribute
to the low basal rates of these mammals is that their food is a resource that may be
undependable in space and time. Clearly, this is the case in temperate environments,

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618 JOURNALOF MAMMALOGY Vol. 61, No. 4

where feeding is essentially impossible during periods when the soil is frozen, or
nearly so; even in tropical and subtropical environments there may be marked sea-
sonal variations in the availability of soil invertebrates and vertebrates in relation to
a wet-dry seasonality. There is no reason to believe that the chemical composition of
foods used by most armadillos is incompatible with high basal rates.
The unusually low basal rates of termite-eating and desert-dwelling species may
indicate that the availability of termites in the tropics or of soil invertebrates in a
desert is more variable than is the case when a broader spectrum of prey is used or
when a temporally less variable environment is occupied. For example, termitivorous
armadillos feed on prey that tend to be localized in space and, more importantly, may
be available for only short periods of time because of the defenses used by termites
(Lubin et al., 1977). I have observed that termite-eaters in the field often appear to be
in a poor nutritional condition. Low basal rates in the desert-dwelling hedgehog and
bandicoot may reflect a variability in the available food supply that is related to a
seasonally sporadic rainfall. Therefore, the basal rates of termite-eating and desert-
dwelling species may be fixed at a level corresponding to the period of lowest food
availability.

Minimal Thermal Conductance

All mammals included within this study have high thermal conductances (Fig. 9),
most of which vary from 150 to 225% of the values expected from body mass (= 100fc,
where fc is a measure of the agreement of measured conductances with those expected
from the standard relation of McNab and Morrison, 1963). The high conductances of
most armadillos and hedgehogs result from the replacement of a fur coat by protective
armor. High minimal conductances, however, are also typical of bandicoots, which have
no such armor.
Certain species have rather low minimal conductances. They include those with a
temperate distribution (e.g., the hedgehog E. europaeus, 130%, and an armadillo, Z.
pichiy, 113%), or those that have an unusually low basal rate of metabolism (e.g., T.
matacus, 133%; S. setosus, 108%; and P. aethiopicus, 119%). Other temperate species,
however, do not have low minimal conductances: e.g., D. novemcinctus invades tem-
perate environments in both the northern and southern hemispheres in spite of its
high thermal conductance (ca. 200%). An interesting exception is found in D. pilosus,
where a high altitude (2,400-3,000 m) distribution (in Peru) is associated with such
a heavy fur coat that the carapace is obscured (Wetzel and Mondolfi, 1979). Well-
developed fur coats are also present in the small armadillos of the genus Chlamyph-
orus.
It appears that the high conductances of armadillos and other armadillo-like mam-
mals have their significance, mainly, as a means of minimizing heat storage in mam-
mals that are active in burrows (McNab, 1979b). Evidence for this interpretation is
found in the observation that low conductances occur only in small species or in those
with low basal rates, that is, in species least likely to store heat.

Interaction of Basal Rate, Minimal

Conductance, and Body Mass
In the simplest model of endothermy (McNab, 1980), the interaction of basal
rate (VbO2), minimal conductance (Cm), and body mass (m) defines the temperature
differential maintained at the lower limit of thermoneutrality (AT,) (McNab, 1970,
1974):
ATe = VbOICm
= 3.42 fm* mM075/1.00'f mn050
= 3.42F m025, (1)

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November 1980 McNAB-ARMADILLO ENERGETICS AND DISTRIBUTION 619

where F equals the ratio fm/fc,which is the ratio of the mass independent variation
in basal rate to the mass independent variation in minimal conductance and which
represents variations in ATe independent of mass. Thus, armadillos that have basal
rates one-half of expected (fm= 0.5) and minimal conductances twice those expected
(fc = 2.0) have temperature differentials at Te that are only one-quarter (F = 0.5/2.0 =
0.25) those of "standard"mammals of the same size. A small ATe means that the lower
limit of thermoneutrality is high, that body temperature is low, or that some combi-
nation of these features is present. The armadillo with the largest temperature differ-
ential relative to that expected from mass, Z. pichiy (F = 0.38), has the most temperate
distribution.
ATfeis expected from equation (1) to increase with m025,but armadillos, like other
burrowing mammals (McNab, 1979b), have a ATe independent of mass, at least at
masses greater than 2 kg. This independence of mass occurs because V^o2and Cmare
both proportionalto mass raised to the same power, i.e., ca. m?-60(McNab, 1979b). As
a result, body temperature of armadillos is also independent of mass, especially within
a climatic unit (Fig. 7).
Armadillos tend to compensate for a small body size with a modest increase in
insulation. For example, in Tolypeutes the insulation appears to be derived from air
that is trapped when the carapace is partially or completely closed, and not due to an
increase in pelage. However, the two smallest armadillos, Chlamyphorus truncatus
(ca. 125 g) and C. retusa (ca. 250 g), are furry. C. truncatus has a carapace that is
supported by the neural arches of the vertebral column; pelage grows underneath the
carapace and on the venter (Minoprio, 1945), so that the layer of air trapped under
the carapace must be an effective insulator.
The small size of C. truncatus raises a question as to its thermal behavior. An
analysis of the scaling of metabolism and temperature regulation in endotherms shows
that if the Kleiber relation found at large masses is carried unmodified to small masses,
the ability of an endotherm to thermoregulate is greatly reduced. In fact, the smallest
mass consistent with effective thermoregulation at a basal rate equal to 50% of the
value expected from the Kleiber relation is about 166 g. At smaller masses endothermy
fails; therefore, an armadillo weighing 125 g and having fm equal to 0.5 would be
expected to enter torpor, although some compensation for small size may be found in
a reduction of fc For example, the fc required of a 125 g armadillo for ATt to equal
6.0?C, a value typical of larger armadillos, can be estimated from equation (1) as
follows:

6.0 = 3.42(-?5 )(125)? 25.

Thermal conductance in C. truncatus therefore must equal about 95% of the value
expected from mass in temperate mammals. Larger differentials would require lower
conductances. A reduction in minimal conductance, compensatory for a low basal rate
coupled with a small body size, also has been demonstrated in marsupials (McNab,
1978a) and heteromyid rodents (McNab, 1979a), and I have similar data for anteaters.
Otherwise, small armadillos can maintain endothermy at a mass of 125 g, if they have
a basal rate no less than 0.62 cm3 O2/g'h, which is 61% of the Kleiber value and 121%
of the armadillo value (e.g., fm = 0.5). Obviously, only further study of this species
will determine whether it uses torpor and has a basal rate typical of other armadillos
or has a higher basal rate to preserve endothermy.

Daily Energy Expenditure in Dasypus novemcinctus

Continuous 24-h measurements of rate of metabolism in a 2.9-kg D. novemcinctus
at 9, 24, and 30?C show the highest daily rates occurring at 9 and the lowest at 30?C

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620 JOURNALOF MAMMALOGY Vol. 61, No. 4

20-
W -4700g
x 30C /
o 24oC
* 9C \

344
E-?Tb

0 10-
(.3

D 5-
34 2 e
z-
CL T32.1

.L
o-? I I _

0. W:2900g
o,- X 3oc

12 12C 18 24 06

FIG. 10.-Energy expenditure as a function of time of the day, ambient temperature,and body
mass in two Dasypus novemcinctus.

(Fig. 10). A close inspection of these data, however, shows some anomalies. For ex-
ample, at 9?C the daily rate (139.4 kcal or 6.8 watts) is only 1.6 times the measured
basal rate, whereas the standard rate of metabolism (in similarly sized individuals, 3.3
kg) at 9?C is approximately 3.9 times the basal rate (Fig. 1D). This small increase
undoubtedly reflects a reduction in effective thermal conductance produced by a nest
and may also indicate that little activity occurred. Yet, there was some activity, as is
shown by the sinusoidal shape of the curve. The normal body temperatures measured
at the end of the two runs exclude the possibility that the low rates were due to low
body temperatures.
Expenditures in the 2.9 kg individual at 24 and 30?C are more difficult to analyze.
At 240C the expenditures are only about 1.1 times the basal rate, in spite of evidence
of activity. In part, the low expenditures are related to a 1?C fall in body temperature.
Most peculiarly, the expenditures at 30C are only the 1.6
timesf measured "basal" rate,
even though body temperature a the end of the runs was normal. There was little
activity at this tempproximature.If the 24-h expenditure at 9?C is compared to the 24-h
expenditure at 30C, rather than to theffective
rate measured for 2 to 3 h under "by a
nestandard"
conditions, the ratio becomes 4.1:1, which is close to the increase expected from Fig.
1D. This calculation suggests that the factor by which the rate of metabolism increases,
as a result of the fall in Tdividual
agrees with the conductance derived from Fig. D, but
that the minimal
that the minimal rate
rate is lower than the
lower than the "basal"
"basal" rate.
rate.

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November 1980 McNAB-ARMADILLO ENERGETICS AND DISTRIBUTION 621

The 4.7 kg individual had its highest rate of metabolism at 9?C (Fig. 10); still, this
rate was only 2.8 times the basal rate, in spite of activity and a normal body temper-
ature. At 30?C the daily expenditure was about 92% of the basal rate; there was little
activity and body temperature was normal. Most interestingly, the total daily expen-
diture was lowest at 24?C:it was only 49% of the basal rate, even though this ambient
temperature is below thermoneutrality.One factorcontributing to the low expenditure
was that body temperature was 2.5?C below the normal level. At 24?C, then, both
individuals permitted body temperature to fall, a tendency that was also seen under
standard conditions (Fig. ID).
At low ambient temperatures the rate of metabolism requires several days to arrive
at a steady-state. For example, the 4.7 kg individual was taken from a room maintained
at 24?C and placed directly into the chamber regulated at 9?C, where it stayed for 96
h (Fig. 11). This individual originally had a body temperature of 31.7?C. During the
first 24 h there appeared to be little activity and the body temperature was probably
permitted to fall. The total energy expenditure during this period was only 68.2 kcal
(3.3 watts, or 55% of the measured basal rate). During the second night, rate of me-
tabolism increased, presumably associated with activity; the 24-h energy expenditure
stabilized at a new, higher level (174.1 kcal, 8.4 watts, or 1.4 times the basal rate) and
body temperature rose to 33.3?C. During the third night, another increase in energy
expenditure occurred in relation to activity (to 294.1 kcal, 14.3 watts, or 2.4 times the
basal rate); body temperature now was 34.6?C. During the fourth night the rate of
energy expenditure again increased, but returned in the morning to the level of the
previous morning; body temperature did not increase above the level of the previous
day (34.4?C). The total energy expenditure showed a modest increase to 340.2 kcal
(16.5 watts, or 2.8 times the basal rate).
Clearly, nine-banded armadillos permit body temperature to fall at intermediate
environmental temperatures and, furthermore, may take several days to adjust to a
rapid decrease in ambient temperature. Both of these behaviors reduce energy ex-
penditure; they may be more highly pronounced in large individuals. It is of interest
that Dasypus in Florida often are not seen for a few days immediately after the arrival
of a marked cold front in winter (Gause, 1980), a behavior that may reflect the
physiological lag in responding to a decrease in ambient temperature.
These data on daily energy expenditures raise questions on the significance of
the rates reported in Fig. 1D: why does Dasypus sometimes respond immediately to
low temperatures with an increase in metabolism, and other times with a fall in body
temperature? Is this difference simply related to the length of the cold exposure? At
present these questions cannot be answered.
Limits to a Temperate Distribution in Armadillos
Armadillos are essentially tropical in distribution. They may face a climatic limit in
temperate zones as a result of their low rates of metabolism, high thermal conduc-
tances, and temperature-sensitive food supply. There are few mammals that have been
shown to have a thermal limit to their distribution. These possibly include: the Vir-
ginia opossum, which is in part limited by the size of its fat stores and the availability
of its food resources (Brocke, 1970); vampire bats, where wing-loading limits food
transport in flight and, therefore, may limit tolerance to low cave temperatures
(McNab, 1973); and some temperate cave bats, which are limited in distribution to
regions that contain cool caves, where hibernation can occur (McNab, 1974).
Armadillos feed mainly on soil invertebrates; consequently, foraging at air temper-
atures below freezing would be of little value, especially if the soil were frozen or
covered with snow. In fact, armadillos in Florida tend to forage during the day in
winter, when it may freeze at night, whereas they are nocturnal during the spring and
summer, thereby evading high daytime temperatures and heat loads (similar obser-

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622 JOURNALOF MAMMALOGY Vol. 61, No. 4

vations were made on C. vellerosus in Argentina by Greegor, 1975). In cooler regions

armadillos would be expected to remain in their burrows when freezing temperatures
occur during the day.
There are two alternative solutions to the starvation incurred during protracted
periods when foraging for food is of little value. One is to accumulate appreciable fat
stores to be used at normothermic rates. The second is to evade starvation by greatly
reducing energy expenditure through entering torpor and, on a seasonal basis, hiber-
nation. These solutions require different physiological and morphological adjust-
ments.
Maintaining body temperature.-The ability of an armadillo to withstand a period
of starvation while remaining normothermic in a burrow depends upon many factors,
including (1) the amount of energy stored as body fat, and (2) the rate at which an
armadillo uses these stores, as determined by burrow temperature, body temperature,
thermal conductance, and activity. The maximal length of this period is given by the
following relation:

t (days) (kcal/day) (2)

E (kcal/day)

where the available energy store (S) equals: (energy content per g fat) x (original
fraction fat content of body minus fraction fat content of body at death) x (original
body mass in g) = 9.3(ft - fo)m. The rate of energy expenditure (E) at temperatures
below the region of thermoneutrality equals C(T b - Ta) = 0.115 f m050(TT - Ta),
where the coefficient 0.115 has the units kcal/day- ?C and m is in grams, assuming that
the animal is inactive. Therefore, equation (2) becomes

t= 80.9(f - ) (m03)

Equation (3) was evaluated for various periods (t) as a function of body mass and
fat reserves. Based on the field measurements of Gause (1980), adult (>3.0 kg)
male and nonpregnant female Dasypus in Georgia and Florida commonly have
from 14 to 19% of the total mass as fat in October and November; pregnant females
have about 24%; and immatures (<3.0 kg) have only about 10% fat. To estimate t, it
was assumed that (1) the minimal amount of body fat compatible with survival (fo) is
about 2% of total mass, (2) minimal thermal conductance is twice the value expected
from mass (fc = 2.0), and (3) body temperature is 34.5?C. The calculated survival times
are plotted in Fig. 12 as a function of body mass at two burrow temperatures (10 and
0?C) for three fat deposits (10, 14, and 24%).
It is clear from equation (3) and Fig. 12 that the maximal time period for starvation
tolerated by armadillos (1) increases with body mass, (2) increases with the size of fat
deposits, and (3) decreases with a decrease in burrow temperature. Thus, a 5-kg adult
armadillo storing 14% of its total mass as fat can survive starvation for about 10 days
at a burrow temperature of 0?C and about 14 days at 10?C. The smallest armadillos
encountered in Florida and Georgia between October and February weigh about 2
kg, although G. Galbreath (pers. comm.) states that in central Florida immatures in
winter may weigh as little as 1.3 kg (due to low fat content?). Therefore, if a 2-kg
immature had stored only 10% of its mass as fat, it could withstand starvation for only
4 days at 0?C or 6 days at 10?C, which would make it difficult for armadillos of this
mass to survive winter in a cold climate. Gause (1980) observed that the first
individuals to forage during a prolonged cold period are the immatures and preg-

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November 1980 McNAB-ARMADILLO ENERGETICS AND DISTRIBUTION 623

20-

.5

15 -

Cr

z-
X
LIJ
5-
0(.9
c1:
LIJ
wJ
0- * I I I1
18 24 06 12

TIME OF DAY (hours)

FIG. 11.-Energy expenditure as a function of time of the day over a 4-day period in a 4.7-kg
Dasypus novemcinctus.

nant females, which means that the large fat deposits of pregnant females may be a
compensation for a high cost of pregnancy.
These observations and calculations make it clear that all individuals in a population
are not equally tolerant of a cold winter. Although adult male armadillos can often
survive a cold winter if they have sufficient fat deposits, several cold winters in a row
could so reduce the recruitment of young into a population that the temperate edge
of a population would shrink equatorally with adult mortality.

25-

20-

03

0 2 4 6
BODY MASS (kg)
FIG. 12.-Survival time for tolerating starvationas a function of body mass, fat content of the
body, and ambient temperature. See text for the basis of these calculations.

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624 JOURNALOF MAMMALOGY Vol. 61, No. 4

It can be concluded that my (1971) analysis of Bergmann's rule overlooked the

possibility that a large body size can transitorily contribute to survival in a cold climate
during periods of starvation. Calder (1974) clearly appreciated this possibility. It
should be reemphasized, however, that the maintenance cost for a large individual is
greater than it is for a small individual because maintenance is proportional to m?'75
(in thermoneutrality) or to m? 50(below thermoneutrality).
It is of special interest to compare the northern limits of distribution of Dasypus
with those of the opossum, Didelphis virginiana, which also is of tropical origin. The
armadillo extends as far north as central Oklahoma and Arkansas, and southern Mis-
sissippi, Alabama, and Georgia (Humphrey, 1974), but Didelphis enters central Min-
nesota, northern Wisconsin, central Michigan, southern Ontario, northern New York,
and southern Vermont and New Hamsphire (Brocke, 1970). What accounts for the
greater tolerance to a cold winter in Didelphis?
Brocke (1970) estimated that ft = 0.270, fo = 0.083, and fc = 1.0 for Didelphis in
Michigan. A 3.3-kg opossum at 10?C would be expected from equation (3) to survive
35.0 consecutive days without foraging, assuming that its body temperature is 34.8?C
(McNab, 1978a). Even in the northern United States few opossums would have to
remain in burrows for 35 consecutive days; Brocke (1970) estimated that in central
Michigan up to 62% of an opossum's winter energy expenditure comes from foraging.
A 3.3-kg adult Dasypus at 10?C would only survive 11.4 days, or 3 weeks less than an
opossum. Most of the difference between these species in tolerance to cold is related
to the excellent insulation of the opossum and the poor insulation of Dasypus. This
difference is emphasized by the climatically flexible conductance of Didelphis: in
Panama fc equals 1.7 or 1.8, in Florida 1.3 or 1.4, whereas in Michigan it may be 1.0
(McNab, 1978a). Dasypus of all ages, however, use twice as much fat in northern
Florida and southern Georgia between October and February as they do in southern
Florida (Gause, 1980). Thus, in the absence of a climatically flexible insulation,
Dasypus has a climatically dependent energy expenditure. Observations in
this paper on Dasypus and in the work of Brocke (1970) on Didelphis indicate that
both species may extend these calculated periods somewhat by having minimal rates
of metabolism less than "basal" rates.
Finally, if survival times increase with body mass, what prevents D. novemcinctus
from extending t by being even larger? This question takes special significance when
it is realized that D. bellus was found in the southern U.S. in the Pleistocene and had
a mass of 20 to 30 kg. It is unclear whether D. novemcinctus evolved directly from
D. bellus or whether it ecologically replaced D. bellus (Robertson, 1976). In either
case, Dasypus in North America decreased in size. It should be remembered that the
largest armadillos today are limited in distribution to the tropics. The principal re-
action of D. novemcinctus to cool environmental temperatures is to seek shelter in
burrows. In fact, the presumptive evolution of a small body mass in D. novemcinctus
may have been related to an increased dependence on burrowing as a response to
cold ambient temperatures. The evolution of a small body mass in association with
the acquisition of burrowing habits also has been suggested to have occurred in the
tortoise genus Gopherus (Auffenberg, 1962; Auffenberg and Weaver, 1969). In both
Dasypus and Gopherus the larger species failed to survive the Pleistocene, whereas
the contemporary species are smaller and have burrowing habits.
Why is a large body size not as good as burrowing habits in promoting survival of
armadillos in a cool climate? Equation (3) suggests that a 25-kg armadillo could extend
survival time by 12 days at a temperature of 0?C compared to a 5-kg individual. The
problem with this calculation is that it ignores the freezing of superficial tissues that
would occur in animals exposed at night in winter and it ignores the fact that a large
body mass has a higher cost of maintenance than a smaller mass.
It can be concluded that Dasypus is limited in its expansion into temperate envi-

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November 1980 McNAB-ARMADILLO ENERGETICS AND DISTRIBUTION 625

ronments in North America (1) by a food that is unavailable when the ground is frozen
or is covered with snow and (2) by the inability of Dasypus to reduce energy expen-
diture. The tolerance of D. novemcinctus to cool winters is a compromise between
the increased tolerance to starvation attained by a large body mass and the evasion of
low winter temperatures acquired by burrowing, a habit that requires a small body
mass. The only other solution, of course, is to evade low ambient temperatures by
entering torpor.
Entering torpor.-The use of torpor generally requires a small body mass (Morrison,
1960). It is therefore significant that the armadillo with the most extensive temperate
distribution, Zaedyus pichiy, has only half the mass of D. novemcinctus and is the
only edentate known to enter torpor. Dasypus, on the other hand, can only slightly
extend survival time by entrance into a shallow, transitory depression of body tem-
perature. The smaller body mass of Zaedyus, however, does not make it vulnerable
to low temperatures, even during thermoregulation, because of its low minimal con-
ductance. The consequences of the difference in body mass and minimal conductance
between Dasypus and Zaedyus can be evaluated for survival times by applying equa-
tion (3). For example,

tz ot
(mz/m?)0 50
td fcz/fcd

(1.74/3.32)0.50 = 51
1.1/2.3

where the subscript z stands for Zaedyus and d stands for Dasypus. Thus, Zaedyus
has a minimal conductance more than low enough to compensate for its smaller body
mass.
The interaction between body size and the propensity to enter torpor is illustrated
in the tenrec Setifer setosus. Setifer encounters seasonally cool environmental tem-
peratures and periodic droughts on the plateau of Madagascar (Eisenberg and Gould,
1970). Its low rate of metabolism and low thermal conductance permit it to live off of
its fat reserves for an appreciable period, in spite of its small mass, but the main means

0-
C 10- ^SETIFER
O f\-tlc o ARMADILLOS
- HEDGEHOGS
\
8. \\\ I+ TENREC
(I)

8
_ \_ \ TEMPERATE
11,,~~ \\ 5~ ~SPECIES
o - \\ \-

5-
i'Y' TROPICAL
SPECIES \
THATENTERA Z\ \ \ ZAEDYUS
-~. TEMPERATE
ZONE E. EUROPAEUS
EUROPAEUS STRICTLY
LL E.
- I \\ \ TROPICAL
SPECIES
TOLYPEUTES_p DASYPUS /
Z CH.VELLEROSUS \ /
LU \
(X o
LL -o

0 LOG
Q) -I
10M
LOG

0.1 1.0 10 100

BODYMASS (kg)
FIG. 13.-Variation in body temperature (over a range in ambient temperature in which body
temperature is independent) as a function of body mass in tropical and temperate armadillos and
armadillo-like mammals.

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All use subject to JSTOR Terms and Conditions
626 JOURNAL OF MAMMALOGY Vol. 61, No. 4

by which Setifer tolerates cold or dry periods is to enter torpor. Setifer goes into
torpor with a greater frequency than Zaedyus, apparently in relation to the smaller
mass of the tenrec: temperate mammals with armadillo-like habits use torpor with
increasing frequency as body mass is reduced (Fig. 13). Small tropical species, such
as the hedgehog E. albiventris, however, do not readily enter torpor (Fig. 13).
The limitations associated with maintaining body temperature at high levels or with
tolerating starvation make it clear that the most effective response to seasonally cold
environments in soil and litter omnivores is a reduction in mass and the evolution of
torpidity, which has occurred in such species as Zaedyus pichiy, Erinaceus europaeus,
Setifer setosus, and Echinops telfairi. These interactions again raise the question
whether the tiny armadillo Chlamyphorus truncatus readily enters torpor or whether
its fossorial habits provide what is essentially a tropical microclimate.

ACKNOWLEDGMENTS
This work depended completely on the kind cooperation of the Lincoln Park Zoo (Chicago)
and, especially, that of the Director, L. E. Fisher, and the Associate Director, D. A. Meritt, Jr.
J. Eisenberg, National Zoological Park,Washington,also loaned animals for this study, as did R.
Sampsell of the Crandon Park Zoo in Miami. Various drafts of this manuscript were critically
reviewed by A. Carr, D. Webb, and G. Gause, University of Florida; G. Galbreath, University
of Chicago; K. Redford, HarvardUniversity; and C. Beuchat, Cornell University. W. Auffenberg,
University of Florida, freely discussed his views on the evolution of tortoises with me. G. Mont-
gomery, Smithsonian Tropical Research Institute, kindly informed me of some aspects of the
field biology of tropical armadillos. T. Carter and J. Shaw, Oklahoma State University were
thoughtful hosts and guides at their field camp in Minas Gerais, Brasil. I thank two reviewers
of this manuscript, one of which was D. Hinds, California State University (Bakersfield), for
their constructive comments. To all of these individuals I extend my gratitude. This work was
assisted by NSF Grant GB-20689.

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