bennett, nagy - 1977 - energy expenditure in free-ranging lizards

8/20/2019 Bennett, Nagy - 1977 - Energy Expenditure in Free-Ranging Lizards

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98

ALBERT F BENNETT AND KENNETH A. NAGY

Ecology, Vol. 58, No. 3

TABLE

Rates of CO, production and body mass in

Sceloporus occidental is during spring and fall

Adults

d d P

P

Total Juveniles

SPRING

Metabolic rate

(ml COPg-I h-l)

Field

.211 .227 .220 .290

(.021,5) (.031,6) (.019,11) (.015,5)

11.9 11.9 11.9 4.4

ody

(g) (1 .1 5) (0.8.6) (0.6.11) (0.5.5)

FALL

Metabolic rate

(ml COPg- h-9

Field

.233 .I78 .I98

(.071,4) (.037,7) (.OM, 11)

Mean (standard error,

N .

HzO equilibrated in

<

1 h in the side-blotched lizard,

Uta stansburiana, another small iguanid

K. A.

N.,

at its point of capture. Animals were recaptured in

1

wk 2 7.4 days, range 5-20 days), and blood sam-

ples were taken again. Tritium content of H2 0distilled

from blood samples was measured by liquid scintilla-

tion; 18 content was determined by the proton-

activation method of Wood et al. (1975). Carbon

dioxide production was calculated using Eq. 8 in Nagy

(1975). Although isotopes could have re-entered

lizards when they were in burrows, no errors in COz

production estimates should occur from this as long as

all the COz in the burrow came from the lizard itself

(Lifson and McClintock 1%6). Eleven of 17 injected

animals were recaptured in the fall; 16 of 21 injected

animals were recaptured in the spring. During both

field periods, lizards lost body mass at slow rates

(1 34% body mass per day in spring and 1.52% in fall).

Rates of resting metabolism during a simulated natu-

ral thermal cycle were then determined for the recap-

tured animals by measurement of OZconsumption and

COz production. During the fall, laboratory mea-

surements were also made on nine uninjected lizards

which were captured fresh from the study area. Mea-

surements were made on resting animals at their pre-

ferred body temperature of 35°C (McGinnis 1966) dur-

ing the day; nighttime temperatures were 20°C (fall) or

placed in ventilated metabolic chambers inside a dark

controlled-temperature cabinet (regulated at

0.5 C)

at 2300 h local time on the night before metabolic de-

terminations. The thermal cycle of the cabinet was

35°C from 0800 to 1600

h

and 18.5 or 20°C from 1600

to 0800 h. Metabolic rate was measured at 1000-1200 h

and 210&2300 h by sampling the gas composition of

the air excurrent from the chamber. Water vapor and

CO, were absorbed with Drieritea (anhydrous calcium

carbonate) and AscariteW (sodium asbestos anhy-

dride), respectively. Oxygen partial pressure was mea-

sured with a BeckmanTM 2analyzer, and 0 consump-

tion was calculated according to the method of Depocas

and Hart (1957). Carbon dioxide production was mea-

sured on animals in the fall. Paired excurrent air sam-

ples were collected: HzO vapor was absorbed from

one, and both H,O vapor and C0 2were removed from

the other. Carbon dioxide production was calculated

from the difference in

0

content of the two samples

(method from

G.

MacLean,personal communication).

All gas volumes were corrected to STPD conditions.

All statistical comparisons were made by two-tailed

Student's t-tests.

At the conclusion of the nocturnal measurements,

the animals were dissected to determine reproductive

condition. Total body water content was determined

by drying the bodies at 65°C to constant mass.

Metabolic measurements under both laboratory and

field conditions are given in Table 1 . The average re-

spiratory quotient measured in the laboratory was

0.67 0.02 a SE), a value insignificantly different

from 0.70, indicating fat catabolism. Consequently, all

laboratory measurements are expressed as C 02 pro-

duction assuming a respiratory quotient RQ) of

0.70. Because there was no difference p 0.89) be-

tween injected and uninjected lizards, laboratory

metabolic data for these two fall groups are combined

in Table 1.

There were no significant sexual or seasonal differ-

ences p > .05) among groups of adults in either field

or laboratory metabolism. The metabolic rates of the

juveniles in both the field and laboratory during spring

were greater than those of the adults

.04

.01).

Such a difference is expected on the basis of smaller

body size of the immature animals as well as metabolic

increments associated with rapidly growing tissue.

The elevation above resting levels which free exis-

tence entails was determined from the difference be-

tween laboratory and field metabolic rates. Lizards on

the study site in both spring and fall emerged and were

active at -0930 h and disappeared at -1730 h, al-

though activity had begun to diminish around 1700 h.

Thus, field animals apparently maintained their pre-

ferred body temperature (35°C) for -8 h every day



Late Spring 1977 LIZARD ENERGY EXPENDITURE 699

TABLE

.

A comparison of resting and field metabolic expenditure for Sceloporus occident lis on a daily basis. (To

convert from joules to calories, divide by 4.184)

Metabolic cost (jou les per gram per day)

Maintenance in laboratory

Free-living in field

Total field Field active

16

hr at

8

hr at Total In Active in Total Resting

18.5 or 20°C 35°C daily burrowa field Total maintenance at 35 C

SPRING

Adult 15.5 41.0

56.5 15.5 125.9 141.4

2.50 3.07

Juvenile 23.0

66.5 89.5 23.0 163.6 186.6 2.08

2.46

FALL

Adult

21.8 42.7 64.5 21.8 105.4 127.2 1.97 2.47

Estimated assuming metabolic rate in burrow is equal to laboratory metabolism at

18.5

or

20°C.

sume a b iphasic tem pera ture regime of 8 h at 35°C and

16 h at 18.5 or 20°C. Deviation s from this biphasic

model d ue t o morning heating and evening cooling will

be relatively minor. To examine daily metabolic rates

in term s of energy expen diture , CO z volumes (T able 1)

were c onve rted to joules using the facto rs 0.0361 ml

C0,J-' for laboratory results (fat catabolism for fast-

ing animals [Schmidt-Nielsen 19751) and 0.0373 ml

C0,J- ' for f ie ld resu l ts (mixed fat an d protein

catabolism, estimated for the lizard Uta stansburiana

eating mealworms, K. A. N., personal observation).

Results of these calculations are shown in Table 2.

Thu s, 40-50% of the energy utilized b y a free-living

S

occidentalis is allocated to resting or maintenance

costs, and the cost of free existence entails approxi-

mately a doubling of these minimal levels.

Another aspect of energy expendi ture may be

analyzed i f we assume that the addi t ional cos t

involved in free existence is not spread evenly

throughou t a 24-h period, but is confined to the

diurnally active hours. In this case, metabolic rate of

field animals in their burrows would be close to that

measure d at night in the laborator y. This assumption is

probably real is t ic s ince ther e must be only minimal

activity for a lizard with low body tempera ture in the

burrow. Field metabolism is partitioned into its active

and inactive comp onents in Tab le 2. T he co sts of field

activity are apparently 2.5 to 3 x the resting meta-

bolic rate of 35°C. This analysis of activity costs

involves the assum ption that field animals were acti ve

for 8 h during every day of the measurement period.

We were not in the field each day to evaluate this

assumption.

DISCUSSION

T w o intriguing findings of this study ar e the absen ce

of higher field metabolic rates during the reproductive

season and the similarity of energy expenditures in

male and female lizards. One might predict increased

energy cost s in spring as a result of heightened social

cost and /or time involvement, or they ar e balanced by

com para ble levels of activity o r tissue synth esis in the

fall. Th e latter suggestion is supporte d by declining egg

production in summer and the subsequent augmenta-

tion of fat body size in this species (Goldberg 1973).

Although the energy investment in a clutch of eggs

(==3 .8kJ, based o n

an

ave rage value of 25.9kJ/g dry wt

for Sceloporus spp. [Ballinger and Clark 1973]), is

rather high in comparison to daily energetic expendi-

ture, the metabolic cost of forming a clutch (as mea-

sured by COz production) may b e low. This increment

includes only the cost of increased feeding and con-

version of food t o egg material; the energy content of

the egg mass does not appear as a metabolic cost. T he

cost of the synthesis involved in egg formation m ay be

rather low since at least a portion of the egg material is

derived from lipids remaining in the abdominal fat

bodies from the previous year (Ha hn and Tinkle, 1965;

W. W. Mayhew ,personal communication). H owe ver,

we are not certain that our field measurem ents include

yolk depositi on, although egg formation is S . occiden-

talis normally occurs during the time of our study (W.

W. Mayhew,personal communication) and five of the

six females in our study had oviducal eggs at autopsy.

Obviously, more extensive studies must be under-

taken to clarify the energetic cost of reproduction in

small lizards.

Given the observation that ectothermic vertebrates

a t a bod y tem per atu re of 3.Z°C hav e resting m etabo lic

rates that a re 10 to 17% of those in endotherm s (He m-

mingsen 1960, Be nnett and D aw son 1976), it is of con-

siderable ecological relevance t o know whethe r energy

expe nditur es of free-living anima ls show a sim ilar ratio

between the two groups. King (1974) has calculated

allometric regression equations that predict the daily

energy cost of free-living birds and rodents, based on

doubly labeled H,O studies as well as othe r methods

involving less direct measures. These equations pre-

dict daily energy ex pend itures of 58.6 and 38.87 kJ for

an 11.9 g bird and ro dent, resp ectively. Th e daily ex-

penditure of an adult S. occidentalis in spring is



700

A L B E RT F . B E N N E T T A N D K E N N E T H A . N A G Y

Ecology, Vol. 58, No. 3

lizard

Sauromalus obesus

during spring; these rat ios

dec rea se to 1-2 whe n calculated on a yearly basis

(Nagy and Shoemaker 1975) . However , the ra t io of

cost o f f ree l iv ing to m ain tenance cost i s remarkably

similar in the se vertebra te gro ups: the rat ios for l izards

are 2 .0 to 2 .5 in

S occidentalis

(Table 2) and 1.7 in

Sauromalus obesus

(Nagy and Shoe mak er 1975) ; fo r

birds, 2.8 in Progne subis (Ut ter and LeFebvre 1970)

and 2.3 in Mimus polyglottos (Utter 1971); and for

rodents (mean monthly averages), 2 .8 in Perognathus

formosus

(Mullen 1970), 2.4 in

Dipodomys merriami

and 2.5 in Dipodomys microps (Mullen 197la), and 3.5

in Peromyscus crinitus (Mullen 1971b). The primary

reason for this discrepancy is that the free-l iving in-

c rem en t r a t i o is calculated from daily rest ing

metabolism at both warm (diurnal) and cool (noctur-

nal) body tem peratures for the l izards , so the de-

nominator of this rat io is

<

10-17 of en do the rm

levels s ta ted abov e. Thu s, an iguanid l izard ca n l ive on

much less energy than can a similar-sized bird or

mammal . This econ omy of the saur ian mode of li fe i s

i l lus t ra ted by th e observat ion that t he amo unt of food

required by a small insec t ivorous bird for 1 day is suf-

ficient for a

S occidentalis

for =35 days .

I t i s apparen t that th e cycl ic thermal reg ime of these

l izards results in a large energetic savings in com pari-

son to a homeothermic endotherm. Despi te the fact

t h at ~ 6 7 f t h e d a y i s s p e nt u n de r gr o un d , o nl y

11-17 of th e daily energy expen diture is used the re

(Table 2). If a l izard remained underground al l day,

instead of emerging and being act ive, i t would reduce

i ts d ail y e n e rg y r e qu i re m e n t b y ~ 8 0 .While ac-

t ive in the f ield, S occidentalis use s -15.90 and

12.975 g-I h-I in spring and fall, respec tively. T he ma x-

imal rat e of aer obic m etabolism is 42.685 g-I h-I a t

35°C for adul t s o f th is species , assuming an RQ of

0 .7 (Bennet t and Gleeson 1976) . Thus, the average

metabolic r at e during field act ivi ty is abou t on e fou r th

the potential scope. However, ut i l izat ion of the ful l

aerobic scope en tai l s considerab le anaerobic metab-

olism, which would restr ict act ivi ty rapidly (Bennett

and Dawson 1976).

This research was supported by N S F Grant PCM 75-10100

(A.F.B.) and Co ntract E(04-1) GEN-12 between the U .S. E n-

ergy Research and Development Administration and the

University of California (K. A. N.) . We thank S . Rockhold

and T. Gleeson for help in collecting animals, and W. W.

Mayhew for unpublished observations on reproduction in

Sceloporus

Ballinger, R. E. , and D. R. Clark, Jr . 1973. Energy content

of lizard eggs and th e measu rement of reproductive e ffort .

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127-223. In C. G an s and W. R . Daw son [ed s.] Biology of

the Reptilia, Vol. 5 (Physiology A). Academic Press, New

York.

Bennett , A. F. , and T. T. Gleeson. 1976. Activity me-

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Zoo l. 49:6 76.

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1957. Use of the Pauling oxy-

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bennett, nagy - 1977 - energy expenditure in free-ranging lizards

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