AMER. ZOOL., 25:945-954 (1985)
The Uses of Anaerobiosis by Amphibians and Reptiles1
ROBERT E. GATTEN, JR.
Department of Biology, The University of North Carolina at Greensboro,
Greensboro, North Carolina 27412
SYNOPSIS. Amphibians and reptiles rely upon anaerobic glycolysis to support their energetic requirements under a variety of circumstances. Although adult frogs derive most of
the energy for muscle contraction during intense, short-term locomotion from glycolysis,
anuran tadpoles have a very low rate of lactate formation during 30 sec of burst swimming;
instead, they rely largely on the use of phosphocreatine stores. Among squamate reptiles,
the rate of lactate formation during vigorous exercise is largely related to the duration
of activity and to body temperature. Recent studies have shown that fossorial, limbless
reptiles do not differ from surface-dwelling, quadrupedal species in the rate of glycolysis
during intense activity. The energetics of locomotion differs significantly between swimming and running turtles; thus the site of activity influences the role of anaerobiosis in
movement. Lactate levels increase in some frogs during calling and nest building and in
some reptiles during prey capture and ingestion. However, voluntary locomotion and
diving by reptiles are rarely accompanied by an increase in lactate levels. Freshwater turtles
rely heavily on glycolysis during aquatic hibernation. Thus, it can be concluded that
amphibians and reptiles derive a significant proportion of their energetic requirements
from anaerobic metabolism only under selected circumstances when the benefits outweigh
the costs associated with the accumulation of lactate.
INTRODUCTION
In 1886, Marcuse demonstrated that vigorously contracting frog skeletal muscle
accumulates large amounts of lactic acid.
Over the subsequent decades, muscle
biochemists and exercise physiologists have
continued to use frog muscles in their
attempts to understand the mechanics and
energetics of contraction. The importance
of glycolysis, with the concurrent buildup
of lactic acid, is now well understood (Shephard, 1982). Most of those working with
frog muscle in laboratory experiments have
given little thought to the role that glycolysis might play in the normal activities
of the intact animal in its natural environment. However, about a decade ago, our
perspective on the role of anaerobiosis in
the provision of power for amphibians and
reptiles during normal movement began to
grow (Bennett and Dawson, 1972; Bennett
and Licht, 1972, 1973, 1974; Seymour,
1973). As a consequence, we now have a
fairly good understanding of the role of
glycolysis during muscular exercise in these
ectotherms, especially during intense,
short-term "burst" activity (Bennett, 1978,
1980, 1982; Taigen et al, 1982). In this
paper, I will review some of the recent
research in this area of exercise physiology
and also consider the role of anaerobiosis
during diving and hibernation by reptiles.
ANAEROBIC METABOLISM DURING
MUSCULAR ACTIVITY
Glycogen is the major substrate and lactate is the major end-product of anaerobic
metabolism in vertebrates. Other endproducts such as pyruvate, succinate, or
alanine accumulate much more slowly than
lactate (Hochachka and Storey, 1975;
Hochachka et al., 1975; Bennett, 1978;
Shephard, 1982). Measurements of blood
lactate, although common in studies of
human performance (Astrand and Rodahl,
1977), do not necessarily yield a precise
estimate of the intensity of glycolysis in
muscle or other tissue because lactate is not
uniformly distributed throughout the body
and may not reach a maximal level in the
blood until hours after the cessation of
activity (Moberly, 1968; Bennett and Licht,
1972; Gatten, 1975). Therefore, in most
the studies of anaerobiosis discussed
of
1
From the Symposium on Animal Energetics: here, lactate measurements were carried
Amphibians, Reptiles, and Birds presented at the Annual out on homogenates of whole animals.
Meeting of the American Society of Zoologists, 27Although glycolysis can provide the mus30 December 1983, at Philadelphia, Pennsylvania.
945
946
ROBERT E. GATTEN, JR.
30-
ADULTS
LARVAE
ITAILS)
ISARTORIUS)
20-
O)
10-
n
LACTATE
I
n
PC
LACTATE
PC
FIG. 1. Concentrations of lactate and phosphocreatine (PC) in the tails of Rana catesbeiana tadpoles and in
the sartorius muscle of Rana pipiens adults at rest (open bars) and after intense, short term activity (hatched
bars). Larval data from Gatten et al. (1984); adult data from Mainwood el al. (1972).
cles with ATP very rapidly, it has a number
of significant drawbacks (Bennett, 1980).
For example, the accumulation of lactate
is accompanied by fatigue and followed by
a long recovery period during which the
animal has a reduced capacity for locomotion. Thus, we might expect this process to be used only when the benefits of
a rapid supply of energy exceed the costs
associated with a buildup of lactate.
Anaerobiosis in larval anurans
Adult frogs accumulate lactate rapidly
during short bursts of intense exercise such
as that employed during escape from a
predator (Bennett and Licht, 1973, 1974;
Hutchison andTurney, 1975; Carey, 1979;
Hillman and Withers, 1979; Hutchison and
Miller, 1979; Taigen et al, 1982). Vigorous activity over short intervals appears to
have survival value in anuran tadpoles as
well (Huey, 1980; Feder, 1983). Therefore, Gatten et al. (1984) have recently
asked if glycolysis is of equal importance
in larval anurans and in their adult counterparts during intense, short-term movement. We measured the rate of accumulation of lactate in tadpoles of barking tree
frogs (Hyla gratiosa), bullfrogs {Rana catesbeiana) and grassfrogs (R. utricularia) swimming vigorously for 30 sec. Their anaerobic scopes (rate of lactate accumulation in
/tg of lactate per gram of body mass per
minute of activity) are only about 20% of
those of adult hylid and ranid frogs (Gatten
et al., 1984). Our results thus confirm the
early observation of a low anaerobic scope
in bullfrog larvae (Bennett and Licht,
1974). If glycolysis does not provide much
power for such intense swimming, from
what source is the ATP for contraction of
the tail muscles derived? Exhaustive exercise by these tadpoles is accompanied by a
depletion of phosphocreatine (PC) from
their tails (Fig. 1); during this time the lactate level changes very little (Gatten et al.,
947
ANAEROBIOSIS IN AMPHIBIANS AND REPTILES
TABLE 1. Average rate of lactate formation in squamate reptiles during activity.
Species
Duration of
activity
(min)
Tb(°C~)
Body mass
(g)
Lactale formation (>ig g"1
mm l )
Reference
Quadrupedal lizards
Anolis bonairensis
Anolis carolinensis
3
Dipsosaurus dorsalis
0.5
2
Phrynosoma platyrhinos
Sceloporus occidentalis
0.5
2
Uta stansburiana
0.5
0.5
28
20
30
37
37
25
30
35
40
45
37
20
25
30
35
40
20
5.0
4.5
4.5
4.5
33.4
35.2
35.2
35.2
35.2
35.2
18.5
13.1
13.1
13.1
13.1
13.1
4.0
4.0
1.2
1.2
1.2
37
Xantusia vigilis
0.5
12
20
30
300
1,240
1,340
1,540
1,700
554*
644*
659*
907*
665*
980
536*
512*
862*
757*
587*
1,180
1,780
540
Bennett et al., 1981
Bennett and Licht, 1972
Bennett and Licht, 1972
Bennett and Dawson, 1972;
Bennett and Gleeson, 1976
Bennett and Licht, 1972
Bennett and Gleeson, 1976
Bennett and Licht, 1972
Bennett and Licht, 1972
1,320
1,560
Limbless lizards
Anniella pulchra'
Ophisaurus ventralis1
2
2
25
25
Crotalus virtdis
Masticophis flagellum
Nerodia sipedon
Thamnophis butlen
Thamnophis elegans
Thamnophis sirtalis
5
5
0.5
2
2
4
35
35
25
25
20
25
4.9
32.2
Snakes
304.2
265.8
3.7
19.0
14.4
1.2
426
956
Kamel and Gatten, 1983
Kamel and Gatten, 1983
194
348
971
404
545
224
Ruben, 1976
Ruben, 1976
Pough, 1978
Kamel and Gatten, 1983
Feder and Arnold, 1982
Pough,1977
424
Kamel and Gatten, 1983
Amphisbaenian
Trogonophis wiegmanni*
2
25
5.0
* Calculated from nM ATP (g x 2 min)"1 in Bennett and Gleeson (1976) assuming that 16.7
formed by anaerobic means represents the accumulation of 1,000 jig of lactate.
F
= fossorial.
1984). Rapid contractions of adult frog sartorius muscle coincide not only with a significant reduction in PC but also a large
rise in lactate concentration (Fig. 1) (Mainwood et al., 1972). Thus, larval and adult
anurans appear to differ in the degree to
which they can liberate ATP by glycolysis
during short term, vigorous exercise. In
contrast with our results, Quinn and Burggren (1983) found that tadpoles swimming
less intensely than our specimens accumulated large quantities of lactate over 5
min. Thus, it appears that the significance
of glycolysis in tadpoles differs between
burst swimming and longer term locomotion.
ATP
Anaerobiosis in squamate reptiles during
intense activity
Lactate accumulates rapidly in lizards and
snakes during vigorous exercise of 0.5-5.0
min (Table 1, Fig. 2). Stepwise multiple
regression analysis of the data in Table 1
reveals that the duration of muscular activity accounts for 59% of the observed variance in the rate of lactate formation. Figure 2 illustrates the average rate of lactate
formation of squamates active for different
intervals. Because the maximal rate of lactate formation during activity (=anaerobic
scope, Bennett and Licht, 1972) persists
for only about 30 sec, animals active for
948
ROBERT E. GATTEN, JR.
1800-
QUADRUPEDAL
LIZARDS
1500•
O 30 SEC
c
©
2 MIN
I
•
3 MIN
O)1200HI
LIMBLESS
LIZARDS
o
A
900-
2 MIN
SNAKES
en
a 30 SEC
(3 2 MIN
• 3-5MIN
I - 600-
AMPHISBAENIAN
X
CC
2 MIN
o
UJ 300-
o
<
10
20
30
40
50
V°ci
FIG. 2. Average rate of lactate formation in squamate reptiles during periods of activity of 0.5-5.0 minutes
as a function of body temperature. Points connected by lines are for a single species. See Table 1 for sources
of data.
longer times (2-5 min) may have a high
anaerobic scope but a low average rate of
lactate formation over the prolonged
interval of exercise. Body temperature
accounts for an additional 10% of the variance in the rate of lactate formation; neither body size, the presence or absence of
limbs, nor the habitat occupied contribute
significantly to the variance. The equation
relating the average rate of lactate formation to duration of exercise (0.5-5.0
min) and temperature (20-40°C) in squamate reptiles is
Lactate formation (ng lac. g~'min~1) =
780 - 281 (Time in min)
+ 18(Temp. in °C)
(1)
(n = 30 P < 0.001
r2 = 0.69)
As is apparent from Figure 2, the average
rate of lactate accumulation is highest in
short bouts of activity; at 30°C, the value
for 0.5 min of activity is 1.56 times that for
2 min of maximal exercise. Although not
apparent from Figure 2 (because it is drawn
on arithmetic rather than semi-log axes),
eq. 1 predicts (1) that the thermal sensitivity (Qio) of lactate formation in squamates
will decline with rising temperature at any
duration of activity and (2) that the Q10 of
lactate formation rises with the duration
of activity. Thus, low temperatures reduce
the rate of glycolysis to a greater extent in
prolonged (i.e., >2 min) exercise than in
brief (i.e., 30 sec) bouts of activity. The
absence of a statistically significant influence of body size on lactate formation
among these species (P = 0.0523) may
result from the relatively narrow range of
sizes of animals studied to date and included
in the analysis (x ± SD = 45.0 ± 91.3 g,
range = 1.2-304.2 g) (see also Bennett,
ANAEROBIOSIS IN AMPHIBIANS AND REPTILES
1982, p. 179). However, lactate level at
exhaustion increases with body size in both
Thamnophis sirtalis and Nerodia sipedon
(Pough 1977, 1978); thus the influence of
body size on anaerobic metabolism during
activity is evident intra- but not interspecifically.
949
the site of activity. Recently, Stockard and
Gatten (1983) found that the anaerobic
scope of painted turtles (Chrysemys picta)
swimming vigorously in a tank of water was
three times that of turtles running on a dry
surface. Furthermore, we discovered that
running turtles breathed to such an extent
that their oxygen stores were not utilized;
Anaerobic scope in limbless, fossorial reptiles
in contrast, swimming turtles rarely surRecently Kamel and Gatten (1983) faced and thus partially depleted their oxyexamined the changes in aerobic and gen stores. As a consequence, the relative
anaerobic metabolism that accompany 2 roles of atmospheric oxygen, stored oxymin of vigorous activity in three limbless, gen, and anaerobic glycolysis in providing
fossorial squamates: the lizards Anniella ATP for exercise varied considerably with
pulchra and Ophisaurus ventralis and the the location of exercise (Fig. 3). The total
amphisbaenian Trogonophis wiegmanni. amount of ATP synthesized during activity
Anniella and Trogonophis have rates of lac- was twice as great for turtles in water as
tate formation (Table 1) that are 64% of for those in a dry chamber; furthermore,
that predicted by eq. 1 for squamates active glycolysis provided a greater percentage of
for 2 min at 25°C whereas Ophisaurus has the ATP in swimming turtles than in runa rate 2.25 times that of the other two fos- ning specimens. Additional studies of the
sorial species and 1.43 times that predicted energetics of activity of amphibious repby eq. 1. Thus, there is considerable diver- tiles in terrestrial and aquatic environgence in the rate of lactate formation dur- ments should further elucidate the physing activity among limbless, burrowing iological consequences of locomotion in
reptiles. In spite of this variation, glycolysis different habitats.
makes the same relative contribution to the
total amount of ATP provided in these The role of anaerobiosis during
three species during 2 min of intense exer- "routine" behavior
cise: 73-78% of the ATP is derived from
During the last decade, many workers
this pathway whereas the remainder comes have sought to determine the importance
from aerobic metabolism. Such a parti- of glycolysis in amphibians and reptiles
tioning of energy sources for exercise is during manually or electrically induced
common among reptiles (Bennett, 1982). maximal-intensity locomotion in the labOn the basis of these comparisons, Kamel oratory (see Bennett, 1978, 1982, and Taiand Gatten (1983) conclude that in spite gen et al., 1982). Only recently have physof significant differences between limbless, iological ecologists begun to examine the
fossorial reptiles and their quadrupedal, role that glycolysis plays during more natsurface dwelling counterparts both in anat- ural, voluntary behaviors. Recently, Pough
omy and in the mechanics of locomotion, and Gatten (1984) found that male spring
there are insufficient data to distinguish peepers (Hyla crucifer) in a breeding chorus
between them using metabolic indices.
have a whole body lactate level slightly elevated above that of resting animals. This
Anaerobiosis during locomotion in
increase is most likely due to glycolysis in
limb muscles rather than in the abdominal
different habitats
Many amphibians and reptiles are active muscles used in calling because the latter
in both aquatic and terrestrial environ- apparently are powered by fatty acid oximents. Because the mechanics and ener- dation, not glycolysis (Taigen et al., 1985).
getic cost of locomotion differ substantially Ryan et al. (1983) found that calling male
between these two media (Schmidt-Niel- neotropical frogs (Physalaemus pustulosus)
sen, 1983), it seems likely that the role of had a mean whole body lactate level 56%
anaerobic metabolism in a reptile or above that of resting frogs, but the differamphibian during movement will vary with ence was statistically insignificant, most
950
ROBERT E. GATTEN, JR.
25 °C
2 MIN
•
Chrysemys picta
FROM CHAMBER AIR
1 3 FROM O 2 STORES
FROM GLYCOLYSIS
IN DRY CHAMBER
44%
56%
IN WATER
V
X
0
26%
3%
71%
1
2
TOTAL SCOPE I pM ATP g
3
1
4
1
miiT )
FIG. 3. Total metabolic scope for activity of painted turtles running in a dry chamber and swimming in
water. The total scope is the rate of formation of ATP from both aerobic and anaerobic metabolism during
exercise. It is calculated from data on consumption of oxygen from chamber air, on depletion of oxygen
stores, and on accumulation of lactate using the equations of Bennett and Licht (1972) and the data of Stockard
and Gatten (1983).
likely because of the low sample sizes. Lactate accumulates significantly in neotropical frogs during nest construction (Ryan et
al., 1983) and in salamanders during attempts to escape from snakes (Feder and
Arnold, 1982) and during courtship (Bennett and Houck, 1983). Among reptiles,
lactate accumulates in snakes subduing and
ingesting salamanders (Feder and Arnold,
1982) and occasionally during voluntary
diving (Seymour, 1979, 1982). There is a
buildup of lactate in lizards capturing and
swallowing crickets (Pough and Andrews,
1985a), in lizards engaged in territorial
defense (Bennett et al., 1981; Pough and
Andrews, 19856), and in female green sea
turtles during nesting (Jackson and Prange,
1979). Hatchling sea turtles accumulate
large quantities of lactate while digging out
of the nest and in their dash from the nest
to the surf (Dial, pers. comm.). However,
glycolysis appears to be of little or no significance during prolonged crawling (concertina) by the bipedal amphisbaenian, Bipes
biporus (Dial, Gatten, and Kamel, unpub-
lished data), or during voluntary diving by
marine iguanas (Amblyrhynchus cristatus) and
freshwater turtles (Gleeson, 1980; Gatten,
1981, 1984).
Although lactate may accumulate in
amphibians and reptiles during some routine activities, there are a number of problems that impede the assessment of the
physiological and/or adaptive significance
of glycolysis in such behaviors. Mean resting lactate levels (and standard deviations)
vary dramatically among the studies cited
above (e.g., 37 ± 19 ng g~' in Hyla crucifer
[Pough and Gatten, 1984] as compared
with 320 ± 220 ng g"1 in Physalaemus pustulosus [Ryan et al, 1983]). Thus, a similar
increase in glycolysis during a given behavior may prove to be statistically significant
in one study but not in another. Assessment of what constitutes "resting" behavior and resting lactate level is needed in
each study. Furthermore, most studies
report lactate levels for a group of animals
engaged in a certain behavior but often do
not quantify the duration of such activity.
ANAEROBIOSIS IN AMPHIBIANS AND REPTILES
951
Thus, the rate of lactate formation (and/
or degradation) cannot be calculated. I
would hope to see studies in which radioactively tagged lactate is injected into animals and their behavior and subsequent
lactate level followed (see Brooks et al.
1973). Such investigations would permit an
analysis of the rate of lactate formation
(and degradation) under near-natural conditions. Additionally, although a given
behavior may be accompanied by a large
increase in total body lactate, glycolysis may
provide a relatively insignificant portion of
the total ATP because aerobic metabolism
may also increase dramatically. For example, lactate accumulation is marked but
anaerobiosis provides less than 8% of the
total ATP during nest building by frogs
(Ryan et al, 1983) and during the capture
and ingestion of prey by lizards (Pough and
Andrews, 1985a). Finally, the use of high
energy phosphates may be a more significant source of energy and have greater
adaptive value than glycolysis in certain circumstances. For example, tadpoles escape
from capture attempts of turtles by very
short duration (x = 11 sec) bursts of swimming not accompanied by the accumulation of lactate (Feder, 1983); under those
circumstances, the use of ATP and PC
stores will be much more important to survival than will glycolysis (see also Gatten et
al, 1984). Attention to these problems in
future studies should result in an increased
refinement in our understanding of the significance of glycolysis during routine activities of amphibians and reptiles.
tary diving by these animals. When painted
turtles (Chrysemys picta) are permitted to
dive or surface at will for up to 5 days, they
do not accumulate lactate; however if they
are induced to swim vigorously for 2 min,
prohibited from surfacing for 1 hour by
manual prodding, or forced to dive in
deoxygenated water for 24 hr, they accumulate lactate rapidly and to very high
levels (Fig. 4) (Gatten, 1981; Stockard and
Gatten, 1983). Painted turtles swimming,
diving, and surfacing at will in outdoor
pools in the summer also have very low
lactate levels (Fig. 4) (Gatten, 1981). Similarly, loggerhead musk turtles diving voluntarily for 24 hr at 22°C do not accumulate lactate (Gatten, 1984). These data,
together with those for lactate levels in
marine snakes and the marine iguana (Seymour and Webster, 1975; Heatwole, 1978;
Seymour, 1979; Gleeson, 1980) and for
voluntary dive times and records of oxygen
consumption of freely diving reptiles (Smith
etai, 1974; Heatwole, 1975; Seymour and
Webster, 1975; Bartholomew etai., 1976;
Gatten, 1980, 1984; Lewis and Gatten,
1985) strongly suggest that voluntary, quiet
dives by reptiles are only rarely accompanied by reliance on glycolysis. Instead,
the use of oxygen stores is supplemented
in some species by extrapulmonary oxygen
uptake and the dive is terminated before
oxygen stores are exhausted (see Seymour,
1982, for review).
ANAEROBIC METABOLISM DURING DIVING
If turtles do not use their very high
capacity for anaerobic metabolism during
routine diving, when do they use it? Hibernation seems to be a good candidate. Many
aquatic turtles overwinter underwater or
buried in mud whereas terrestrial species
often spend the winter months in burrows
(Gregory, 1982; Seymour, 1982); in both
situations, low oxygen levels may be
encountered. To test the possibility that
aquatic turtles rely on glycolysis during such
times, I measured the lactate levels of
painted turtles (Chrysemys picta) in an outdoor tank with water 76 cm deep over 67
days in the winter (Gatten, 1981). The tur-
In 1963, Belkin demonstrated that
freshwater and terrestrial turtles are 7-25
times as tolerant to anoxia as are lizards,
snakes, crocodilians, and marine turtles.
This great ability of freshwater chelonians
to withstand both anoxia {i.e., 100% N2)
and forced dives is due in part to their
capacity to rely on glycolysis and to endure
the buildup of lactate (Belkin, 1961; Robin
etai, 1964; Jackson, 1968; see also Bennett
and Dawson, 1976, and Seymour, 1982,
for review). However, only recently has any
attention been focused on the role that glycolysis might play during routine, volun-
ANAEROBIC METABOLISM DURING
HIBERNATION
952
ROBERT E. GATTEN, JR.
Chrysemys picta 25 °C
LAB
RESTING IN AIR, 15 h
FREELY DIVING, 12 h
FREELY DIVING, 5 DAYS
MAXIMAL ACTIVITY IN WATER, 2 min
THREAT INDUCED DIVE, 1h
FORCIBLE SUBMERGENCE, 24 h
FIELD
FREELY DIVING IN POOLS
200
400
600
800
1000
1200
1800
2000
1
WHOLE BODY LACTATE lug g I
FIG. 4. Total body lactate concentrations of painted turtles under a variety of conditions. Data from Gatten
(1981) and Stockard and Gatten (1983).
ties rested quietly on the bottom of the
tank and were never observed at the surface. Ice covered the surface on 42 days
and the mean water temperature was 3.7°C
(range 0-8°C). Lactate levels increased
during the winter to extremely high levels
(5,580 fig g"1). These and similar results
by Ultsch and Jackson (1982) demonstrate
that painted turtles rely heavily on glycolysis to supply their energetic requirements
during aquatic hibernation.
Terrestrial turtles also have a high
capacity for anaerobiosis (Belkin, 1963) and
may utilize it during hibernation in burrows. During the winter of 1982-83, I
measured the lactate levels in 14 box turtles (Terrapene Carolina) in a field in South
Carolina. That winter was relatively mild
and the turtles often emerged from their
burrows during warm spells. Their lactate
levels were low (x ± SD = 100 ± 38 ng
g~') and did not increase between November and March (Gatten, 1986). Thus, it
appears that during mild winters, this
species does not rely on glycolysis to meet
its energy needs; apparently enough oxygen is present in the burrow to meet the
aerobic requirements of these turtles.
CONCLUSION
It is clear that amphibians and reptiles
rely on anaerobic metabolism to support
their activities under a variety of circumstances. Depending on the species and condition, glycolysis may or may not be used
and may or may not provide a significant
proportion of the total ATP supply.
Anaerobiosis is clearly of great importance
during short term, intense muscular exercise such as that used during escape from
a predator. The intensity of glycolysis during exercise varies with the environment
in which the activity occurs, at least in one
species of turtle. Lactate accumulates during some reproductive behaviors of amphibians and reptiles. Glycolysis seems to
be of little significance in routine, quiet
diving by reptiles but of major importance
ANAEROBIOSIS IN AMPHIBIANS AND REPTILES
in aquatic hibernation. Further studies of
(1) the role of ATP and PC stores during
activity, (2) the relative importance of glycolysis and aerobic metabolism during
aquatic and terrestrial locomotion by
amphibious species, and (3) the significance of anaerobiosis during routine
behavior would seem to be most desirable.
ACKNOWLEDGMENTS
I am grateful for the financial support
provided over the years by the Department
of Biology and the Research Council of the
University of North Carolina at Greensboro. My work at the Savannah River Ecology Laboratory (in conjunction with J. C.
Caldwell and J. Congdon) was supported
by contract DE-AC09-76SR00819 between
the U.S. Department of Energy and the
University of Georgia's Institute of Ecology and by a travel contract from Oak
Ridge Associated Universities. I am very
grateful to A. F. Bennett for constructive
comments on an earlier draft of the manuscript.
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