Division of Comparative Physiology and Biochemistry, Society for Integrative and

Comparative Biology

Metabolism of Squamate Reptiles: Allometric and Ecological Relationships

Author(s): Robin M. Andrews and F. Harvey Pough
Source: Physiological Zoology, Vol. 58, No. 2 (Mar. - Apr., 1985), pp. 214-231
Published by: The University of Chicago Press. Sponsored by the Division of Comparative
Physiology and Biochemistry, Society for Integrative and Comparative Biology

Stable URL: http://www.jstor.org/stable/30158569 .

Accessed: 06/08/2014 08:36

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .
http://www.jstor.org/page/info/about/policies/terms.jsp

.
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of
content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms
of scholarship. For more information about JSTOR, please contact support@jstor.org.

The University of Chicago Press and Division of Comparative Physiology and Biochemistry, Society for
Integrative and Comparative Biology are collaborating with JSTOR to digitize, preserve and extend access to
Physiological Zoology.

http://www.jstor.org

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

METABOLISM OF SQUAMATE REPTILES: ALLOMETRIC

AND ECOLOGICAL RELATIONSHIPS'
ROBINM. ANDREWSAND F. HARVEYPOUGH
Departmentof Biology,VirginiaPolytechnicInstituteand State University,Blacksburg,Virginia24061-0794;
and Sectionof Ecologyand Systematics,CornellUniversity,Ithaca,New York 14853-0239
(Accepted9/20/84)
We used multiple regressionanalysis to evaluate the relationship between metabolic
rate and three independent variables-mass, temperature, and standard or resting
state-for squamate reptiles. For comparisons among adults of different species,
mass raised to the .80 power explains 88% of the variation in metabolic rate. (The
.80 mass exponent is significantly greater than the .75 predicted by theoretical
considerations.) A further 8% of the variation in metabolic rate is explained by body
temperature and whether the lizard is in a standard or resting metabolic state.
Residuals were used to determine whether metabolic rates varied as a function of
phylogenetic relationship or ecological grouping. Familial associations explained
16% of the variation in metabolic rate for varanids, lacertids, iguanids, colubrids,
scincids, xantusiids, gekkonids, and boids. More variation (45%) was explained when
lizards were partitioned into four ecological categories:day-active predators, hervibores,
reclusive predators, and fossorial predators. A single equation relating metabolic
rate to mass is thus inappropriate to estimate the metabolism of squamates. For
intraspecific comparisons, the mass exponents of the relationship between metabolic
rate and mass are significantly lower than .80 for 25 of 28 data sets. Estimating the
metabolic rates of juvenile squamates from equations based on comparisons among
species is thus invalid. Moreover, there is significant variability among mass
exponents among the 14 species that met the statistical requirements for analysis of
covariance, and a common mass exponent cannot be assumed for intraspecific
comparisons.
INTRODUCTION
Large animals use more energy than
small ones, but the correct expression of
that truism has long been a subject of
The relationship between
controversy.
metabolic rate (MR) and mass (M) is most
commonly expressed as a power (or allometric) function of the form MR = aMb,
where a and b are the mass coefficient and
' We would like to thank RaymondHuey, Robert
Gatten, and Kirk Millerfor theirhelpfulcomments
on the manuscriptand JeffreyBirchof the Statistical
ConsultingLaboratoryat VirginiaPolytechnicInstitute and State University (VPI & SU) and Philip
Dixon for advice on data analyses.We are grateful
to the following for informationor advice: Jeffrey
Graham, Virginia Hayssen, Hal Heatwole, Dennis
King, Howard Lawler,WilberMayhew,Lee Miller,
CharlesMyers,Alan Savitzky,LuciaSeveringhouse,
and RichardShine. The BiologyDepartmentof VPI
& SU supported F.H.P. during a sabbaticalleave.
The researchwas supported,in part,by a VPI & SU
small projectsgrantto R.M.A. and by Hatch funds
(projectno. 412) from CornellUniversityto F.H.P.
Physiol. Zool. 58(2):214-231. 1985.
1 1985 by The University of Chicago. All
rights reserved. 0031-935X/85/5802-8403$02.00

mass exponent, respectively. Kleiber (1961)

and Hemmingsen (1960) thought that the
mass exponent should equal .67, as predicted by the ratio of surface to volume
of geometrically similar figures. However,
interspecific comparisons for a wide variety
of taxa produced higher mass exponents.
Thus, Kleiber (1961) advocated the adoption of .75 as the true scaling factor of the
relationship between MR and M because
it provided the best fit for data that he
analyzed and because of its convenience
for taking logarithms with a slide rule.
Subsequently, theoretical arguments have
been advanced to support Kleiber's "rule."
A mass exponent of .75 can be derived
from principles of the mechanics of locomotion (McMahon 1973) and from the
geometry of four dimensions (Blum 1977).
Recently, the mass exponent of .67 has
reemerged as the predicted exponent for
comparisons of different-sized individuals
of a single species (Heusner 1982). Moreover, Feldman and McMahon (1983) argue
from their reanalysis of the data used by
Heusner (1982) that both .75 and .67 are

214

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

ALLOMETRY OF REPTILIAN METABOLISM

statistically valid mass exponents for the

relationship between MR and M; the former is appropriate for comparisons among
species and the latter for comparisons
within species.
Do .75 and .67 represent generally applicable scaling factors for the relationship
between metabolic rate and mass for comparisons among and within species, respectively? This question has been addressed for interspecific comparisons
among mammals (Hayssen and Lacy 1984)
and for selected families of mammals
(Kenagy and Vleck 1982; Hinds and
MacMillen 1984). These authors found
values of b that ranged from .55 to .69.
Moreover, Hayssen and Lacy (1984) found
significant variation in b among phylogenetic lineages of mammals. For mammals
at least, the use of the mass exponent of
.75 as a baseline for metabolic comparisons
among species appears to be invalid.
The only taxon for which the relationship between MR and M has been evaluated as a basis of comparisons within
species is mammals (Heusner 1982).
Whether these results are generalizable to
other taxa, or even to all mammals, is
unknown. Mammals are not a particularly
good group for intraspecific comparisons
because the range of body size of individuals after weaning is relatively low. Heusner (1982) circumvented this difficulty by
comparing domestic species that have been
selected for high variance in adult size.
The object of this paper is to review the
relationship between MR and M for the
squamate reptiles. We will address two
questions: (1) Are mass exponents of .75
and .67 appropriate as general models
describing the metabolism of squamates
for inter- and intraspecific comparisons,
respectively? (2) Can the variation in MR
of squamates be attributed to phylogenetic
or ecological differences among species?
We restrict our analyses to standard and
resting metabolism of the squamate reptiles
(lizards, snakes, tuataras, amphisbaenians),
which comprise over 90% of living reptiles.
Crocodilians and chelonians were excluded
because relatively few data exist for these
groups, particularly for intraspecific comparisons of metabolic rate. We focused on
standard and resting metabolism because
information about the intraspecific allom-

215

etry of MR and M during activity is

essentially nonexistent, and the information dealing with species comparisons of
activity metabolism has recently been reviewed by Bennett (1982).
MATERIAL AND METHODS

Bennett and Dawson's (1976) review of

the metabolism of reptiles was used as the
major source of data on MR and M for
papers published before 1976, and the
recent literature was searched for additional reports. Inclusion of data was based
on the following considerations:
1. Animals had to be fasted and inactive. We considered that a two- or threeday fast insured that small species were
postabsorptive but that a longer period
would be necessary for larger species
(Coulson and Hernandez 1980).
2. Metabolism had to be measured under standard or resting conditions. Reptiles
exhibit daily rhythms of metabolism that
may persist even under conditions of constant light or dark (Wood et al. 1978;
Heusner and Jameson 1981). We therefore
categorized metabolism as resting when it
was measured for fasting individuals during
the period of normal activity (daytime for
most squamates) and as standard when it
was measured for fasting individuals during
the period of normal inactivity (night for
most squamates).
3. Temperature had to be within the
range of normal activity. This range was
20-30 C for most species. Higher temperatures were included only for those species
with correspondingly high selected body
temperatures. For example, the upper limit
for Sceloporus was 35 C and for Dipsosau-

rus, Cnemidophorus,Acanthodactylus,and
Varanus40 C.

4. The period of acclimation to experimental temperatures varied considerably

among the studies cited. At the extremes,
acclimation periods ranged from several
hours to several weeks. Because daily fluctuation in temperature and light is necessary to elicit normal behavior (Regal 1980),
acclimation at a constant temperature for
periods of more than a few days is probably
not biologically realistic. Moreover, long
periods of acclimation at a high temperature are stressful (Marion 1982). Given
the variability in the literature, we consid-

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

216

R. M. ANDREWS AND F. H. POUGH

ered for our purposes that 2-3 h of acclimation was sufficient for small species but
that large species should have been acclimated for several days.
5. When more than one data set was
available per species, we selected the best
in terms of experimental rigor as judged
by sample size, specification of experimental conditions, etc. Thus, no species was
represented more than once at any one
temperature and metabolic state.
Unless specified, all statistical tests were
conducted with SAS software (Ray 1982).
INTERSPECIFIC ALLOMETRY

OF METABOLIC RATE

We included only measurements of metabolism of adults in our analysis of the

interspecific relationship between MR and
M. We used published values of mean
metabolic rate (ml 02 h-W STPD) and
mean mass (g) of individuals in each data
set. For reports in which metabolic rates
of adults were taken from ontogenetic
series, we used the metabolic rate associated with the largest individual. Although
mean adult mass would have been the
most consistent index of species size for
all our analyses, this datum was seldom
given in the cited studies. However, because species size in our analyses spanned
almost five loglo units, greater precision
in the index of adult mass for each species
would not have altered any of the reported
results.
Stepwise multiple regression (maximum
R2 improvement technique) was used to
evaluate the influence of temperature,
metabolic state (standard or resting), taxon
(snake or lizard-the sphenodontid and
the trogonophid being arbitrarily coded as
lizards), and mean adult mass (loglo MR
in ml 02 h-'). Log transformation of MR
and M linearizes the relationship between
these two variables for regression analysis.
Other variables used in the stepwise analysis were not transformed. This procedure
implies an exponential relationship between these independent variables and the
dependent variable. That relationship is
appropriate for temperature because it
provides a Qio of '-2 (Robinson, Peters,
and Zimmermann 1983).
For statistical comparisons among families and ecological groupings, standardized

residuals were used rather than the observed metabolic rates. Standardized (Student) residuals were calculated as being
(observed MR - expected MR)/Sy, where
the expected MR is the MR predicted by
the multiple regression equation and Sv is
the standard error of the expected MR at
a given log M. Because of the loglo transformation of observed metabolic rate, the
residuals are in loglo units. Comparisons
based on residuals reflect both the direction
(positive or negative) and magnitude of
deviations from the expected oxygen consumption and are independent of the absolute magnitude of observed values. In
order to reduce potential bias associated
with the differing numbers of observations
per species, the mean standardized residual
for each species was used in comparisons
of families or ecological groups. The residuals for all observations, for individual
families, and for ecological groups were
normally distributed (Kolmogorov D tests).
INTRASPECIFIC

ALLOMETRY

OF METABOLIC RATE

Analysis of covariance was used to evaluate the relationship between loglo MR

and loglo M for comparisons within species. Data sets for each species had to
include both juveniles and adults. Because
hatchling size is smaller relative to adult
size in large than in small species (Andrews
1982), we used as a guideline the rule that
our observations should include juveniles
as small as 10% and 30% of the mean
adult mass of large and small species,
respectively. Because of statistical and experimental problems associated with repeated-measures designs, we did not use
data sets that represented multiple measurements of the same individuals.
Data for most species were obtained by
projecting transparencies of published plots
of loglo MR versus loglo M on log-log
paper so that the values could be read
directly. The analysis of covariance was
based on only one set of observations per
species. When several data sets were available for the same species (e.g., for different
temperatures), the set in which the agreement between our calculation of a and b
and the published values was the greatest
was used in the analysis. For two species,
the original observations were used as they

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

ALLOMETRY OF REPTILIAN METABOLISM

were either presented in the publication

(Graham 1974) or obtained from the authors (Bakker and Andrews 1984).
RESULTS
INTERSPECIFICCOMPARISONS

A total of 226 observations of 107 species of squamates was used to evaluate the
relationship between metabolic rate and
the independent variables (table 1). Mass
entered at the first step of the stepwise
multiple regression analysis and accounted
for 88% of the variation in metabolic rate.
Temperature entered at the second step
and accounted for an additional 8% of the
variation in metabolic rate. Metabolic
state, although as significant as the preceding independent variables (P < .001), accounted for only an additional .6%. Taxon
type (lizard or snake) did not make a
significant contribution to the overall
model (P > .50). None of the interaction
terms in multiple regression models was
significant (P > .05). Therefore, the relationship among MR, adult mass, temperature (C), and state (0 = standard, 1
= resting) was expressed in terms of the
multiple regression equation
loglo MR = -1.87
+ .800 loglo M + .038 temperature
+ .140 metabolic state (1)
(F3,225= 1656.5, P < .001, R2 = .96).
After taking antilogarithms, this equation
becomes
MR

.013M.80 X

10.038 temperature
X 10.14 metabolic state.

(2)

The mass exponent (b) of the multiple

regression equation is .80 (SEb = .012).
This value is significantly different from
.75 (P<.001,
t-test; Sokal and Rohlf
[ 1981]). The Q o for the influence of temperature on metabolism is 2.4. This value
is typical of squamate Qio's over the temperature range of 20-40 C (Bennett and
Dawson 1976). The metabolism of squamates under resting conditions is 1.4 times
that of squamates under standard conditions.

217

PHYLOGENY AND ECOLOGY

Most families of squamate reptiles appeared in the late Mesozoic or early Cenozoic (Goin, Goin, and Zug 1978). These
families differ in morphology, ecology,
and behavior-do they differ also in metabolism? We compared metabolic rates
(as represented by the standardized residual) of 87 species in eight families that
were represented by five or more species
each (table 2). The variation among these
families was statistically significant (F7,86
= 2.4, P < .05 by one-way ANOVA). Of
the total variance, 16% was explained by
the model (variance among families).
However, a posteriori Tukey tests showed
that the family with the highest mean MR
(Varanidae) and the family with the lowest
mean MR (Boidae) were not statistically
different (P > .05). Varanids and lacertids
were different from boids at the .10 level,
but the remaining families were indistinguishable.
Many ecological and behavioral characteristics of squamate reptiles cut across
taxonomic divisions, and different specializations may be represented within a family. Are metabolic specializations associated with ecological and behavioral specializations?
We divided the lizards into four ecological categories: day-active predators, herbivores, reclusive predators, and fossorial
predators (fig. 1 and table 1). Differences
in metabolic rates among the four categories are highly significant (F3,63 = 17.5,
P < .001 by one-way ANOVA). Moreover,
45% of the total variability in the data set
is explained by the model (ecological category). Day-active predators have significantly higher metabolic rates than do reclusive predators, and the latter in turn
have significantly higher metabolic rates
than do fossorial predators. Herbivores fall
between day-active predators and reclusive
predators but cannot be distinguished statistically from either group.
INTRASPECIFICCOMPARISONS

We found published accounts of the

relationship between MR and M for ontogenetic series of 17 species (table 3).
Because data sets at different temperatures
and at the two metabolic states were avail-

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

(1963)"
(1963)"

(1966)"
(1966)"
(1981)
(1981)
(1979)
(1979)
(1976)
(1976)
(1976)
(1982)
(1982)
data
data
data
(1983) (1983)
Tucker
Tucker
(1981)
(1981)
1974)"
1974)"
1974)"
and
and
Bramham
Bramham
Templeton
Murphy
MurphyGorman
Templeton
Weathers
Weathers
Weathers
Gatten Gatten Feder Gorman
Feder
unpublished
unpublished
unpublished
and
and
and
and
and
and
and and
(1971,
(1971,
(1971,
and
and
(1979)
(1979)
(1975)
and (1984)
and and
and
and

Source

Snyder
Dunson
Bennett
Snyder
Snyder
Snyder
Dunson
Bartholomew
Bartholomew
R.M.A.,
R.M.A.,
Putnam
Feder
Feder
Snyder
Snyder
Wilson
Dawson
Kamel
Fusari
Kamel
Putnam
R.M.A.,
Bennett
Wilson
Wilson
Dawson

.249
.780
.576
.679
.406
.205
.061
.123
.187
1.185
-.589
-.431
-.098
-.375
-.492
-.770 -.777
-.726-.082
-.250
-.401
-1.249
-1.483
-1.709
-2.157 -1.115
-1.749
Residual
Standardized
h-')
02
Rate
Metabolic
(ml

.69.771.65 1.26 .34.32 .70.35.535.93

.20.30.21.26.69.92.06.09.05.13.03
4.93
16.41
16.63
36.55
70.56
40.32

SPECIES

SQUAMATE

Mass
(g)

373373
504504504

3.53.6 1.81.82.04.44.44.4.4 .4 .5 .5 .3
11.2
11.7
292932.2 4.54.9 9.5
61.5

20 30203037

303020 3025

2025

252725302734 27 202630 2530273027

RRRRR

S RRRS

RS

S S S RS RS RRRRRS RS

4 4 4 4 4

1 1

1 1

2 2 2 2 2 2 2 2 2 2 2 2 2 2 2

VARIOUSBody
IN

TABLE

(C)

Temperature

CONSUMPTION

State
Metabolic

OXYGEN

1
NDND

Category
Ecological

beattyi
frenatus
multicarinatus
platyurus
ventralis
antillensis
Species
switaki
variegatus
pulchra
fragilis
gecko
multicarinatus
antillensis
frenatus
barbatus
frenatus
frenatus
beattyi
lesueurii
pulchra
cinereus
macrolepis
lesueurii
notatus
fragilis
G.Ophisaurus
Cosymbotus
G.Hemidactylus
H.H.H.Sphaerodactylus
Coleonyx
Gekko
Gonotodes
S. S. S. S.
Anniella
A.Gerrhonotus
A. Anarbylus
P. P. Anguis
Amphibolurus
A.Physignathus
Anniellidae:
Gekkonidae:
Agamidae: Anguidae:
Sauria:
barbatus
lesueurii

218

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

(1975)
(1963).
(1963)a
(1963)"
(1959)"
(1959)i
(1979)
(1979)
(1972)
(1972)
(1972)
(1973)
(1972)
(1973)
(1977)
(1977)

Hughes
(1981)
and

(1971)
(1971)
(1971)
(1971)

Nellis
Nellis
Asato
Asato
(1982)
(1975)
(1975)
Jameson
Templeton
Templeton
Templeton
Dawson
Dawson
Dawson
Dawson
Gorman
Gorman
Levendahl
Whitford
Whitford
Whitford
Whitford
and
and Levendahl
al.
al.
al.
and
and
(1963).
(1963)"
(1963).
(1960)"
(1960)"
(1965)a
(1965).
(1965)a
and
(1960)a
and
and
and
Fitzpatrick,
(1969)'
and
and
and
and
and
(1972)'
(1972)'
(1972)' (1969)'
(1969)'
and
et et et
and
and
and
and
and
and
(1967)a
(1967)a
Maher
Dawson
Mueller
McManus
Bennett
Maher
Dawson
Dawson
Bennett
Bennett
Bennett
Moberly
Moberly
Moberly
Moberly
Moberly
Boyer
Boyer
Mueller
Mueller
Heusner
Dutton
Dutton
Hughes
Bennett
Moberly
Prieto
Bennett
Bennett
Dutton,
McManus
Bennett
Andrews
Andrews
Prieto
Prieto
Mayhew
Mayhew
Prieto
Mayhew
Bennett

.327
.867
.306
.000
.054
.845
.928
.475
.045
.930
.406
.482
.455 .802 .349
.370
.398 .149
.022
1.023
1.605
1.119
1.076
1.763
-.933
-.531
-.781
-.699
-.693-.527
-.505
-.679
-.488
-.010
-.244
-.774
-.756
-.426-.473
-1.330
-1.118

.821.25
.781.70
.49.85.12.342.40
.44.82 1.08
.16
1.68
1.12
1.58
5.40
8.40
5.25
5.81
3.94
2.45
3.39
3.24
3.51
6.30
2.04
6.63
2.72
4.59
4.35
4.78
4.40
10.33
10.80 1.75
31.80
64.39
50.51
29.85
119.25

5.05.05.010.0
4.34.312.0
4.54.51.51.430 30 30 35 35 35 35 515151
4.1
12.0
16.0
16.0
16.0
13.0
24.0
21.0
79579579535352828
574574574150150

2530273320 30 20 30 20 30 37 25 30 35402030372030 372535253520 30 37 20 30372030253037 25 20 25 30 20

RRS RRRS RRRRS S S S RRRRR RRRRRRRRS S S RRRRRS RRRS

4 4 4 4 4 4 4 4 4 4 4 3 3 3 3 3 3 3 3 3 3 4 4 4 4 4 4 4 3 3 3 3 3 4 4 4 4 4 4 4 4

cornutum

collarisdorsalis
acutus

hispidus

graciosus

iguana

dorsalis
dorsalis
dorsalis
dorsalis
dorsalis
dorsalis
bonairensis
collaris
acutus
bonairensis
collaris
carolinensis
carolinensis
limifrons
limifrons
m'calli
undulatus
m'calli
m'calli
cornutum
douglassi
douglassi
olivaceus
occidentalis
olivaceus
olivaceus
hispidus
hispidus
obesus
obesus
graciosus
graciosus
iguana
iguana
C. C. Dipsosaurus
S. S. S. S. Sceloporus
A.A. A. A. A. A. A.Crotaphytus
D. D. D. D.D. D. Iguana
I. I. Phrynosoma
P. P. P. P. P. P. Sauromalus
S. S. S. S. S. S. S.
Anolis
Iguanidae:
219

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

(1974)
(1974)
(1974)
(1974)

(1968),
(1968),
(1968),

(1974)
(1974)
(1974)
(1974)
(1974)
(1974)
(1974)
(1974)
(1974)
(1974)
(1974)
(1974)

(1978)
(1978)
(1978)
(1978)
Borut
Borut
Borut
Borut
Borut
Borut
Borut
Borut
Borut
Borut
Borut
Borut
Borut
Borut
Borut
Borut

Source

(1982)
(1982)
(1982)
(1982)
(1982)
(1982)
(1982)
Vance
Vance
Vance
and
and
and
and
and
and
and
and
and
and
and
and
Busak
and
and
and
Busak
Busak
Busak
and
al.al.al. al.al.al.al.
(1934)8
and
and
(1968)'
(1968)'
(1968)'
et et et et et et et and
and
and
and
and
Kramer
Duvdevani
Duvdevani
Duvdevani
Duvdevani
Duvdevani
Duvdevani
Duvdevani
Duvdevani
Duvdevani
Duvdevani
Duvdevani
Duvdevani
Pough
Pough
Pough
Pough
Duvdevani
Duvdevani
Duvdevani
Roberts
Roberts
Duvdevani
Murrish
Murrish
Hughes
Roberts
Hughes
Hughes
Hughes
Hughes
Murrish
Hughes
Hughes

.015
.216
.199
.721
.987
.593
.032 .894
.999 2.512
.319
.340
.218 2.034
.606
1.616
1.520
1.918
1.655
3.199
1.273
1.576.301
1.668
2.333
2.466
2.000
-.824
-.041
-.8192.207
-.297
-.807
-1.244
Residual
Standardized
h-')

.49
.21.51.90 1.87
.24.932.01
.552.38
.391.07
1.25
1.06
1.63
1.62
3.04
1.95
1.17
2.38
3.88
3.05
3.49
2.18
2.72
3.15
6.79
1.42
4.56
2.25
2.03
2.34
3.50
2.21
02
Rate
Metabolic
(ml

SPECIES

SQUAMATE

Mass
(g)

6.66.66.66.69.0
3.03.03.0 7.87.87.87.89.09.09.09.09.79.79.79.710.9
3.34.04.04.13.34.04.014.0
10.9
10.9
10.9
14.0
14.0

Body
VARIOUS
(Continued)
1 IN
TABLE

(C)

25 30 35 20 253035203037203037

2530 35 40 20 25 30 35 25 30 35 40253035402530 354020

Temperature

CONSUMPTION

S S S RRRRRRRS S S
Metabolic

RRRRS S S S RRRRRRRRRRRRS

4 4 4 4 4 4 4 4 4 4 4 4 4
Category
Ecological

4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4

OXYGEN State

bosianus
Species
mearnsi
stansburiana
stansburiana
stansburiana
sicula
mearnsi
mearnsi
schreiberi
scutellatus
scutellatus
scutellatus
scutellatus
erythrurus
erythrurus
erythrurus
schreiberi
schreiberi
schreiberi
bosianus
erythrurus
bosianus
pardalis
pardalis
pardalis
pardalis
bosianus
undulatus
undulatus
undulatus
undulatus
undulatus
undulatus
undulatus
U. U. U.U. U. Acanthodactylus
A. A. A. A. A. A. A. A. A. A. A. A.A. A. A. A.A. A. A.L.
S. S. S. S. S. S. S. Uta
Lacertidae:

220

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

(1976)
(1979)
(1966)8
(1979)
(1966)8
data
data
(1965)8
(1965)8
Bligh
al.al.
1974)8
1974)8
1974)a
1974)a
and
1974)a
(1966)a
et et
Bertram
Bertram
Gorman
Gorman
(1978)
(1978)
Andrews
Andrews
al.
al.al.
(1970)8
(1970)8
(1970)8
unpublished
unpublished
unpublished
(1970)8
(1970)8
(1970)8
et
and
and
(1934),
(1981)
(1934)a
(1935)'
(1981)
and
and
(1981)
(1981)
(1971,
(1971,
(1971,
(1971,
(1965)'
and (1971,
Young, et et
(1978) (1978)
(1978) and
(1982)
(1982)
(1984)
(1984)

data

Maher
R.M.A.,
Dawson
Dawson
Withers
R.M.A.,
Bennett
Withers
Bakker
Pough
Dawson
Wilson
Wilson
Dawson
Withers
Hudson
Hudson
Bartholomew
Bartholomew
Wilson
Bennett
Asplund
Louw,
Earll
Earll
Wood
Cragg
Kramer
Kramer
Kramer
Cragg
Cragg
Withers
R.M.A.,
Wilson
Wilson
Asplund
Asplund
Wood

.163
.275 1.024.194
-.938 -.952

.081
.837 .696
.459
.500 .522
.094 .036 1.527
.885
.905
.471 .354
-.944
-.560
-.078 -.169
-.200
-.948 -1.155
-.348-.108-.014-.033
-.863-.073 1.128
-.016
-.317
-1.624
-1.669
-1.325
-2.293

.18.25.12.31.59.68
.84 .60 .41.681.70 .20
.981.63
1.68
1.47
1.50
1.12
5.10
6.70
2.20
2.35 8.87
2.52
4.86 92.88
13.31
13.83
10.20
15.55
22.71
44.37
42.41
64.544.93
150.00
149.26
175.44
322.50

71 5431 20

7.37.325.0
7 9.6303030 1.11.11.01.07.47.4
2.8
18.0
18.0
18.0
25.0
261261
9633440
493493461461461 85 85
3440
7500
7500

30 20 3020 30 30

23 3330 33 20 20 30 30 302030 3723332030303020 3020 30 37

27 40 203037

35203025 35

S S S S S S

RRS R RR RR RRRRRRRRS RRRRRR

S RRRR

RS S S S

4 4 4 4 4 4

1 1 1 1 4
I 1 4 4 1 1
4 4 4 4 4
NDND4 4 4 4 4
NDNDNDNDND

4 4 4 4 4

rugosus murinus
ocellatus
labillardieri
meleagris
fasciatus
cunninghami

sepsoides
lateralis
gronovii
scincoides

albigularis

rugosusmurinus
tigris
tigris bengalensis
rugosus
tigris
bengalensis
exanthematicus
exanthematicus
vivipara
scincoides
viridis
viridis
ocellatus
obsoletus
trilineata
trilineata
inexpectatus
obsoletus
sicula
meleagris
cunninghami
obsoletus
sepsoides
lateralis
gronovii
V.V. V. V
T. T. Cnemidophorus
T. Trachydosaurus
C. C. C. C. Varanus
S. Tiliqua
C. Ctenotus
S. Sphenops
L. L. L. L. L. L. Acontias
S. Scincella
E. Eumeces
Egernia
E. E. E. E. Scelotes
A.Chalcides
Teiidae:
Varanidae:
Scincidae:
221

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

(1974)"
Tucker
Source

and
(1972)a
(1972)a(1979)
(1972)a
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
(1979)
Mautz
Mautz
Mautz
Mautz
Mautz
Mautz
Mautz
Mautz
Mautz
Mautz
Mautz
Bennett
Bartholomew
Mautz
Mautz
Mautz
Mautz
Mautz
Mautz
Mautz
Mautz
Mautz
Mautz
Mautz
Bennett
Bennett
Mautz
Mautz
Mautz
Mautz
Mautz
Mautz

.111
.009
.436
.310
.154 .012
.226 .249
.059
.352
.453
1.104
-.077
-.660 -.396
-.324
-.456
-.356
-.631
-.703
-.792-.280
-.688
-.073-.498
-.757
-.448
-1.434
-1.702
-1.366
-1.265
-1.539
Residual
Standardized

SPECIES

.681.10
.30.39.65.42.49.69.621.32
.771.25
.661.33
.25.37.52.31.44.54.17.26.20.31
1.54
1.99
1.87
1.75
16.18
51.90
74.81
220.50

h-')
02
Rate

Metabolic
(ml
SQUAMATE

Mass
(g)

6746746744410

5.05.05.05.05.05.0
3.53.53.53.53.53.51.51.51.51.5
19.0
19.0
19.0
19.0
19.0
19.0
25.0
25.0
25.0
25.0
25.0
25.0

Body
VARIOUS
(Continued)
1 IN
TABLE

(C)

20 30 3730

2025302025302025 30 20 25 30 20 25 302025 30202530202530 253025 30

Temperature

CONSUMPTION

S S S R

S S S RRRS S S RRRS S S RRRS S S RRRS S R R

OXYGEN State

Metabolic
4 4 4 4

2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2

Category
Ecological

gaigeae
Species

riversiana

henshawi

vigilis
riversiana
vigilis
vigilis
riversiana
henshawi
henshawi
vigilis
varius riversiana
riversiana
riversiana
henshawi
henshawi
henshawi
smithi
smithi
smithi
smithi
smithi
smithi
gaigeae
gouldi
gouldi
gouldi
gaigeae
gaigeae
gaigeae
gaigeae
V. V. V. V. Klauberina
L. L. L. L. L. L. L. L. L. L. L. Xantusia
K.K.K.K.K.Lepidophyma
X. X. X.X. X. X. X. X. X.
Xantusiidae:

222

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

(1970)8
(1970)a

(1969)a
(1969)8

(1971)a
(1971)'

(1983)
(1972)8
(1980)
(1980)
(1980)
(1980)
(1980)
(1980)
(1966)8
Whitford
Whitford
Whitford
(1970)8
Armitage
Armitage
(1965)8
(1965)a
(1965)8 Whitford
(1965)8
al. (1965)8
(1965)8
(1965)8 (1965)8
(1965)a
(1965)8
(1965)8
(1965)8
(1965)8
Borut
Gatten
(1971)8
(1971)a
al.
et
al.
al.
al.
al.
al.al.al.
al.al.al.and
al.
al.
al.
and
and
and
and
and
Mendes
Mendes
Mendes
Mendes
Mendes
Mendes
(1928)'
(1936)a
(1936)8
et
et et et and
et and
et et et
et et
et
et et et (1976)
(1976) (1982)
and
and
and
and and
and (1911)a
Dmi'el
Galvao
Kamel
Clausen
Clausen
Jacobson
Hill
Baldwin
GalvTo
Galvio
Galvio
Ruben
Hutchison
Buikema
Smith
Davies
Abe
Jacobson
Galvio
Galvio
Vinegar
Galv~o
Galvio
Galvao
Buikema
Abe
Abe
Abe
Abe
Abe
Galvio
Galvio
Jacobson
Galvao
Greenwald
Greenwald
Galv~o
Jacobson

.573
.984
.146 .020 1.076
.261 1.430.074
1.401
1.1861.398
1.354
3.445
-.104
-.312
-.015
-.007
-.793
-.958
-.100-.6061.865
-.512
-.945
-.122
-.152
-.946
-.572
-1.210
-1.943 -.346 -.105
-2,204
-2.041 -.834
-1.145
-1.261
-1.157

.631.17 6.95
.81.28.58 6.86
1.24
1.21
1.68 7.56
3.43
6.86
2.07
4.72
19.24
10.41
19.79
13.63
14.28
10.78
31.2831.60
30.407.84
38.56
85.76
34.08
47.74 2.99
21.98
22.61
23.02
44.95
23.73
166.40
216.00
222.66

5.04.4
19
84 238985486225481763881353517.27.265 65 11.0
61.0
22.0
314
8001961961961217
40140140142735 238
1130
2680
2997
1440025600
12370

20202032 20 30

2020202030 252025302620 2530 20 20202030 2020203020 20 20 30 20 30 20 30 20 25

RRRS RR

RRRRRRRRRRRRRRRRRRRRRRRRRRRRRRRS

NDNDNDNDNDND NDNDNDNDNDNDNDNDNDNDNDNDNDNDNDNDNDNDNDNDNDNDNDNDNDNDNDNDNDNDNDND

getulus

mikanii
cliffordii
bifossatus
poecilogyrus
butleri
trigeminus
olfersii
serra
patagoniensis
hexalepis
melanoleucus
rhombifera
dekayi
natrix

roseofuscagigas
punctatus
quadricarinatus
murinus
modestus
molurus
guttata
albifrons
constrictor
modestus
modestus
rhombifera
notaeusmolurus
miliaris
miliaris
punctatus
miliaris
melanoleucus
melanoleucus dekayi
hexalepis
Thamnophis
Pituophis
Sphalerosophis
Philodryas
Philodryas
Storeria
P. P. Philodryas
S. Sibynomorphis
Chironius
Natrix
Nerodia
N.Oxyrhopus
S. Salvadora
E. Lichanura
L. L. L. Leimadophis
Masticodryas
Eunectes
Python
Dipsas
Diadophis
D.Elaphe
Helicops
H.H.Lampropeltis
P. Cyclagras
Boa
Boidae:
Colubridae:
Ophidia:
223

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

(1979)

(1971)8
(1971)a
Source

(1983)

(1981)
(1970)
(1970)
Lykkeboe
Whitford
Whitford (1965)8
(1965)a
(1965)8
(1965)a
Lee
Lee
Davies
al.al.al.al.
and
and
and
(1971)a
(1971)a
(1974)
and
and
(1976)
andet et et et

Gatten
and

Wilson Kamel
Aleksiuk
Ruben
Jacobson
Aleksiuk
Taylor
Galvio
Galvio
Galvio
Graham
JohansenWilson
Galvio
Jacobson

.581
.876
.872
.388
1.414
-.862-.687-.471-.371
-.401
-.658
-2.349
Residual
Standardized

-1.181
-1.202

h-')
SPECIES

1.75
1.52
1.75 1.96 6.96 5.67
4.65
6.60
2.25
02 2.32
21.59
24.08
Rate
Metabolic
(ml

9.46
13.33

-2.156active.

.19

and

article.

SQUAMATE

Mass
(g)

31312538200555050253

116 30163

5.0
430430

Body
VARIOUS
(Continued)
1 IN
TABLE

(C)

day
=
4

herbivore;
= present
3 the

of

20302020 2920202020

30

3525

21 25

25

reclusive;
= section
2

Cited

Temperature

CONSUMPTION

RRRRRRRRR
Metabolic

OXYGENState

S S

NDNDNDNDNDNDNDNDND ND NDND
Category
Ecological

RR

NDND

fossorial;
=
1 Literature

in

included
determined;
notnot
= and
ND

(1976)
standard;
= Dawson
S

strigatus
Species

guentheriplaturus
viridis
berus

punctatum

and
wiegmanni

resting;
= Bennett

in
neuwiedii
sirtalis merremii
sirtalis
sirtalis
proximus
proximus
punctatum
Vipera Sphenodon
Trogonophis
T. T. T. T. T. Thamnodynastes
Crotalus
S.
X. X. Pelamis
Xenodon
Given
Viperidae: Sphenodontidae:
Hydrophiidae:
Trogonophidae:
NOTE.-R
a
Sphenodontia:
Amphisbaenia:

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

225

ALLOMETRY OF REPTILIAN METABOLISM

TABLE 2

FAMILIES
REPRESENTED
RESIDUALS
FORSQUAMATE
AND MEANSTANDARDIZED
MEANRESIDUALS
ANDFORECOLOGICAL
OF LIZARDS
CATEGORIES
BY FIVEOR MORESPECIES
STANDARDIZED
RESIDUAL

RESIDUAL
CLASSIFICATION

Family:
Varanidae.......

NUMBEROF
SPECIES

.096

10

.096

........
Iguanidae
Colubridae......
Scincidae........
Xantusiidae
......
Gekkonidae
......
Boidae..........

18
29
12
5
10
5

.035
.030
-.049
-.074
-.076
-.121

category:
Ecological
Day-active.......
Herbivores
.......
Reclusive........
Fossorial........

38
6
15
8

.065
-.020
-.076
-.216

Lacertidae.......

(SE)

(SE, CV)

.583

(.045)

(.271, 104)

.577

(.044)

(.025)
(.036)
(.039)
(.037)
(.039)
(.060)

.210
.180
-.295
-.445
-.461
-.737

(.018)
(.034)
(.028)
(.041)

.389
-.121
-.456
-1.295

(.271, 148)

(.152,308)
(.213,636)
(.236,277)
(.222, 111)
(.237, 163)
(.366, 111)
(.107, 169)
(.207,418) J
(.170, 144) J
(.245,54)

(P > .05 by Tukey tests)are connectedby brackets.

NOTE.-Meansthat do not differsignificantly
of variation.
SE = standard
error;CV = coefficient
able for some species, the number of data
sets totaled 28. Overall, the mean value
of b, the mass exponent, was .67, identical
with the predicted value for intraspecific
comparisons. However, values of b ranged
from .51 to .80. Analysis of covariance
was used to determine whether these values
could be considered homogeneous. Three
species listed in table 3 were not included
in the analysis. For two species (Sceloporus

DISCUSSION
COMPARISONS
INTERSPECIFIC
GENERAL

Metabolic rate is typically expressed only

as a function of mass. Because metabolism
is simultaneously affected by other variables, univariate analyses limit comparisons among taxa to studies conducted
under the same conditions. Our approach

graciosus and Elaphe guttata) the observations of MR and M were not reported,
and for the third species (Liophis miliaris)
we could not replicate the author's estimates of a or b. For the remaining species,
our derived estimates of a and b were
within 5% of the published values.
We first tested the null hypothesis that
the slopes (b) of the regressions of loglo M
did not differ from one another. This
hypothesis was rejected because there was
a significant interaction between species
(the class variable) and log10 M (the covariate) (F13,318 = 2.0, P = .021). Consequently, further comparisons of MR
among species are invalid. Therefore, a
posteriori tests were used to compare values of b among species. Because the largest
and the smallest are not significantly different (P > .05 by Tukey test; Zar [1984]),
no further tests were conducted.

~a

Iv
e
<Do
-act
oo . . .
o ..... 2 oA

.au 1,t,

0.0

o
s

,a

cca

0 0

Fo
........
0 a"
-2.0
....
.t.0

-o0e

2:4

0o0

3:2

4.0

LOG1oMASS (G)

FIG. 1.-Metabolic rates of lizards in four ecological

categories as a function of body mass. Each species
is represented by the mean standardized residual of
the relationship between metabolic rate and three
independent variables (mass, temperature, and standard or resting metabolic state). See Material and
Methods for details. The ecological categories are
day-active predators (A), herbivores (A), reclusive
predators (0), and fossorial predators (0). Means for
each category are indicated by arrows on the vertical
axis.

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

(1981)
(1984)
(1984)

(1979)
(1979)
(1979)
(1979)
(1979)
(1966) (1979)

(1980)
(1980)
(1980)
(1980)
(1980) (1972)
(1980)

(1981)
(1981)
Jameson
Bertram
Gorman
Gorman
Gorman
Gorman
Gorman
Gorman
(1978)
(1978)
Borut Andrews
Andrews
Source
Feder
Feder
al.
al.
Mendes
Mendes
Mendes
Mendes
Mendes
Mendes
and
(1974)
and
(1969)
andand
and
(1969)
and
and
and
(1969)
and
and
(1982)
and (1978)
et et
(1976)
and
and
SPECIES
and
and
and
and
and
and
Hudson
Bennett
Mueller
Mueller
Feder
Feder
Bennett
Bennett
Bennett
Bennett
Bennett
Bakker
Heusner
Mueller
Davies
Dmi'el
Smith
Pough
Cragg
Wood
Wood
Abe
Abe
Graham
Abe
Abe
Abe
Abe
SQUAMATE

VARIOUS
(C)
IN

2025 30 20253030263025

3033253025 35 2530 35 30 27 27 27 332740 2734

Temperature
MASS
BODY
AND

RRRRRRS RRR
State
Metabolic

S RS S S S RRRRS S S RS R S R

RATE

METABOLIC
OF

Mass
(g)a
TABLE Body

5 5 5 1.52 3.512 128585 1.81.8

4
196196196401401401116 500800 252520
1,217
7,500
7,500

REGRESSIONS

.548
.761
.705
.695
.682
.785
.633
.685
.744
.554
.753
.67.78.57.51.694
.585
.674
.729
.650
.62.70 .647
.626
.585
.560
.753
.802
Mass
Exponent
INTRASPECIFIC

Methods).

FOR

and
1.
.128
.201
.430
.168
.249
.139
.127
.208
.17
.145
.680
.199
.317
.150
.23 .883.39 .394
.306
.411
.198
.333
.488
.338
.257
1.2c
1.21 .313
Mass
table
Coefficient
EXPONENTS
in Material
study.
(see
AND
given
each
in
.
.
those values.
.
.
.
are covariance
.
of figured
COEFFICIENTS
.
observed
.
murinus
MASS
from
cliffordiib
frenatush
getulusb
analysis
platyurusb
occidentalisb
antillensis
graciosus
Species
ocellatusbexanthematicush
an
lateralisb
individual
modestus
viviparab
miliarisplaturusb
guttata
in
bonairensis
modestusb
modestus
antillensisb
murinusb
ocellatus exanthematicus
miliaris
miliaris
graciosus
graciosus bonairensisb
Used
Recalculated
Largest
V.Sceloporus
Varanus
Cosymbotus
C. Gonotodes
G. NOTE.-Abbreviations
Chalcides
C. Sceloporus
a b C
Lacerta
S. S. Scincella
Hemidactylus
A.Cnemidophorus
Elaphe
Anolis
Spalerosophis
Lampropeltis
Helicops
H.H.Liophis
L. L. Pelamis
Sauria:
Ophidia:

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

227

ALLOMETRY OF REPTILIAN METABOLISM

has been to use multivariate statistics as a

means to express metabolism as a function
of the three independent variables that are
most important in studies of squamate
reptiles. Thus, equation (2) expresses the
relationship between MR and M over a
temperature range of 20-40 C and for
individuals under either standard or resting
conditions.
Our predictions of metabolism based
on multivariate analysis agree closely with
the results of univariate analyses (Bennett
and Dawson 1976). For example, with the
appropriate substitutions for temperature
and metabolic state, our equation (2) reduces to MR = .103 M.80 (resting, 20 C)
and MR = .248 M.80 (resting, 30 C).
For reptiles in general (mostly squamates), Bennett and Dawson (1976) expressed the relationships as MR = .102
M.80 (resting, 20 C) and MR = .278 M"77
(resting, 30 C).
In our analyses, metabolic rate scales to
mass by a power of .80. The metabolism
of free-living iguanid lizards also scales to
mass to the .80 power (Nagy 1982). These
results are not in accord with theoretical
predictions (McMahon 1973; Feldman and
McMahon 1983) of a .75 scaling factor.
Thus, metabolic rates of squamates increase faster with mass than expected, and
they also increase faster with mass than
has been observed for a class-wide analysis
of the metabolic rates of mammals (Hayssen and Lacy 1984).
Equation (2) provides a flexible estimator of the metabolic rates of squamate
reptiles that is useful either for comparisons
of the vertebrate classes (e.g., Pough 1980)
or for other general uses in which the
magnitude of the intergroup difference
greatly exceeds the magnitude of the variation within groups. Equation (2) is not
suitable for comparisons among squamates, however, because significant variation exists among taxonomic and ecological groupings.
INTERSPECIFIC COMPARISONS:

PHYLOGENY

AND ECOLOGY

Metabolic rates of squamate reptiles

vary as a function of both phylogenetic
relationship and ecology. Considerably
more variation in metabolism was explained by ecological groupings (45%) than
by family (16%). That relationship suggests

that some families are ecologically diverse

and that this diversity is associated with
intrafamilial variation in metabolic rates.
Families that are ecologically homogeneous have low intrafamily metabolic
variation. This point is illustrated in table
2 by the contrast of the coefficients of
variation for the standardized residuals of
ecologically diverse families (colubrids,
scincids, and iguanids) and those of ecologically homogeneous families (varanids,
xantusiids, gekkonids, and boids). (Our
characterization of families as ecologically
diverse or homogeneous in this context is
based on the species represented in our
sample, which do not necessarily reflect
the characteristicsof the family as a whole.)
Sorting skinks and iguanids by ecological
characteristics reduces the variance, apparently by producing more homogeneous
groups. It thus appears that ecology is
more important than phylogeny in determining levels of resting and standard metabolism among squamate reptiles.
INTRASPECIFIC

COMPARISONS

The theoretical prediction that the relationship between MR and M for comparisons within species should differ from
comparisons among species was supported
only in a very general sense, but not in
specific details of the prediction. Heusner
(1982) proposed that mass exponents for
comparisons within species should be
lower than the mass exponent for comparisons among species. He further suggested that the relatively high mass exponent for comparisons among species was
an artifact of inappropriately fitting a
regression line through independent sets
of data with common slopes but different
intercepts.
Heusner's contention that the mass exponents for comparisons within species
should be less than the mass exponents
for comparisons among species is correct
for squamate reptiles. All but three of the
28 mass exponents for intraspecific data
sets (table 3) are significantly smaller than
.80, the mass exponent for comparisons
among species (P < .05 by t-tests; Sokal
and Rohlf [1981]). Moreover, if a common
multiple regression line is fitted to all of
the intraspecific data (disregarding species
identity), the resulting equation is

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

228

R. M. ANDREWS AND F. H. POUGH

MR = .036 M.82 X

10.024 temperature

x 10.094metabolicstate (3)

(F3,345= 2877.7, P < .001, r2 = .96).

As Heusner predicted, the mass exponent
of this equation is very similar to that
based on comparisons among species
(eq. [2]).
In contrast, Heusner's prediction that
the mass exponent for comparisons within
species should be .67 was not supported
by our analysis. Indeed, variation in mass
exponents among species is so great that
no common mass exponent can be assumed. For that reason, it is not possible
to test Heusner's prediction that mass
coefficients (a) should increase with species
size (i.e., that the adjusted means in an
analysis of covariance should increase with
species size).
WHY DO METABOLIC RATES DURING
INACTIVITY

VARY?

The existence of significant variation in

metabolic rates during inactivity among
ecological groupings of squamates is perplexing. Squamate reptiles are typically
inactive for a major portion of each day
(Andrews 1971, 1984; Bennett and Nagy
1977; Anderson and Karasov 1981; Huey
1982). Consequently, the energy requirements of individuals while they are inactive
may comprise a substantial fraction of
their total energy requirements. It would
thus appear advantageous for all individuals, irrespective of foraging mode or diet,
to be energy conservative while inactive.
This is clearly not the case, and that
paradox suggests that metabolism during
inactivity is related to broader aspects of
physiology or ecology.
Rates of standard and resting metabolism may be indirectly linked to other
features of metabolism. For example, Taigen (1983) noted a positive correlation
between rates of metabolism at rest and
during forced locomotion for 17 species
of anurans and suggested that the physiological characteristics that permit high rates
of oxygen consumption during activity are
associated with an obligatory increase in
resting metabolism. Although rates of metabolism during activity may be correlated
with rates during inactivity for some squamates (like the active and sedentary

searchers discussed in the next section),

that relationship is apparently not obligatory. For example, several species of Varanus do conform to the predicted pattern;
they have high metabolic rates during
exercise, high aerobic scopes, and high
resting metabolic rates (Bennett 1982). In
contrast, the legless lizard Ophisaurus ventralis also has a high metabolic rate during
exercise and a high aerobic scope, but this
lizard has a low resting rate of metabolism
(Kamel and Gatten 1983). Cnemidophorus
are active foragers and sustain high metabolic rates during activity (Bennett and
Gleeson 1979), but they have low resting
metabolic rates (table 1).
McNab (1980) has suggested that basal
metabolic rates in mammals are in some
manner causally associated with reproductive potentials (rmax).He proposed that
species with a high rmax are characterized
by high rates of basal metabolism and
high rates of energy flow. This hypothesis
was not supported by statistical analysis
of data for mammals (Hayssen 1984).
McNab's hypothesis cannot be tested for
squamates with the data currently available, but the observation that xantusiids
have both low reproductive potentials and
low metabolic rates compared to dayactive lizard predators (Tinker, Wilbur,
and Tilley 1970; Mautz and Case 1974;
Mautz 1979) is consistent with the hypothesis. However, Hayssen (1984) further
argued that there is no basis for an obligate
relationship between resting and reproductive metabolism of the sort that underlies McNab's reasoning.
ECOLOGICAL CONSEQUENCES

OF VARIATION

IN METABOLIC RATE

Energy flow through populations of

squamates should vary considerably, in
part as a function of ecological specializations and the associated metabolic differences. First, species differ in their metabolic
rates during inactivity. For example, dayactive lizard predators have mean metabolic rates two times those of fossorial
lizards (table 2). Because metabolism during inactivity is a substantial fraction of
total energy requirements, day-active lizards will, in general, have greater energy
requirements than will fossorial lizards of
the same size. Second, differences in longterm energy budgets among species with

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

ALLOMETRY OF REPTILIAN METABOLISM

different ecological specializations may be

increased by a possible association between
foraging mode and metabolic rates during
inactivity. Taxa such as xantusiids (Mautz
and Case 1974), boids (Montgomery and
Rand 1978), and sphenodontids (Wilson
and Lee 1970), which restrict their daily
activity to small areas, have low metabolic
rates during inactivity, whereas taxa such
as varanids (Bennett 1982) and lacertids
(Nagy, Huey, and Bennett 1984), which
move more extensively, have high metabolic rates during inactivity. Moreover,
lizards that are sit-and-wait predators have
lower metabolic rates during inactivity
than do lizards that are widely foraging
predators, but the difference is not statistically significant (P > .05 by Tukey test;
data from table 1).
PREDICTING
METABOLIC
RATESOF SQUAMATES

The limited data available to Bennett

and Dawson (1976) indicated that comparisons within and among species had
the same mass exponent. Thus, the metabolism of juvenile squamates is commonly estimated from general equations
that relate MR to M for interspecific comparisons of adults (e.g., Andrews 1979;
Porter and James 1979; Thompson 1981;
Troyer 1984). Our analysis shows that this
procedure is invalid, because most mass
exponents for comparisons of ontogenetic
changes in metabolism within species are
significantly lower than the value of .80
that applies to interspecific comparisons
of adults. Unfortunately, the heterogeneity
of mass exponents for intraspecific relationships of MR and M means that there
is no easy alternative method of estimating
the metabolism of juvenile squamates. An
accurate description of energy requirements of juvenile squamates requires that
the relationship between MR and M be
measured for the species in question.
The metabolism of adult squamate rep-

229

tiles can be described by equation (2),

which relates MR to body mass, temperature, and metabolic state. Despite the
ease with which this equation can be used,
variation among taxonomic and ecological
groupings of squamates limits its application. For lizards, nearly one-half of the
variance in MR can be attributed to some
combination of behavior, habitat, and diet.
If that information is available for the
species in question, the estimate of metabolism provided by equation (2) can be
improved by using the mean untransformed residuals in table 2 to adjust the
intercept of equation (2). This procedure
assumes that the value of b for the groups
is identical.
CONCLUSIONS

The pattern and extent of variation in

standard and resting metabolic rates of
lizards and snakes are far from being
clearly revealed by our analysis because
the taxonomic and ecological diversity of
the group has scarcely been sampled. Only
16 of the approximately 34 families of
squamates are represented by observations
of MR, and only eight of these are represented by observations of five or more
species. The number of comparisons of
ecologically homogeneous groups of species is similarly limited. For example, the
prediction that carnivorous lizards would
have higher metabolic rates than would
herbivorous lizards (Pough 1983) could be
tested only by a comparison of five species
of varanids with four species of iguanines
and two scincids. Not only are more observations of these taxa necessary, but the
comparison would profit from observations
of ecologically similar but phylogenetically
distinct groups. For example, measurements of the large carnivorous teiids Callopistes and Tupinambis and of the lacertid
Lacerta lepida or of the herbivorous sincid
Corucia and the agamids Uromastix and
Hydrosaurus would be especially valuable.

LITERATURE CITED
ABE, A. S., and E. G. MENDES.1980. Effect of body
ANDREWS,R. M. 1971. Structural habitat and time
size and temperature on oxygen uptake in the
budget of a tropical Anolis lizard. Ecology 52:262watersnakesHelicopsmodestusand Liophismil270.
iaris (Colubridae). Comp. Biochem. Physiol.
_
1979. Reproductive effort of female Anolis
65A:367-370.
.
(Sauria: Iguanidae). Copeia 1979:620limifrons
ANDERSON,R. A., and W. H. KARASOV. 1981.
626.
Contrasts in energy intake and expenditure in sit_
. 1982. Patterns of growth in reptiles. Pages
and-wait and widely-foraging lizards. Oecologia
273-320 in C. GANS and F. H. POUGH, eds.
49:67-72.

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

230

R. M. ANDREWS AND F. H. POUGH

Biology of the reptilia. Vol. 13. PhysiologyD:

physiologicalecology.AcademicPress,New York.
. 1984. Energeticsof sit-and-waitand widelysearchinglizard predators.Pages 137-144 in R.
L. MAL. E. HUNT,J. L. KNIGHT,
A. SIEGEL,
eds. Ecology and
LARET,and N. ZUSCHLAG,
systematics:a tribute to H. S. Fitch. University
of KansasMuseumof NaturalHistory,Lawrence.
ANDREWS, R. M., and T. ASATO. 1977. Energy

utilization of a tropicallizard.Comp. Biochem.

Physiol.58A: 57-62.
1984.Intraspecific
BAKKER,
A., and R. M. ANDREWS.
variationin metabolicrateof Chalcidesocellatus.
J. Herpetol.18:85-86.
A. F. 1982. The energeticsof reptilian
BENNETT,
activity. Pages 155-199 in C. GANSand F. H.
POUGH,eds. Biology of the reptilia. Vol. 13.
Physiology D: physiologicalecology. Academic
Press,New York.
A. F., and W. R. DAWSON.
1972. Aerobic
BENNETT,
and anaerobicmetabolismduringactivityin the
lizard Dipsosaurus dorsalis. J. Comp. Physiol.
81:289-299.
. 1976. Metabolism. Pages 127-223 in C.
GANSand W. R. DAWSON,
eds. Biology of the
reptilia. Vol. 5. Physiology A. Academic Press,
New York.
1979. Metabolic
BENNETT,A. F., and T. T. GLEESON.
expenditure and the cost of foraging in the lizard
Cnemidophorus murinus. Copeia 1979:573-577.
BENNETT,A. F., and G. C. GORMAN.1979. Population density and energetics of lizards on a
tropical island. Oecologia 42:339-358.
BENNETT,A. F., and K. A. NAGY. 1977. Energy
expenditure in free-ranging lizards. Ecology
58:697-700.

BLUM,J. J. 1977.On the geometryof four-dimensions

and the relationshipbetween metabolism and
body mass. J. Theor. Biol. 64:599-601.
COULSON,R. A., and T. HERNANDEZ.1980. Oxygen
debt in reptiles: relationship between the time
required for repayment and metabolic rate. Comp.
Biochem. Physiol. 65A:453-457.
CRAGG, P. A. 1978. Oxygen consumption in the
lizard genus Lacerta in relation to diel variation,
maximum activity and body weight. J. Exp. Biol.
77:33-56.
DAVIES, P. M. C. 1982. The ontogenetic weight
dependence of metabolism in the Florida king

snake, Lampropeltisgetulus floridana. Comp.

Biochem. Physiol. 73A:291-295.

DMI'EL,
R., and A. BORUT.1972.Thermalbehavior,
heat exchange, and metabolism in the desert
snake Spalerosophis cliffordi. Physiol. Zool. 45:7894.
DUNSON,W. A., and C. R. BRAMHAM.1981. Evaporative water loss and oxygen consumption of
three small lizards from the Florida Keys: Sphae-

rodactyluscinereus,S. notatus,andAnolissagrei.
Physiol.Zool. 54:253-259.

and J. L.
DUTTON, R. H., L. C. FITZPATRICK,
HUGHES. 1975. Energetics of the rusty lizard
Sceloporus olivaceus. Ecology 56:1378-1387.
DUVDEVANI,I., and A. BORUT. 1974. Oxygen consumption and evaporative water loss in four
species of Acanthodactylus (Lacertidae). Copeia
1974:155-164.

EARLL,C. R. 1982. Heating, cooling and oxygen

consumptionratesin Vananusbengalensis.Comp.
Biochem.Physiol.72A:377-381.
FEDER,M. E., and FEDER,J. H. 198 1. Diel variation

of oxygenconsumptionin threespeciesof Philippine gekkonidlizards.Copeia1981:204-209.

FELDMAN,H. A., and T. A. MCMAHON.1983. The

3/4 mass exponent for energymetabolismis not

a statisticalartifact.Respir.Physiol.52:149-163.
M. 1984.Temperatureresponsesof standard
FUSARI,
aerobicmetabolismby the Californialeglesslizard,
Anniella pulchra. Comp. Biochem. Physiol.
77A:97-102.
GOIN, C. J., O. B. GOIN, and G. R. ZUG. 1978.

Introductionto herpetology.3d ed. W. H. Freeman, San Francisco.378 pp.

GRAHAM, J. B. 1974. Aquaticrespirationin the sea
snakePelamisplaturus.Respir.Physiol.21:1-7.
HAYSSEN,V. 1984. Basal metabolic rate and the
intrinsicrate of increase:an empiricaland theoreticalreexamination.Oecologia64:419-421.
HAYSSEN,V., and R. C. LACY.1984. A reexamination

of mammalianmetabolicrates.Am. Zool. 24:957.

A. M. 1960. Energy metabolism as

HEMMINGSEN,

relatedto body size and respiratorysurfacesand

its evolution. Reports of the Steno Memorial
Hospital(Copenhagen)4:7-58.
A. A. 1982. Energymetabolismand body
HEUSNER,
size. I. Is the 0.75 mass exponent of Kleiber's
equation a statistical artifact?Respir. Physiol.
48:1-12.
HEUSNER,A. A., and E. W. JAMESON,JR. 1981.

Seasonal changes in oxygen consumption and

body composition of Sceloporus occidentalis.
Comp. Biochem.Physiol.69A:363-372.
1984. Energy
HINDS,D. S., and R. E. MACMILLEN.
scaling in marsupials and eutherians. Science
225:335-337.
1966. PhysiJ. W., and F. W. BERTRAM.
HUDSON,
ological responsesto temperaturein the ground
skink, Lygosoma laterale. Physiol. Zool. 39:2129.
HUEY, R. B. 1982. Temperature, physiology, and the
ecology of reptiles. Pages 25-91 in C. GANS and

F. H. POUGH,eds. Biology of the reptilia.Vol.

12. PhysiologyC: physiologicalecology.Academic
Press, New York.
J. L., L. C. FITZGERALD,
G. W. FERGUSON,
HUGHES,
1982.Oxygenconsumption
and T. L. BEITINGER.
and temperatureacclimationin the northernprairie swift Sceloporus undulatus garmani from
Kansas.Comp. Biochem.Physiol.71A:611-613.
JOHANSEN,K., and G. LYKKEBOE.1979. Thermal
acclimation of aerobic metabolism and 02-Hb
binding in the snake, Vipera berus. J. Comp.

Physiol. 130:293-300.

KAMEL,S., and R. E. GATTEN,JR. 1983. Aerobic

and anaerobic activity metabolism of limbless

and fossorialreptiles.Physiol.Zool. 56:419-429.
KENAGY, G. J., and D. VLECK.1982. Daily temporal

organizationof metabolismin small mammals:

adaptation and diversity. Pages 322-338 in J.
ASCHOFF,S. DAAN, and G. GROOS, eds. Verte-

bratecircadiansystems.Springer,Berlinand Heidelberg.
M. 1961. The fire of life: an introduction
KLEIBER,
to animalenergetics.Wiley, New York. 454 pp.

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions

ALLOMETRY OF REPTILIAN METABOLISM

Louw, G., B. A. YOUNG, and J. BLIGH.1976. Effect
of thyroxine and noradrenaline on thermoregulation, cardiac rate and oxygen consumption in

the monitorlizardVaranusalbigularisalbigularis.

J. Therm. Biol. 1:189-193.

MARION,K. R. 1982. Reproductive cues for gonadal
development in temperate reptiles: temperature
and photoperiod effects on the testicular cycle of
the lizard Sceloporus undulatus. Herpetologica
38:26-29.
MAUTZ, W. J. 1979. The metabolism of reclusive
lizards, the Xantusiidae. Copeia 1979:577-584.
MAUTZ, W. J., and T. J. CASE. 1974. A diurnal
activity cycle in the granite night lizard, Xantusia

henshawi.Copeia 1974:243-251.

MCMAHON,T. 1973. Size and shape in biology.

Science 179:1201-1204.
MCMANUS,J. J., and D. W. NELLIS.1973. Temperature and metabolism of a tropical lizard, Anolis
acutus. Comp. Biochem. Physiol. 45A:403-410.
MCNAB,B. K. 1980. Food habits, energetics, and the
population biology of mammals. Am. Natur.
116:106-124.
G. G., and A. S. RAND. 1978. MoveMONTGOMERY,
ments, body temperature, and hunting strategy of
a Boa constrictor. Copeia 1978:532-533.
MUELLER,C. F. 1969. Temperature and energy
characteristics of the sagebrush lizard (Sceloporus
graciosus) in Yellowstone National Park. Copeia
1969:153-160.
NAGY, K. A. 1982. Energy requirements of freeliving iguanid lizards. Pages 49-59 in G. M.
BURGHARDTand A. S. RAND, eds. Iguanas of
the world. Noyes, Park Ridge, N.J.
NAGY, K. A., R. B. HUEY, and A. F. BENNETT.

1984. Field energetics and foraging mode of Kalahari lacertid lizards. Ecology 65:588-596.
PORTER,W. P., and F. C. JAMES.1979. Behavioral
implications of mechanistic ecology. II: The African rainbow lizard Agama agama. Copeia
1979:594-619.
POUGH,F. H. 1980. The advantages of ectothermy
for tetrapods. Am. Natur. 115:92-112.
. 1983. Amphibians and reptiles as low-energy
-systems. Pages 141-188 in W. P. ASPEY and
S. I. LUSTICK,eds. Behavioral energetics:vertebrate
costs of survival. Ohio State University Press,
Columbus.
POUGH,F. H., and R. M. ANDREWS.1984. Individual
and sibling-group variation in metabolism of lizards: implications for the origin of endothermy.
Comp. Biochem. Physiol. 79A:415-419.
POUGH,F. H., and S. D. BUSACK.1978. Metabolism
and activity of the Spanish fringe-toed lizard
(Lacertidae:Acanthodactylus erythrurus.J. Therm.
Biol. 3:203-205.
PRIETO, A. A., and W. G. WHITFORD.1971. Physiological responses to temperature in the horned

lizards,Phrynosomacornutumand Phrynosoma
douglassi. Copeia 1971:498-504.
PUTNAM, R. W., and R. W. MURPHY. 1982. Low
metabolic rate in a nocturnal desert lizard, Anarbylus switaki Murphy (Sauria: Gekkonidae).
Comp. Biochem. Physiol. 71A:119-123.

231

RAY, A. A., ed. 1982. SAS user's guide: statistics.

1982 edition. SAS Institute, Cary, N.C.
REGAL, P. J. 1980. Temperature and light requirements of captive reptiles. Pages 79-89 in J. B.
MURPHY and J. T. COLLINS, eds. Reproductive

biology and diseases of captive reptiles. Contributions to herpetology, no. 1. Society for the
Study of Amphibians and Reptiles.
ROBINSON, W. R., R. H. PETERS, and J. ZIMMER-

MANN. 1983. The effects of body size and temperature on metabolic rate of organisms. Can. J.
Zool. 61:281-288.
RUBEN,J. A. 1976. Aerobic and anaerobic metabolism
during activity in snakes. J. Comp. Physiol.
109:147-157.
SMITH,G. C. 1976. Ecological energetics of three
species of ectothermic vertebrates.Ecology 57:252264.
SNYDER,G. K. 1975. Respiratory metabolism and
evaporative water loss in a small tropical lizard.
J. Comp. Physiol. 104:13-18.
1979. Water loss and oxygen consumption
..
in tropical Sphaerodactylus. Oecologia 38:107110.
SNYDER,G. K., and W. W. WEATHERS.1976. Physiological responses to temperature in the tropical
lizard, Hemidactylus frenatus (Sauria: Gekkonidae). Herpetologica 32:252-256.
SOKAL,R. R., and F. J. ROHLF.1981. Biometry: the
principles and practice of statistics in biological
research. 2d ed. W. H. Freeman, San Francisco.
859 pp.
TAIGEN,T. L. 1983. Activity metabolism of anuran
amphibians: implications for the origin of endothermy. Am. Natur. 121:94-109.
TAYLOR,B. M., and P. M. C. DAVIES.1981. Changes
in the weight dependence of metabolism during
the sloughing cycle of the snake Thamnophis
sirtalis parietalis. Comp. Biochem. Physiol.
69A: 113-119.
THOMPSON,J. 1981. A study of the sources of
nutrients for embryonic development in a viviparous lizard, Sphenomorphus quoyii. Comp.
Biochem. Physiol. 70A:509-518.
TINKLE,D. H., H. M. WILBUR,and S. G. TILLEY.
1970. Evolutionary strategies in lizard reproduction. Evolution 24:55-74.
TROYER,K. 1984. Diet selection and digestion in
Iguana iguana: the importance of age and nutrient
requirements. Oecologia 61:201-207.
WILSON, K. J., and A. K. LEE. 1970. Changes in
oxygen consumption and heart rate with activity
and body temperature in the tuatara, Sphenodon
punctatum. Comp. Biochem. Physiol. 33:311322.
WITHERS,P. C. 1981. Physiological correlates of
limblessness and fossoriality in scincid lizards.
Copeia 1981:197-204.
WOOD, S. C., K. JOHANSEN, M. L. GLASS, and

G. M. O. MALOIY.1978. Aerobic metabolism of

the lizard Varanus exanthematicus: effects of activity, temperature, and size. J. Comp. Physiol.
B. 127:331-336.
ZAR, J. H. 1984. Biostatisticalanalysis. 2d ed. PrenticeHall, Englewood Cliffs, N.J. 718 pp.

This content downloaded from 143.229.38.132 on Wed, 6 Aug 2014 08:36:25 AM

All use subject to JSTOR Terms and Conditions