Content uploaded by Chloe Adamopoulou
Author content
All content in this area was uploaded by Chloe Adamopoulou on May 05, 2014
Content may be subject to copyright.
䉷
2000 by the American Society of Ichthyologists and Herpetologists
Copeia, 2000(2), pp. 610–614
Small Clutch Size in a Mediterranean Endemic Lacertid
(Podarcis milensis)
C. A
DAMOPOULOU AND
E. D. V
ALAKOS
The reproductive strategy of Podarcis milensis exhibits some peculiarities when
compared with other congeners. Males and females attain sexual maturity at a min-
imum body size of 47 and 42 mm SVL, respectively, both at an age of about one
year. Podarcis milensis has a very small clutch size, with a mean of 1.73 and a range
of 1–3 eggs, and produces multiple clutches annually. Both sexes exhibit a pro-
longed reproductive period extending from January to August.
M
EMBERS of the family Lacertidae are
widespread in the Old World, being dis-
tributed over Europe, Africa, and parts of Asia.
The family comprises over 230 specieswhich are
assigned to about 30 genera (Arnold, 1989). Re-
productive traits of European lacertids, espe-
cially from the western Mediterranean region,
have been well documented by various authors
(Pollo and Pe´rez-Mellado, 1990; Castilla et al.,
1991; Carretero and Llorente, 1997), whereas
life-history information on lizards occurring in
the eastern Mediterranean are poorly known
and for only a few species (Chondropoulos and
Lykakis, 1983; Valakos, 1990).
In this paper, we describe the unusual repro-
ductive cycle of Podarcis milensis, a lizard endem-
ic to the Aegean Archipelago (Greece). This
knowledge is valuable for its conservation and
protection, since the species is the only small
lacertid in the area.
M
ATERIALS AND
M
ETHODS
Species.—Podarcis milensis is restricted to the Mi-
los Island group (Milos, Kimolos, Polyaigos, An-
timilos, and islets). It is a small but robust lizard
with a characteristic blue color pattern in males.
The species remains active all year. It is mostly
a ground dweller, exhibiting dense populations
both in open sandy areas such as sand dunes
and in cultivated land.
Study area and climate.—The study area is located
in the center of Milos Island (24
⬚
22
⬘
E,36
⬚
40
⬘
N),
in a sandy coastal area between the sea and
Lake Achivadolimni. Vegetation consists almost
entirely of Thymus sp. and Juniperus oxycedrus
ssp. macrocarpa. Podarcis milensis is extremely
abundant and uses the small bushes of the area
for shelter. The climate is considered semiarid
Mediterranean, with annual rainfall varying
from 0 to 200 mm. A dry season exists from May
through October. The annual temperature, ac-
cording to the meteorological station on the is-
land, ranges from 10 C to 26 C (min
⫽
8,max
⫽
31.5 ). However, in the study area, the air
temperature in summer reaches 37–38 Cat mid-
day.
Field and laboratory methods.—A total of 341 adult
lizards (218 females and 123 males) were in-
cluded in the study, all coming from Milos Is-
land. Of these, 182 animals came from museum
collections, whereas the remaining 159 came
from the study site. After capture, specimens
were weighed to the nearest 0.1 g with a Pesola
balance and processed immediately. In the lab-
oratory, the following measurements were taken
for each specimen: SVL (to 1 mm), longest and
shortest axes of the right testis, number and di-
ameter of ovarian follicles and number, length
and width of oviductal eggs. Female sexual ma-
turity was assessed by the presence of enlarged
vitellogenic follicles (more than 3 mm in di-
ameter) or oviductal eggs, whereas the simul-
taneous presence of large vitellogenic follicles
and oviductal eggs was considered evidence for
multiple clutches. The size at sexual maturity
for males was estimated by the presence of sec-
ondary sexual characters such as the character-
istic light blue color of the throat. All field spec-
imens were deposited at the Zoological Muse-
um of the University of Athens. The same mea-
surements were taken for museum specimens
previously collected (see Materials Examined).
The mean length of the nine eggs deposited in
the laboratory was 15.3 mm (range
⫽
14–18,
S.D.
⫽
1.11) and the mean width 8.0 mm
(range
⫽
7–9, S.D.
⫽
0.64). Only eggs matching
or exceeding these parameters were used in es-
timating egg size and volume from preserved
animals. Estimates of testis and egg volumewere
obtained using the formula for the volume of
an ellipsoid.
Age classes for females were determined by
the von Bertalanffy equation and were as follows
(Adamopoulou, 1999): (1)
⬍
44 mm SVL; (2)
44
ⱕ
SVL
⬍
53 mm; (3) 53
ⱕ
SVL
⬍
57 mm;
611ADAMOPOULOU AND VALAKOS—PODARCIS REPRODUCTION
Fig. 1. Annual variation of testis volume:SVL ratio
in adult males of Podarcis milensis. Sample size is in-
dicated above each month.
T
ABLE
1. P
ERCENTAGE
(%)
OF
S
EXUALLY
M
ATURE
Podarcis milensis F
EMALES OF
E
ACH
C
LASS
H
AVING
1, 2,
OR
3
E
GGS PER
C
LUTCH
. Mean SVL, mean clutch size, and mean egg length for each class (with range and SD) are
shown in the first three columns. The sample size for each class is given in parentheses.
Age class Mean SVL (mm) Mean clutch size Mean egg length (mm)
Clutch size
1
2
(%) 3
I (17) 42.6, (42–3.5), SD
⫽
0.55 1.66, (1–2), SD
⫽
0.57 15, SD
⫽
0 33.3 66.7 —
II (129) 48.6, (44–52), SD
⫽
2.47 1.72, (1–3), SD
⫽
0.58 16.2, (14–20), SD
⫽
1.49 34.7 58.7 6.6
III (54) 54.5, (53–56.5), SD
⫽
1.06 1.77, (1–3), SD
⫽
0.74 15.4, (14–18), SD
⫽
1.12 41 41 18
IV (18) 58.0, (57–61), SD
⫽
1.07 1.66, (1–3), SD
⫽
0.7 18.0, (17–21), SD
⫽
1.77 44.4 44.4 11.2
and (4)
ⱖ
57 mm. We determined the time of
hatching and SVL of hatchlings in the field by
the presence of a ventral navel scar (Gala´n,
1996).
Comparisons between the two samples (mu-
seum and field specimens) were made using
analysis of covariance (ANCOVA) with SVL as
the covariate. The relationships between clutch
size, female body size, and mean egg volume
were examined using linear regression analyses,
whereas monthly changes in testis/SVL ratio
were assessed using analysis of variance (ANO-
VA).
R
ESULTS
In general, P. milensis males are larger than
females. In our sample, the mean SVL for adult
males was 56.7 mm (range
⫽
47–68, SD
⫽
4.7,
n
⫽
123), and the mean SVL for adult females
was 50.4 mm (range
⫽
42–61, SD
⫽
4.42, n
⫽
218).
Testing the two samples.—We found no significant
differences between museum and field speci-
mens in clutch size (F
(1,123)
⫽
2.20, P
⬎
0.05),
egg length (F
(1,59)
⫽
0.81, P
⬎
0.05), egg width
(F
(1,79)
⫽
0.24, P
⬎
0.05), mean egg volume
(F
(1,53)
⫽
1.15, P
⬎
0.05), number of large vitel-
logenic follicles (F
(1,26)
⫽
0.02, P
⬎
0.05), or tes-
tis volume (F
(1,120)
⫽
0.5, P
⬎
0.05). Therefore,
the two samples were pooled together for fur-
ther analysis.
Males.—Minimum size at sexual maturity was
found to be 47 mm SVL. Testes exhibit their
maximum volume in January and February. Af-
ter a period of stability at slightly smaller sizes
from March to May, testes volume decreased in
June and reached minimum size in July, with
recrudescence beginning in August. A second
gradual decrease in testes volume began in No-
vember and continued through December, fol-
lowed by a rapid increase to maximum values
in January (Fig. 1). There was a significant dif-
ference between months in testes volume/SVL
ratio (ANOVA, F
(9,113)
⫽
3.63, P
⬍
0.05).
Females.—The smallest reproductive female
measured 42 mm SVL which, according to our
estimations, was reached by most females at the
age of 12 months. The mean clutch size (based
on oviductal eggs) was 1.73 (range
⫽
1–3, SD
⫽
0.64, CV
⫽
0.36, n
⫽
126). The mean second
clutch size was 1.27 (range
⫽
1–3, SD
⫽
0.53, n
⫽
29) and was significantly different from the
first one (t-test, t
⫽
3.56, P
⬍
0.05). The average
egg length was 16.1 mm (range
⫽
14–21, SD
⫽
1.521, CV
⫽
0.09, n
⫽
62) and the average egg
width 8.2 mm (range
⫽
7–11, SD
⫽
0.738, CV
⫽
0.09, n
⫽
82). According to our field obser-
vations, the first hatchlings appear at the end of
April and the last at the end of September. They
have an SVL of 24–31 mm.
Females of all age classes did not differ in
clutch size (F
(3,122)
⫽
0.927, P
⬎
0.05), number
of enlarged vitellogenic follicles (F
(2,26)
⫽
1.551,
P
⬎
0.05), or width of oviductal eggs (F
(3,78)
⫽
1.065, P
⬎
0.05). There was a significant differ-
ence between age classes in egg length (F
(3,58)
⫽
3.795, P
⬍
0.05); larger females of class 4 car-
ried the longest eggs of all female age classes
(Table 1).
In Figure 2, the percentage of sexually ma-
612 COPEIA, 2000, NO. 2
Fig. 2. Seasonal variation in the percentage of sex-
ually mature females in Podarcis milensis (n
⫽
218).
Females with (A) oviductal eggs, (B) oviductal and
large vitellogenic follicles (
⬎
3 mm), (C) large vitel-
logenic follicles (
⬎
3 mm), (D) without reproductive
activity.
T
ABLE
2. R
EPRODUCTIVE
P
HENOLOGY OF
E
ACH
F
EMALE
A
GE
C
LASS IN
Podarcis milensis. Reproductive season was
estimated by the first and last appearance of oviductal eggs whereas evidence for later clutches was given by
the simultaneous presence of oviductal eggs and large vitellogenic follicles. The sample size is given in paren-
theses.
Female classes
Reproductive season
according to the presence of
oviductal eggs Evidence for later clutches
I (17) May —
II (129) April–July April, May, June, July
III (54) January–July April, May, June
IV (18) January–August February, March, May, June, August
ture females with or without reproductive activ-
ity is plotted for each month from January on-
ward with a peak in May and a gradual decline
toward August. In May, almost 90% of the fe-
males in our sample were reproducing.
The smallest females start their reproductive
activities in May (Table 2). It seems that they
have no second clutch, although this may be
due to the small sample examined. Females of
the second class, which represents the majority
of the population, have large vitellogenic folli-
cles from March onward, whereas we have evi-
dence for further clutches in April to July. The
larger females of the third and fourth age class
start their reproductive activity in January and
end in August. Females of the fourth age class
carry eggs from February to August. Beginning
in October, all females were reproductively in-
active. The simultaneous occurrence of oviduc-
tal eggs and enlarged vitellogenic follicles dur-
ing most months of the reproductive season
confirms that at least a proportion of individual
females produce at least two clutches per year.
There was no significant correlation between
clutch size and female SVL (r
⫽
0.09, R
2
⫽
0.008, P
⬎
0.05) or female SVL and mean egg
volume (r
⫽
0.152, R
2
⫽
0.023, P
⬎
0.05), but
mean egg volume was significantly inversely cor-
related with clutch size (r
⫽⫺
0.475, R
2
⫽
0.225,
P
⬍
0.05).
D
ISCUSSION
Podarcis milensis, compared to other Podarcis
species, exhibits an exceptionally small clutch
size in combination with the capability of pro-
ducing more than one annual clutch. Bauwens
and Dı´az-Uriarte (1997) analyzed patterns of
lacertid life-history variation and proposed that
species within this clade can be arranged along
a single, multivariate axis. Podarcis milensis clear-
ly is placed at one end of this continuum as a
small-sized species that matures early and has
small clutches of relatively large young, multiple
broods per year, and a short adult lifespan.
The species displays a prolonged reproduc-
tive period extending from January to the end
of summer. During both years of this study,
large females were seen either pregnant or cop-
ulating in January. Males P. milensis exhibit a re-
productive cycle synchronized with that of fe-
males. Podarcis milensis is the first European lac-
ertid to our knowledge having such an extensive
breeding season and small clutch size. Other
Mediterranean Podarcis species studied (P. erhar-
dii, Naxos Island, Valakos, 1990; P. taurica, Io-
nian archipelago, Chondropoulos and Lykakis,
1983; P. bocagei, Iberian peninsula, Gala´n, 1996;
P. pityusensis, northeast Spain, Carretero et al.,
1995; P. atrata, Columbretes islands, Bauwens
and Dı´az-Uriarte, 1997) have shorter breeding
seasons, larger clutch sizes, and larger SVLs at
reproductive maturity.
The fact that no significant relationship be-
tween SVL and either clutch size or mean egg
volume was found implies that P. milensis has
reached an evolutionarily optimum egg volume
and clutch size, showing no increase in the two
variables with an increase in body size. The neg-
ative correlation between mean egg volume and
613ADAMOPOULOU AND VALAKOS—PODARCIS REPRODUCTION
clutch size may reflect the extent to which fe-
male P. milensis ‘‘burden’’ themselves with eggs.
For example, the space available for eggs in the
body cavity of females may place an upper limit
on their volume (Shine, 1992). To avoid pro-
ducing nonviable eggs or hatchlings, females
must increase egg size at the expense of clutch
size.
It seems that for some reason P. milensis has
evolved a low and quite invariable clutch size,
producing large eggs in relation to those of oth-
er lacertids for which data are available. Never-
theless, small clutch size may not be an adap-
tation but the consequence of selection on oth-
er life-history parameters such as large offspring
size. Larger eggs produce larger young which in
turn have a survival advantage over smaller ones
(Ferguson and Fox, 1984; Sinervo, 1990). If this
is the case in P. milensis, high intraspecific com-
petition might increase selection for large eggs
with the potential for enhanced offspring sur-
vival rather than larger clutch size. Population
density at the study site reaches a level of 550–
600 animals/ha (Adamopoulou, 1999), which is
considered high, the consequences of which are
manifested in at least two ways.First, adultmales
have been seen expressing aggressive behavior
toward juvenile males both in the laboratory
and in the field, even killing them instantly by
neck biting when put together. Second, canni-
balism (whole hatchlings in the stomach) has
been detected in adult males. Alternatively, the
effect of high predation on adult lizards might
result in selection for early reproduction (Gadg-
il and Bossert, 1970), which is associated with
small clutch size and more than one clutch per
season (Tinkle et al., 1970). Indeed, adult P. mil-
ensis are exposed to a similar array of predators
as are continental species (Pe´rez-Mellado et al.,
1997), including birds of prey and three species
of snakes such as the Blunt-Nosed Viper Macro-
vipera schweizeri, 21.4 % of the diet of which con-
sists of P. milensis (Adamopoulou et al., 1997).
On the other hand, low clutch number is as-
sociated in this species with the potential for
frequent ovipositions, which is favored by weath-
er conditions that probably favor the extension
of the reproductive season. In winter, individual
P. milensis take advantage of numerous sunny
days to bask, since the air temperature in the
sand dune of Achivadolimni reaches 20 C in
January and February.
To summarize, we cannot offer a single ex-
planation for the evolution of low clutch size in
P. milensis. However, considering the ability of
the species to produce multiple clutches, the
most plausible mechanism for producing more
offspring may be to increase clutch frequency,
thus spacing clutches temporally and spatially.
Selection may have favored the evolution of op-
portunistic reproductive behavior in females, in
which energy is invested not in the number or
size of eggs per clutch but in their frequency,
thus taking complete advantage of favorable cli-
matic conditions within the constraints of age
and physiological state. The extended isolation
of the Milos Islands group (since the upper
Pleistocene; Papanikolaou and Dermitzakis,
1981) may have enabled P. milensis to develop a
more efficient reproductive strategy than the
other Podarcis species of the Aegean with regard
to the special climatic conditions of insular
Mediterranean-type ecosystems.
M
ATERIAL
E
XAMINED
Institutional abbreviations are as listed in Lev-
iton et al. (1985). The specimen number is fol-
lowed by the collecting locality and the month
and year of collection as noted on the labels:
ZMFK 1657–1711, ZMFK 1742–1801 (Milos, 5/
1953), ZMFK 30999–31030 (Milos, 6/1956),
NMW 15257:1–15257:29 (Milos, 5/1954), NMW
24035:6–24035:14 (Milos, 7/1979), NMW 11
452:1–11452:11 (Milos, 7/1932).
A
CKNOWLEDGMENTS
We thank W. Bo¨hme [Herpetological Collec-
tion of the Alexander Koenig Zoological Insti-
tute and Museum (Bonn, Germany)] and F. Tie-
demann and H. Grillitsch (Naturhistorisches
Museum of Wien) who kindly allowed us to ex-
amine Podarcis milensis specimens. We also thank
two anonymous reviewers for their useful com-
ments. This study was supported by the General
Secretariat for Research and Technology, proj-
ect 1298/95ED. The collection of specimens
was carried out according to Presidential De-
cree 67/81.
L
ITERATURE
C
ITED
A
DAMOPOULOU
, C. 1999. Structure and function of
epigeic animal communities with emphasis in the
lizard Podarcis milensis (Sauria: Lacertidae), in in-
sular ecosystems of the Aegean. Unpubl. Ph.D.
diss., Univ. of Athens, Athens, Greece.
,E.D.V
ALAKOS
,
AND
A. L
EGAKIS
. 1997. Notes
on the diet and reproduction of the Cycladesblunt-
nosed viper Macrovipera schweizeri (Werner, 1935).
Herpetozoa 10:173–175.
A
RNOLD
, E. N. 1989. Towards a phylogeny and bio-
geography of the Lacertidae: relationships within
an Old World family of lizards derived from mor-
phology. Bull. Brit. Mus. (Nat. Hist.) 55:209–257.
B
AUWENS
, D.,
AND
R. D
I
´
AZ
-U
RIARTE
. 1997. Covariation
614 COPEIA, 2000, NO. 2
of life-history traits in lacertid lizards: a comparative
study. Am. Nat. 149:91–111.
C
ARRETERO
,M.A.,
AND
G. A. L
LORENTE
. 1997. Repro-
duction of Psammodromus algirus in coastal sandy ar-
eas of NE Spain. Amphib.-Reptilia 18:369–382.
, ,X.S
ANTOS
,
AND
A. M
ONTORI
. 1995.
Caracterı´sticas reproductoras de una poblacio´n in-
troducida de Podarcis pityusensis. Rev. Esp. Herpetol.
9:93–102.
C
ASTILLA
, A. M., L. J. B
ARBADILLO
,
AND
D. B
AUWENS
.
1991. Annual variation in reproductive traits in the
lizard Acanthodactylus erythrurus. Can. J. Zool. 70:
395–402.
C
HONDROPOULOS
,B.P.,
AND
J. J. L
YKAKIS
. 1983. Ecol-
ogy of the Balkan wall lizard Podarcis taurica ionica
(Sauria: Lacertidae) from Greece. Copeia 1983:
991–1001.
F
ERGUSON
,G.W.,
AND
S. F. F
OX
. 1984. Annual varia-
tion of survival advantage of large juvenile side-
blotched lizards, Uta stansburiana: its causes and
evolutionary significance. Evolution 38:342–349.
G
ADGIL
,M.,
AND
W. H. B
OSSERT
. 1970. Life history
consequences of natural selection. Am. Nat. 104:1–
24.
G
ALA
´
N
, P. 1996. Sexual maturity in a population of
the lacertid lizard Podarcis bocagei. Herpetol. J. 6:87–
93.
L
EVITON
, A. E., R. H. G
IBBS
J
R
., E. H
EAL
,
AND
C. E.
D
AWSON
. 1985. Standards in herpetology and ich-
thyology. Part I. Standard symbolic codes for insti-
tutional resource collections in herpetology and
ichthyology. Copeia 1985:802–821.
P
APANIKOLAOU
,D.J.,
AND
M. D. D
ERMITZAKIS
. 1981.
The Aegean Arc during Burdigalian and Messinian:
a comparison. Riv. Ital. Paleont. 87:83–92.
P
E
´
REZ
-M
ELLADO
, V., C. C
ORTI
,
AND
P. L
O
C
ASCIO
. 1997.
Tail autotomy and extinction in Mediterranean liz-
ards. A preliminary study of continentaland insular
populations. J. Zool. Lond. 243:533–541.
P
OLLO
,C.J.,
AND
V. P
E
´
REZ
-M
ELLADO
. 1990. Biologı´a
reproductora de tres especies Mediterra´neas de
Lacertidae. Mediter. Ser. Biol. 12:149–160.
S
HINE
, R. 1992. Relative clutch mass and body shape
in lizards and snakes: is reproductive investment
constrained or optimized? Evolution 46:828–833.
S
INERVO
, B. 1990. The evolution of maternal invest-
ment in lizards: an experimental and comparative
analysis of egg size and its effects on offspring per-
formance. Ibid. 44:279–294.
T
INKLE
, D. W., H. M. W
ILBUR
,
AND
S. G. T
ILLEY
. 1970.
Evolutionary strategies in lizard reproduction. Ibid.
24:55–74.
V
ALAKOS
, E. D. 1990. The ecology of the lizard Po-
darcis erhardii in a typical insular ecosystem on Nax-
os island. Unpubl. Ph.D. diss., Univ. of Athens, Ath-
ens, Greece.
(CA) U
NIVERSITY OF
A
THENS
,D
EPARTMENT OF
B
I
-
OLOGY
,Z
OOLOGICAL
M
USEUM
,P
ANEPISTIMIOU
-
POLIS
157 84, A
THENS
,G
REECE
;
AND
(EDV)
U
NIVERSITY OF
A
THENS
,D
EPARTMENT OF
B
I
-
OLOGY
,S
ECTION OF
A
NIMAL AND
H
UMAN
P
HYS
-
IOLOGY
,P
ANEPISTIMIOUPOLIS
157 84, A
THENS
,
G
REECE
.P
RESENT ADDRESS
: (CA) B
IOLOGY
D
E
-
PARTMENT
,E
ARTH AND
M
ARINE
S
CIENCES
B
UILDING
D324, U
NIVERSITY OF
C
ALIFORNIA
,
1156 H
IGH
S
TREET
,S
ANTA
C
RUZ
.C
ALIFORNIA
95064. E-mail: (CA) chloe@biology.ucsc.edu;
and (EDV) evalakos@biology.db.uoa.gr. Send
reprint requests to CA. Submitted: 23 Sept.
1998. Accepted: 8 Aug. 1999. Section editor:
A. H. Price.
