Vol. 7. pp. 147-152

Asiatic Herpetological Research1997

A Comparison of Embryonic Metabolic Rates in
Two Lizards
Pei-chao Wang and Xiang Ji
12'Department of Biology, East China Normal University, Shanghai 200062. China; -Department of Biology.
Hangzhou Normal College. Hangzhou. J 10012. China
Abstract. -The metabolic rates of eggs in both the wall lizard Gekko japonicus and the grass lizard Takydromus
scptentrionalis were measured through incubation

at32°C.

The ontogeny of embryonic metabolism in boththat develop inspecies of lizards exhibits an exponential pattern, similar to that recorded for some squamatesparchment-shelled eggs, but different from some crocidilians and chelonians that develop in parchment-shelled

and brittle-shelled eggs.

Both the embryos and hatchlings of T scptentrionalis have higher metabolic rates than those of G. japonicus.
An embryo of T septentrionalis consumes more oxygen than that of G. japonicus, although the latter species has
a much longer incubation period at 32°C.

Takydromus scptentrionalis. Gekko japonicus. Hatchling. Embryonic Metabolic Rate.
Exponential Pattern. Incubation. Egg. Oxygen. Consumption.

Key words:Sauria.

Introduction

al..

1991 ). In contrast, the grass lizard (T septentrion-alis) is a diurnal

Embryonic metabolic characteristics of incubating
eggs have been reported for at least 23 species of living reptiles, including seven species of snakes (Clark.

1953; Dim'el, 1970: Black et al.. 1984). eleven speciesof chelonians (Lynn and Von Brand. 1945; Ackerman.

Gettinger et al.. 1984; Webb et al., 1986;
Thompson 1989; Wang et al.. 1990). one species of1981;

lizard (Wang et al., (1989), three species crocodilians(Thompson, 1989; Whitehead and Seymour, 1990),
and one species of tuatara (Thompson. 1989). Threepatterns of the ontogeny of embryonic metabolism in
reptiles have been recognized in incubating reptilian

eggs:

peaked, sigmoid, and exponential (Thompson.

1989; Whitehead and Seymour. 1990:

Wang

1990).

These patterns are very similar

observedin birds(Vleck etal..

1980:

toWangontogeny of metabolism of the eggs of these species
during incubation.

Materials and Methods
Gravid Gekko japonicus and Takydromus septentrionalis

were collected on buildings in Shanghai and infields on the Zhoushan Islands, respectively.

The cap-thosein aquaria, and fed with mealworms (larvae of Tenebrio molitor). Eggs were laid at room temperatures ofetal..

patterns in lizards (especially in geckos) are different
from those of other reptiles.

speciesincreasingly turgid during incubation (Wang. 1966).
In this paper we compare the characteristics of thetured animals were taken to the laboratory, maintained

metabolic ontogeny are species-specific, and whether

lizard(Wang. 1964).
two to five parchment-shelled eggs each, are laidannually in humid soil where they swell and becomeal..

et1991 ). However, it is still unclear whether patterns of

The twoand active forager in high grasses

One or two, rarely three, clutches of(Gekko japonicus andTakydromus septentrionalis) studied show distinct differences in activity patterns, foraging behavior, andmicrohabits (Liu and Hu. 1940; Wang. 1964. 1966).
The wall lizard (G. japonicus) is a nocturnal, sit-andwait predator found on the walls of old houses andtemples. It remains immobile for more than half of its
One to three clutches two eggs
nocturnal period.
each, are oviposited annually (Liu and Wu. 1940; Ji etEach freshly laid egg was numbered, theandwidth were measured (nearest 0.1 mm),length24-28°C.

and the wet mass recorded (nearest 0.

1mg). Egg vol-ume was calculated by using the ellipsoid equation

V=-4 Turb. where V=volume, a= -2 of width and b= 2ll

The surface area of each eggshell wasof length.
obtained by measuring the width and length axes of
2a and 2b. respectively, and substituting them in theequation for the area of ellipsoid.

b' +a"b-fb" - a"a" + bVol. 7, p. 148

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Asiatic Herpetological Research

1997

1

Asiatic Herpetological Research

997

Vol. 7, p. 149

0.28

0.26 H^.C

0.24-6)

0.22

T.

k

septentrionalis

G. japonicus

0.20-

I

0.18-

Co

0.16-

Q.

0.14-

E
0.12</)

Coo

0.10-10.08cQ>

D)

0.06-

O004 H
0.02•*II

i10—-—-—-30

20

Percentage

of70

60

50

401009080

incubation period

Figure 1 Relationship between oxygen consumption of eggs in two species of lizards (Takydromus septentrionalis
and Gekko japonicus) and the percentage of incubation period at 32 C. Squares (T. septentrionalis) and circles.

(Gekko japonicus) represent mean values of oxygen consumption of eggs. Vertical lines indicate two standard
deviations about the mean. The dashed lines indicate normalization curves of oxygen consumption per egg at different stages of incubation.

nation time in Fig. 1.

The following semi-logarithmicof G. japonicus could not be detected until about theday of incubation (12% of the incubation

regression equations are best fittedfourthbT ± c, where V is oxygen consumption in ml

The average total oxygen consumed during
embryonic ontogeny was 73.48 ml On/egg or 274.79

by those data.
These equations are of the general form: log V= a +*h, and2 /eggs

T is time in days.

mlFor G. japonicus:
log

2 /g

per gram mass of initial egg mass, or 0.0293

ml 0i/mnT per square millimeter of initial egg surface

V = -1.5017+0.0087T ±0.0768(r=0.98.

P<0.01).

area in T. septrionalis, and only 104.42 ml

153.15 ml

For T. septentrionalis:
logperiod).

V= -1.4340+0.0086T ± 0.0740 (r=0.95,2 /g.

2 /eggoror 0.0204 ml On/mm" in G. japonicus,

although the latter species had a much longer durationof incubation that averaged 42.9 days at hatchingP<0.01).

(Table 1).

The slopes (b) of the regression equations of thetwo species lizards are nearly the same (b=0.0086 andb=0.0087). The two species had the same general pat-mass of hatchlings averaged
0.6547 (SD=0.0870. N=16) ml 2 /g * h for T. septen-terns of exponential embryonic metabolic ontogeny astrionalis and 0.4603

thatusually(Dim'el,observed

1970;Black.

inothersquamate1984) and in

reptilesaltricial

birds(Vlecketal.. 1979).

Embryonic metabolic rates of T. septentrionalis on
the0.

1

and second days of incubation averaged
79 ml 2 g * h and 0. 196 ml 2 /g * h for per gram
first1

Metabolic Rates of Hatchlings. The
bolicrate

restingfor G. japonicus.

(SD=0.0476, N=16) ml

2 /g

* h

So that the resting metabolic rate ofT. septentrionalis is 0. 1944 ml

than that of G. japonicus.

*2 /gh, or

42% higher

For G. japonicus, oxygen

consumption of hatchlings and eggs just before pip* hping were 0.2144 (SE=0.0186, N-19) ml 2 /lizard

1mass egg respectively. Oxygen consumption of eggs

meta-per gramand 0.2139 (SD=0.0148, N=19) ml

2 /egg*h. respec-For T. septentrionalis, oxygen consumption oftively.

1997

Asiatic Herpetological ResearchVol. 7, p. 150

new hatchlings and eggs just before hatching were*h and
0.2024 (SD=0.0069. N=16) ml
2 /lizard
0.2072 (SD=0.0300. N=16) ml

2 /egg*h. respec-

oxygen consumption during embryonic ontogeny at
32°C per gram or per square millimeter of initial incubation egg mass or surface area in G, japonicus wasonly 153.15 ml
to 274.79 ml

tively.

2 /g or 0.0204

ml

2 /mirr.

or 0.0293 ml/mm: /g11compared

for T. septentri-

onalis i.e., 179.4% or 143.6% higher, respectively.

Discussion
To our knowledge,

thisisthefirstreportontheInshows that the regression curve ofoxygen consumption for G. japonicus was clearlyaddition. Fig.

1embryonic metabolic ontogeny of lizards. Our results

lower than that of T. septentrionalis.

Also, the stan-show

dard rates of evaporative water loss

inboth these lizards have an exponential
This pattern ismetabolic).
pattern. (Fig.
embryonicthat1some snakes

or lizards that develop inand
those birds with altricial
parchment-shelled eggs
similar tosome gekko

eggs are lower than other reptiles (Dunson and Bramham, 1981; Dunson, 1982). The low level of metabolism may be a characteristic of gecko eggs.

hatchlings. but differs from the peaked and sigmoid
patterns observed in some crocodilians, sea turtles,

sible reason for the difference in embryonic metabo-and fresh water turtles (Vleck et al.. 1979; Ackennan.

lism between the two species

1981a. 1981B; Whitehead and Seymour. 1990).

structural characteristics of the eggshells. The eggs ofWhitehead and Seymour (1990) showed that six
species of reptiles with brittle-shelled eggs exhibitedthe peaked pattern, and ten of thirteen reptilian species with parchment-shelled eggs exhibited a nonpeaked metabolic pattern, i.e.. seven species snake foran exponential pattern, and three species sea turtles of
those for a sigmoid pattern, and other three species
fresh turtles of those are only a peaked pattern. Why

does G. japonicus, with a non-parchment-shelled egg.
also exhibit an exponential pattern?
there are

Unfortunately,

few data dealing with the reasons for theobserved patterns of embryonic metabolic ontogeny

Besides this phylogenetic difference, another pos-T.

parchment-shelled and whensuitable substrates, tend to become larger

septentrionalis

placedin

may be related to theare

during incubation because of water absorption. Theenlarged eggs of T. septentrionalis have a surface area

hatching that reached 282.7% of initial eggshellThis possible increase in pore diamearea (Table).

at1terand shell permeability (Packard. 1980) may pro-mote increased embryonic metabolism.
Both the metabolic rates per hatchling and egg at
pipping were nearly the same. The resting metabolic
rate of new hatchlings can be used to estimate metabolic rates of their eggs just before pipping.

The rest-Some data suggest

ing metabolic rate of hatchlings of T. septentrionalisthat the patterns of embryonic metabolic ontogeny in

was about 29.7% higher than that of G. japonicus.
The difference in resting metabolic rates of new
hatchlings between the two species may be due toin reptiles, especially in lizards.

reptiles may be species specific, but do not necessarily

depend upon the type of eggshell. For example, there
are three patterns of embryonic metabolic ontogeny

amongreptiles

withparchment-shelled eggs.

i.e..

peaked, sigmoid, and exponential pattern (Whiteheadand Seymour, 1990). However, all of seven snakes

examined exhibited an exponential pattern of embryonic metabolic ontogeny, three sea turtles showed asigmoid pattern, and three crocodilians and seven
freshwater turtles exhibited a peaked pattern. Metabolic rates of developing embryos reflect the energetic

demands of both growth and maintenance (Wang et

phylogenetic characteristics, as geckos have a low
metabolism (Feder and Feder. 1981: Dunson andBramham.

1982).

To eliminate

the effect ofbody

mass on metabolic rate, we used the formula M/W
to correct the results, where M is metabolic rate,

W7^
isclose to the average of theandhas the advantage of corcoefficientinterspecies

body mass, and 0.73

isrecting for difference in mass.

The corrected resting

metabolic rates of hatchlings are 0.4768 ml* h for T.

septentrionalis and 0.2942 ml/W

2/W°073 *hal.. 1991). Peaked and sigmoid patterns of embryonicmetabolic rates are likely to be associated with defin-for G. japonicus; the former species is 31.1% higher

ing embryonic growth rates late in incubation, andthan the latter.

exponential patterns of metabolic rate in reptilian
embryos is likely due to continuous increase of theof hatchlings between the two species is not primarily

embryonic growth rate through incubation.
Although G. japonicus had a longer incubation
period than did T. septentrionalis, the former species

consumed less oxygen through incubation. The total

2

We conclude that the difference in metabolic rates
caused by difference in body mass. Instead, there
must be an interspecific difference in metabolic rates

between the two lizard species.

1997

Asiatic Herpetological ResearchVol. 7. p. LSI

Sinica (in Chinese, with English abstract) 37(2): 185-Acknowledgments

192.

This work was supported by National Natural Science

Funds of China and Natural Science Funds of the
Educational Committee of China.
thankWe would like toMuth. Dr. Gary C.

AllanDr.

Packard.

Dr.

Michael B. Thompson. Dr. Shoji Tokunaga, and Dr.
William A. Dunson for providing literature.
Wewould also like to thank Prof. Roger S. Seymour andErmi Zhao for their comments onProf.

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