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Annual Reproductive Cycle in the Scincid Lizard Chalcidesviridanus from Tenerife, Canary IslandsAuthor(s): Paula Sánchez-Hernández , Miguel Molina-Borja , and Martha P. Ramírez-PinillaSource: Current Herpetology, 38(2):170-181. 2013.Published By: The Herpetological Society of JapanURL: http://www.bioone.org/doi/full/10.5358/hsj.32.170

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doi 10.5358/hsj.32.170Current Herpetology 32(2): 170–181, August 2013

© 2013 by The Herpetological Society of Japan

Annual Reproductive Cycle in the Scincid Lizard Chalcides

viridanus from Tenerife, Canary Islands

PAULA SÁNCHEZ-HERNÁNDEZ1

, MIGUEL MOLINA-BORJA1

*,

AND MARTHA P. RAMÍREZ-PINILLA2

1

Grupo de Investigación “Etología y Ecología del Comportamiento”, Depto. Biología

Animal, Universidad de La Laguna, Tenerife, Islas Canarias, ESPAÑA

2

Laboratorio de Biología Reproductiva de Vertebrados, Grupo de Estudios en

Biodiversidad, Escuela de Biología, Universidad Industrial de Santander, Bucaramanga

COLOMBIA

Abstract: Chalcides viridanus is a small skink endemic to Tenerife, the Canary

Islands. This paper describes its annual reproductive cycle and sexual dimor-

phism by use of data from external measurements, dissection, and histological

observation of gonads from monthly samples. Males were significantly larger

than females in head–forelimb length, distance between forelimbs and hind

limbs, tail width, and body mass. Male testes were largest in March, when most

individuals showed active spermiogenesis, although no spermiation was

observed. In April, the testes were somewhat smaller but showed seminiferous

tubules and epididymis ducts with abundant sperm. In this month, female

gonads and ovarian follicles were significantly enlarged, and vitellogenesis was

evident. Oviductal embryos were found in May and June, and parturition took

place at the beginning of August. Both testis mass in males and diameter of the

largest oocyte in females were significantly correlated to abdominal fat body

mass. We conclude that in C. viridanus both sexes exhibit seasonal changes in

gonadal activity with synchronous development of both male and female

gonads in the spring months.

Key words: Scincidae; Chalcides viridanus; Canary Islands; Reproductive cycle;

Viviparity

INTRODUCTION

Knowledge of reproductive cycles and life-

history traits in lizards is important both from

a comparative point of view to understand

their evolutionary processes (Dunham and

Miles, 1985; Bauwens and Díaz-Uriarte, 1997;

Mouton et al., 2012) and from a proximal

causal approach to elucidation, for example,

of responsible environmental factors (Ruben-

stein and Wikelski, 2003; Carretero, 2006).

Viviparity has supposedly originated on more

than 108 separate occasions within the Squa-

mata (Blackburn, 1999), and has often evolved

relatively recently (Heulin and Guillaume,

1989; Camarillo, 1990).

* Corresponding author. Tel: 34–922–31–83–41;

Fax: 34–922–31–83–11;

E-mail address: [email protected]

SÁNCHEZ-HERNÁNDEZ ET AL.—REPRODUCTIVE CYCLE IN SKINK 171

In several lizard clades of temperate regions,

evolution of viviparity has been accompanied

by a shift from spring to autumn gametogene-

sis (Ramírez-Pinilla, 1991; Guillette and

Méndez-de la Cruz, 1993; Mouton et al.,

2012). Irrespective of the reproductive mode

(oviparous or viviparous), most lizards from

temperate and subtropical zones worldwide

reproduce seasonally with ovulation occurring

in spring, and appearance of hatchlings or

neonates in summer and autumn months

(James and Shine, 1985; Zug et al., 2001).

However, several other viviparous lizards

(phrynosomatids, liolaemids, cordylids) ovulate

in autumn and are gravid during winter

months with parturition occurring during the

next spring (Fitch, 1970; Ramírez-Pinilla,

1991; Guillette and Méndez-de la Cruz, 1993;

Ramírez-Pinilla et al., 2009; Mouton et al.,

2012). On the other hand, viviparous species

in aseasonal environments (i.e., tropical regions)

may be able to continually reproduce through-

out the year (Fitch, 1970; Hernández-Gallegos

et al., 2002; Ramírez-Pinilla et al., 2002), or

may show a markedly discontinuous, seasonal

pattern (Vitt and Blackburn, 1983; Méndez de

la Cruz et al., 1999).

The scincid lizards of the genus Chalcides

Laurenti, 1768 include 25 viviparous species,

differing mainly in the degree of body elonga-

tion and limb reduction (Caputo et al., 1995).

They are mainly distributed in the North

Temperate Zone in Southern Europe and

North Africa (Pasteur, 1981; Caputo et al.,

1995; Mateo et al., 1995). The reproductive

phenology has been studied for some species,

revealing that mating occurs from March to

May after hibernation, and neonates appear

from May to August (C. chalcides: Rugiero,

1997; C. bedriagai: Galán, 2003; C. lanzai:

Bogaerts, 2006). Similar patterns have also

been reported for a few other species within

the genus (Salvador, 1985; Schleich et al.,

1996; Spawls et al., 2004), but their compre-

hensive reproductive cycles have not been

described.

In the Canary Islands, a subtropical volcanic

archipelago, this genus has four endemic

species: C. sexlineatus (Gran Canaria), C.

simonyi (Fuerteventura and Lanzarote), C.

coeruleopunctatus (La Gomera and El

Hierro), and C. viridanus (Tenerife and La

Palma) (Báez, 1998; Carranza et al., 2008).

Chalcides viridanus, originally described by

Gravenhorst (1851), is at the base of a western

clade of the genus (Carranza et al., 2008) and

their biological data were revised by Báez

(1998), and is distributed throughout the two

islands, including high altitudes such as the

peak area of Teide volcano (3718 m asl:

Klemmer, 1976). Chalcides viridanus is a

small, diurnal secretive skink that lives under

bushes and stones or inside stone walls. Indi-

viduals are not easily observed in exposed

areas except at midday from March to May

(the authors’ unpublished observations). The

species is viviparous as are other congeners,

and shows morphological variation between

sexes, and within and between islands (Báez

and Thorpe, 1990; Brown et al., 1993). Adult

females may have two to four neonates per

season, and parturition occurs in July and

August. In the present study, we performed a

morphometric comparison and histological

examination of the gonads of male and female

C. viridanus. This is the first description of

complete year-round changes of the gonads in

this species.

MATERIAL AND METHODS

Environment data and specimen collection

We collected skinks in two field sites with

similar habitats and weather characteristics

close to La Laguna city (Geneto, 28°28'476'' N

16°18'976'' W and Los Baldíos, 28°27'52''N

16°19'29''W). Figure 1 shows the monthly

variation of mean temperature and precipita-

tion during 2009 at Los Baldíos meteorologi-

cal station (La Laguna, Tenerife, 28°28'16''N

16°19'43''W), situated at 638 m asl, next to the

catch zone; maximum air temperature

occurred between July and September, and

highest monthly precipitation occurred between

November and March. Drought occurred

between May and October. Photoperiod in

172 Current Herpetol. 32(2) 2013

the Canary Islands changes between 10 to

14 hours of light from the beginning of

winter in December up to the beginning of

summer in June.

The habitats were characterized by small

shrubs and herbs (Lavatera cretica, Oxalis

pes-caprae, Spartium junceum, Rubus ulmi-

folius) together with stone walls and rock piles.

Skinks were captured by hand while they were

basking or by checking under stones. We

sampled individuals between December 2008

and December 2009, one to two days per week

of each month with the aim of collecting at

least ten individuals per month. Despite high

capture efforts in each month, we could only

capture eight skinks during July and August.

We included in our study only male and female

skinks with a minimum body size of 60 mm

because smaller individuals never had differen-

tiated gonads. We released juvenile skinks and

only used adult animals for our study.

Captured specimens were transported inside

cloth bags to the laboratory where they were

kept in individual terraria. These, in turn,

were placed inside small rooms where the

light-dark cycle and temperature were changed

gradually each month so as to simulate values

in the natural environment. Temperatures

inside the rooms ranged from 15°C in

December to 24°C in August and humidity

from 30% in August to 85% in December.

Most specimens were euthanized on the first

or second day after capture, but never more

than four days after capture. Euthanized

skinks were deposited in the Herpetological

Collection of the Department of Zoology

(Universidad de La Laguna) with the accession

numbers DZUL-1064 to DZUL-1180.

Analysis of sexual dimorphism

For each individual, the following measure-

ments were taken with digital calipers (precision

0.01 mm): snout-to-vent length (SVL), head

depth and width (HD, HW), pileus length (PL),

distance between forelimbs and hind limbs

(DFH), distance between left and right fore-

limbs (DFL), distance between right and left

hind limbs (DHL), forelimb length (FLL) hind

limb length (HLL), and tail depth and width

(TD, TW). Body mass (BM) was weighed with

a digital balance (0.1 g precision).

External morphometric variables provided

normality and homoscedasticity require-

ments, and after confirming that they were

linearly and significantly related to SVL,

multivariate analyses of variance (MANOVA

with sex as factor and SVL as covariate) were

applied to these data to test degree of sexual

dimorphism. Between sex and among month

comparisons of SVL were performed with two-

way ANOVA with sex and months as fixed

factors. Alpha level was always set at 0.05 and

Bonferroni correction for multiple compari-

sons was applied (Chandler, 1995).

Gonad morphometrics and reproductive

stages

After taking all biometric traits, and in order

to analyse histological aspects of gonadal

changes among months, specimens were

euthanized by intra peritoneal anesthesia

(1 ml of sodium pentobarbital at 20 mg/kg).

Afterwards, a ventral incision was made and

several internal parameters were taken for

each specimen: length of the largest ovarian

follicle, and length, width and mass of the

gonad and abdominal fat tissue (fat body

volume-FBV, mm3- was calculated using the

ellipsoid formula: (4/3)πa2b, where a and b

are the shortest and largest diameter, respec-

tively). To statistically analyse the data, we

FIG. 1. Annual variation of rains (left axis) and

temperature (right axis) from the study area. Data

correspond to our study year.


initially confirmed normality, homoscedastic-

ity and linearity requirements. After proving

that male testis and ovarian follicle sizes were

significantly related to SVL, ANCOVA was

applied within each sex to each parameter,

using the month as factor and SVL as

covariate. Female gonad mass was not used

because the linearity requirement was not

fulfilled. To explore the relationship of gonad

parameters and fat body volume with environ-

mental variables (precipitation and tempera-

ture), partial correlations were calculated

separately for males and females taking into

account the variation in SVL.

Male and female whole gonads were then

extracted and weighed, fixed in Bouin’s solu-

tion for 12 hours, washed in running water,

and stored in 70% ethanol. Subsequently, the

specimens were dehydrated, embedded in

paraplast, sectioned at 6 μm, and stained with

hematoxylin-eosin. In males, the reproductive

stage was determined according to the classifi-

cation of Ballinger and Nietfeldt (1989) as

follows: Stage 1: growing testes; stage 2: early

spermatogenesis, primary spermatocytes, no

lumen; stage 3: spermatogenesis, abundant

spermatocytes, some tubules with lumen; stage

4: spermiogenesis, undifferentiated spermatids

at luminal margin; stage 5: metamorphosing

spermatids at luminal margin; stage 6: repro-

ductive testis, mature sperm in seminiferous

tubules and epididymes; stage 7: postrepro-

ductive testes, early regression, mature sperm

at luminal margin and cellular debris in the

lumen, epididymes with abundant sperm; stage

8: postreproductive testis, later regression. In

females the reproductive stages were catego-

rized as stage 1: previtellogenic, oocytes <2 mm

in diameter; stage 2: vitellogenic, oocytes

>2.0 mm in diameter, yellowish; stage 3: preg-

nancy, oviductal eggs or embryos; stage 4:

postparturition, wide flaccid oviducts.

Reproductive stage data for each animal

permitted establishing the percentage of males

and females in each reproductive stage for

each month throughout the year. To detect

intra and inter sex variation by month (syn-

chrony) and over time (seasonality), we

employed a G-test of independence.

RESULTS

Number and SVL of specimens captured

We captured 116 specimens, 53 males and

63 females during the whole year and the num-

ber of collected individuals of each sex did not

change significantly from month to month

(G12

=4.85, P=0.96). SVL of males and females

did not differ significantly (F1,92

=2.31, P=0.13)

nor did they change significantly in any month

(F11,92

=1.82, P=0.062, Fig. 2); the interac-

tion of sex and month was not significant

(F11,92

=0.51, P=0.89). Figure 2 also shows

the gonad stages at which adult male and

female skinks were collected.

Sexual size dimorphism

Table 1 shows the statistical data for biomet-

FIG. 2. Monthly distribution of body sizes

(SVL) from 47 males (a) and 63 females (b) of

Chalcides viridanus during the sampling year,

showing gonad stages. A larger symbol for vitello-

genic females corresponds to more than one skink

with similar SVL.


ric traits measured in both sexes. MANOVA

analysis showed that, taking into account all

morphological variables, males and females

differed significantly (F11,96

=6.79, P<0.001)

in relation to SVL (F11,96

=15.01, P<0.001).

This difference was due to males having

significantly larger BM, HD, HW, PL, DHL,

HLL, TW and FBV than females (univariate

analyses within MANOVA, Table 1).

Reproductive data and monthly variation

Male and female gonads were reproductively

active in early spring (March and April); they

showed signs of regression during the summer

through early autumn (July and August to

October) and recrudescence beginning in

winter (December to January). Fat body vol-

ume followed a similar pattern in both sexes

(Figs. 3b and 4b).

There was a significant association between

the reproductive stage of each sex and the

month (G33

=65.59, P<0.001 females,

G66

=114.02, P<0.001 in males), females in

stage 2 (vitellogenic) only appeared during

April and in stage 3 (pregnancy) mainly during

June; parturitions must occur in August,

because in that month we found females with

hypertrophic and very convoluted oviducts,

signs of having given birth recently (stage 4).

In males, reproductive stage 5 was found in

March and April and reproductive stages 6

and 7 from May to June.

In our sample the smallest pregnant female

measured 70 mm and the smallest potentially

reproductive male had an SVL of 75 mm (Fig.

2). Individuals–males or females–smaller than

60 mm SVL did not have differentiated

gonads. Three of the females captured in May

were bigger than 70 mm, but they did not show

evidence of being vitellogenic or pregnant. All

females captured in June and July were

pregnant (Fig. 2).

There were significant regressions between

female or male SVL (or body mass) and gonad

TABLE 1. Sample sizes (N), and mean, standard error (SE), minimum (Min) and maximum values (Max)

of biometric traits (in mm and g) in male and female Chalcides viridanus examined, and the results of

statistical comparison of each trait between sexes. See text for further details. Trait abbreviations are as

follows: snout-to-vent length (SVL), head depth and width (HD, HW), pileus length (PL), distance between

forelimb and hind limb (DFH), distance between left and right forelimbs (DFL), distance between right and

left hind limbs (DHL), forelimb length (FLL), hind limb length (HLL), tail depth and width (TD, TW), body

mass (BM), and fat body volume (FBV, in mm3). Statistically significant P values are highlighted in bold.

Sex Males (N=53) Females (N=63) Intersex variation

Biometric

trait Mean SE Min Max Mean SE Min Max F P

SVL 80.71 0.79 65 90 82.5 0.98 65 98 2.31 0.13

BM 6.69 0.24 2.6 9.9 6.47 0.21 3.7 10.7 7.87 0.006

HD 5.28 0.1 3.6 7.45 4.97 0.7 3.48 6.29 15.33 0.000

HW 6.78 0.8 5.54 8.14 6.35 0.6 5.34 7.48 24.17 0.000

PL 10.29 0.12 8.67 12.69 9.62 0.11 7.62 11.71 31.74 0.000

DFH 51.78 0.77 35.94 60.61 54.48 0.67 42 68.87 2.15 0.16

DFL 5.26 0.1 3.61 6.92 5.19 0.1 3.59 7.27 1.38 0.24

DHL 7.16 0.13 4.44 9.14 6.95 0.1 5.38 8.89 8.26 0.005

FLL 18.53 0.32 13.69 24.17 18.48 0.27 14.05 26.7 0.05 0.81

HLL 12.67 0.19 9.79 15.97 12.12 0.15 9.09 15.04 5.64 0.02

TD 5.4 0.1 3.11 6.81 5.36 0.1 4.27 9.34 0.024 0.088

TW 6.25 0.1 4.34 8.67 6.04 0.08 4.53 7.47 7.1 0.009

FBV 22.33 3.53 0 98.54 10.71 1.44 0.02 71.6 11.76 0.001


parameters and fat body volume (Table 2).

Thus, there was a positive and significant rela-

tionship of body mass and testis mass, and of

female SVL and largest follicle diameter.

Therefore, to analyse the monthly variation in

these parameters, ANCOVA was applied to

adjust for the effect of SVL (or BM).

ANCOVA showed that there were significant

differences among months in the largest

follicle diameter (F11,51

=7.83 P<0.001) and

in female fat body volume (F11,48

=8.73,

P<0.001), their values being significantly

larger in April than in all the other months

(Figs. 3a and b). ANCOVA analysis also

showed that there was a significant difference

among months in testis mass (F11,38

=3.19,

P=0.005), values being larger in March and

April than in the other months (Fig. 4a); male

fat body volume also had higher mean values

in March and April (ANCOVA, F10,35

=2.69,

P=0.014) but post-hoc comparisons among

months did not show any significant difference

between them and the other months (Fig. 4b).

DISCUSSION

Sexual dimorphism

Taking into account that we intentionally

sampled a minimum number of skinks per

month, it is understandable that there was no

significant difference in the proportion of

males and females captured throughout the

year; however, adult males and females could

be captured each month and SVL did not sig-

nificantly change between months for any sex.

Mean SVL of females was slightly larger

FIG. 3. Means (±2SD) of follicular diameter

(a) and female fat body volume (b), in Chalcides

viridanus during the sampling months. Asterisks

indicate significant differences between the marked

and the other months.

FIG. 4. Means (±2SD) of testis mass (a) and

male fat body volume (b), in Chalcides viridanus

during the sampling months. Asterisks indicate

significant differences between the marked and the

other months (see text).


than mean SVL of males, but the difference

did not reach statistical significance. In Chal-

cides, the larger species of the C. chalcides

group (SVL>100 mm in adults, litter size up

to 19; grass swimming clade of Carranza et al.

2008), females are considerably larger than

males, whereas the small species (e.g. C.

polylepis, C. ocellatus, and C. mionecton) are

not dimorphic in body length (Caputo et al.,

2000) as in C. viridanus. Two hypotheses

explain sexual dimorphism in body size in

skinks, the intrasexual selection hypothesis (in

which females select for large males), and

fecundity advantage hypothesis (natural selec-

tion leading to larger body size in females)

(Thompson and Withers, 2005).

Similarly, female to male comparison of

distance between forelimb and hind limb

lengths did not reach significance in our

sample of C. viridanus; within Chalcides,

large snake-like species (C. chalcides and C.

striatus) are dimorphic in abdomen length

(larger in females) whereas short snake-like

and stout skinks are not dimorphic (C.

mionecton, C. ocellatus, and C. polylepis:

Caputo et al., 2000). Longer bodies in female

lizards probably reflect selection pressure

leading to more space available for embryos

inside the female body (Fitch, 1981; Vitt and

Blackburn, 1991).

Several selective pressures for each sex, and

even non-adaptive processes, have been

suggested as long term causes of the differing

pattern of sexual size dimorphism in different

species (Olsson et al., 2002; Cox et al., 2003,

2007); however, different growth rates for

males and females should also be considered

as short-term causes (Badayev, 2002).

Sexual dimorphism was more clearly mani-

fested in several head and body traits, males

having larger relative values than females as in

other skink species (e.g., Mabuya heathi and

M. frenata: Vitt and Blackburn, 1983; Vrcibradic

and Rocha, 1998; Niveoscincus coventryi:

Olsson et al., 2002; Clemann et al., 2004).

These differences can be interpreted in terms

of selection pressures acting on male traits

suitable for intrasexual interactions; head sizes

are commonly larger in winners than in losers

of male encounters in different lizard species

(Hews, 1990; Molina-Borja et al., 1998;

Gvozdik and Van Damme, 2003; Dubey et al.,

2011). Moreover, a larger head size in males

could have been selected in an intersexual

context as they usually continue biting the

female’s neck for a long time during mating

(Sánchez-Hernández et al., 2012). Neverthe-

less, female skinks also compete with other

females and may show agonistic interactions

as intense as among males (Sánchez-

Hernández et al., 2012). As there are no other

behavioural studies for species of Chalcides, it

TABLE 2. Regressions of gonadal traits to snout-vent length (for diameter of the largest follicle in

female) or body mass (for the other traits) in male and female Chalcides viridanus. Degrees of freedom are

given in parentheses below F values.

Sex Male Female

Variable R2

F P R2

F P

Gonad volume

(mm3)

0.09 4.57

(1, 45)

0.038 0.1 7.47

(1,61)

0.008

Gonad mass

(g)

0.21 13.01

(1, 49)

0.001

Diameter of the

largest follicle (mm)

0.08 5.24

(1, 60)

0.02

Fat volume

(mm3)

0.093 4.69

(1, 46)

0.035 0.10 7.47

(1, 61)

0.008

Body mass

(g)

0.6 73.49

(1, 50)

0.0001 0.52 66.78

(1, 61)

0.0001


is still difficult to interpret these dimorphic

traits in terms of intersexual and intrasexual

conflicts.

Size at sexual maturity

The individuals collected had differentiated

gonads from 60 mm SVL on, and the smallest

pregnant female and the smallest potentially

reproductive male had an SVL of 70 and

75 mm, respectively. Therefore, this means

either that individuals smaller than 70–75 mm

SVL were immature or that they could not

reproduce that year. As we do not currently

have data on growth rates, we cannot specify

ages at which sexual maturity occurs. In other

Chalcides of similar body sizes, females may

ovulate at a mean SVL of 82.7 mm (Chalcides

bedriagai: Galán, 2003), and Chalcides lanzai

in captivity have their first clutch at four years

of age. In southeast populations of C. bedria-

gai, sexual maturity is attained at 57–61 mm

SVL (López-Jurado et al., 1978) while in

northwest populations of this species sexual

maturity is reached at about 73–74 mm SVL

(Galán, 2003). Therefore, if we consider a

SVL of 70 mm as the potential size of sexual

maturity for females, C. viridanus would be

placed between the two Iberian populations

just mentioned. We cannot currently ascertain

how long they will take after birth to arrive at

the size of sexual maturity. As three adult

females were not vitellogenic nor pregnant in

the first appropriate month (May), some

individuals may delay ovulation or do not

reproduce every year.

Newborns were only obtained from two

females (before being euthanized), but our

unpublished data showed that they (1 to 3 per

female) had mean SVL of 35.05 mm (±1 SE,

ranging 31.3–39.3 mm). This means that to

attain the size of sexual maturity skinks

should, at least, double their size at birth. We

cannot currently ascertain if there is a relation-

ship between female SVL and number of

offspring because of the small sample size.

Other Chalcides skinks with similar SVL have

clutches of 1–6 (C. bedriagai: Pollo, 2003) or

2–3 offspring (C. sexlineatus: Harbig, 2000)

and have newborn sizes similar to those of C.

viridanus. Furthermore, C. sexlineatus may

begin to reproduce at an age of 24 months

(Harbig, 2000). Taking into account the close

phylogenetic vicinity to the latter species, we

can expect a similar time for first reproduction

in C. viridanus.

Annual reproductive cycle

We have shown that the highest gonadal

development in male and female C. viridanus

occurred during March and April (moderate

temperature increase in springtime) (Figs. 1

and 4). The lowest gonadal size appeared in

the summer months for both sexes. Therefore,

reproductive activity is markedly seasonal in

this species, both sexes are synchronic in

their gonadal development, and mating and

fertilization should occur in April; in fact,

behavioural observations in the laboratory

showed mating during that month (Sánchez-

Hernández et al., 2012). However, males in

stages 7 and 8 during June still might be able

to fertilize females, as they have abundant

sperm in their ducts.

Both sexes of C. viridanus emerge from

winter hibernation during March when tem-

peratures begin to rise and they can be

observed basking in sunny patches on the

ground or on stones, sometimes in pairs. The

onset of testicular activity and follicular

growth is related with increasing ambient

temperatures during March. As shown in Figs.

3 and 4, ovulation and mating must occur in

April, pregnancy during the hottest summer

months, and parturition in August at the end

of summer. Consequently, reproductive activ-

ity in both sexes (final gametogenesis, mating,

and ovulation) is synchronized to the time

when environmental conditions (warm tem-

peratures and available food) provide maxi-

mum energy for reproductive effort.

Males and females were especially difficult

to detect and capture during July and August,

the hottest summer months in Tenerife. As

burrows were commonly detected under stones

where skinks were usually found, we suspect

that animals can retire into the deepest part of


their burrow to avoid high surface tempera-

tures at those times. The high temperatures

and absence of rain during those months,

probably restrict skink activity to under the

ground. The months when skinks were hidden

coincided with the time of female pregnancy,

when they have the lowest fat body values.

From September on, fat body masses and

gonad sizes begin to increase, reaching the

highest values in March and April.

Within the genus Chalcides a similar annual

reproductive cycle has been described for C.

chalcides in central Italy (Rugiero, 1997) and

C. bedriagai from mainland Spain (Galán,

2003); however, in these two species, emer-

gence and mating dates are somewhat delayed

in comparison with those of C. viridanus.

This seasonal pattern with ovulation occurring

in the early spring is typical of many other

Iberian lizard species (Carretero, 2006; Galán,

2009) and of some scincids from temperate

(northern and southern) climates (e.g. Sphe-

nomorphus indicus from China: Huang,

1997; Oligosoma maccanni from South New

Zealand: Holmes and Cree, 2006), and there-

fore follow the generalized pattern known for

temperate lizards. Other temperate skinks are

fall breeders (ovulation and mating occurring

in fall and pregnancy during winter ending

with births in spring) in the cold climates of

high mountains in Mexico (e.g. Plestiodon

copei: Guillette, 1983; P. lynxe: Ramírez-

Bautista et al., 1998).

The differences in reproductive time among

scincid species have been explained in relation

to local ecological conditions. In the case of

C. viridanus there is no indication that males

may produce sperm in late summer or early

autumn or that females could store sperm

during the autumn and winter. The reproduc-

tive cycle reported for C. viridanus should

allow females to access environmental food

resources for vitellogenesis at the end of the

rainy season and warm temperatures during

the end of spring and mid-summer that would

be beneficial for their developing embryos. In

turn, offspring born in August should be able

to obtain adequate temperatures for develop-

ment and enough food (insects and arachnids)

before the beginning of autumn.

At present there are no reproductive data on

any Chalcides species from other Canarian

islands. The reproductive cycle of C. virida-

nus occurs earlier than that of other Canarian

lizards such as Gallotia (Family Lacertidae)

and Tarentola (Family Gekkonidae) in which

mating occurs during May-June and offspring

appear at the end of August or beginning of

September (Molina-Borja and Rodríguez-

Domínguez, 2004). This probably reflects a

need for higher environmental temperatures

for the developing embryos inside eggs of

these species laid underground.

ACKNOWLEDGEMENTS

We thank Axia Rodríguez for her help with

histological analysis, and two anonymous ref-

erees for their useful comments. Ma del Mar

González, María de Fuentes, and Martha L.

Bohórquez helped us to capture the skinks

during field trips. Also, we thank Airan Brito

for allowing us to use the data of his meteoro-

logical station. We are also grateful to

Cabildo Insular de Tenerife for permission to

capture the skinks.

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Accepted: 13 June 2013

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