Arribas_Iberolacerta_martinezricai_Reproduction:HERPETOZOA.qxd 02.03.2018 17:02 Seite 1

HErPETOZOA 30 (3/4): 187 - 202 187 Wien, 28. Februar 2018

reproductive characteristics of the batuecan , martinezricai (ArribAs , 1996) (: sauria: )

Zur Fortpflanzungsbiologie von Iberolacerta martinezricai (ArribAs , 1996) (squamata: sauria: Lacertidae)

OscAr J. A rribAs

KUrZFAssUNG

Der Autor untersuchte das Fortpflanzungsgeschehen von Iberolacerta martinezricai (ArribAs , 1996). Kopulationen begannen Ende April. im Juli trugen alle Weibchen zahlreiche frische Paarungsnarben auf bauch und schwanzbasis. Iberolacerta martinezricai ist monoestrisch. Die Eiablage erfolgte im Juli und Anfang August, am häufigsten gegen Ende Juli. Das Eiablageverhalten wird beschrieben. Eier wurden zwischen 9:00 und 15:30 Uhr (GMT) gelegt, wobei der ganze Ablagevorgang, 33 - 42 Minuten (Durchschnitt: 36.57 Minuten) dauerte. Die Kopf-rumpf-Länge reproduktiver Weibchen betrug 56.7 - 69.71 mm. Die Gelege umfaßten zwei bis sechs Eier (Median und Modalwert: 4, Mittel: 4,23). Die abgelegten Eier klebten nicht aneinander. biometrische Daten von 49 Eiern (darunter 12 Laboraufzuchten) werden angegeben. Während des Großteils der inkubationsphase nahmen Eivolumen und Eimasse durch Wasseraufnahme kontinuierlich zu. Zu beginn der inkubation erfolgte ein rascher Anstieg des Ei-Querdurchmessers (dieser wurde während der Ablage durch die Enge des Geburtskanales verrin - gert). Die inkubation dauerte 33 - 42 Tage (im Mittel 37.75 Tage). Das schlüpfen erfolgte zwischen 3:00 und 22:00 Uhr (GMT) (im Mittel 9.40 Uhr) und dauerte 4.10 - 12 stunden (im Mittel 6.9 stunden). Die Merkmale des schlüpf lings werden beschrieben. Der Eizahn bestand für acht bis 36 stunden (im Mittel 23.6 stunden) nach schlupf beginn. schlüpflinge konnen von Geburt an mit ihrem leuchtend blauen schwanz wedeln und diesen auto - tomieren. Diese auffällige schwanzfärbung verschwand im Laufe des zweiten Kalender-Lebensjahres. AbsTrAcT

The author studied reproductive traits of Iberolacerta martinezricai (ArribAs , 1996). copulation began at the end of April. in July all the females presented numerous recent mating scars on the belly and proximal part of the tail. Iberolacerta martinezricai is monestrous. Oviposition occurred during July and beginning of August, mostly towards the end of July. The female’s behavior during the egg-laying process is described. Eggs were laid from 9:00 to 15:30 h (GMT), the whole process lasting 33 - 42 minutes (average 36.57). snout-vent-length of reproductive females was between 56.7 - 69.71 mm. clutches comprised two to six eggs (median and mode: 4, average: 4.23). Eggs were not glued together but remained separated from each other. biometric data of 49 eggs (12 lab-controlled until their eclosion) are given. During most of the incubation period, the eggs increased their volume and mass continuously by water absorption. There was a rapid increase of egg width at the beginning of the incubation (during oviposition egg width is constricted by the tightness of the birth canal). incubation lasted between 33 - 42 days (average 37.75 days). Eclosions occurred from 3:00 to 22:00 h (GMT) (average 9.40) and lasted 4.10 - 12 hours (average 6.9). Hatchling characteristics are described. The egg-tooth persisted during eight to 36 hours (average 23.6) after the beginning of the hatching process. Hatchlings could autotomize and wave their bright blue tails from birth; this conspicuous caudal coloration was reduced and lost during the second calendar year of life. KEY WOrDs reptilia: squamata, Lacertidae, Iberolacerta , Iberolacerta martinezricai , biology, life history, reproduction, breeding, egg-laying, egg characteristics, incubation, eclosion, hatchling characteristics, juvenile coloration; Peña de Francia, batuecas, spain

iNTrODUcTiON

Iberolacerta martinezricai (ArribAs , this steno-endemic lizard confirmed that the 1996), is the most range-restricted and prob - size of its distribution area is only 12-15 km 2 ably one of the rarest and most threatened located in three 10 km x 10 km UTM grid in continental Europe. A re- squares (29TQE48; 29TQE38; 29TQE39) cent survey of the and distribution of with an estimated total occupied area between Arribas_Iberolacerta_martinezricai_Reproduction:HERPETOZOA.qxd 02.03.2018 17:02 Seite 2

188 OscAr J. A rribAs

20-25 km 2 and a population of 1,200 to Lizard were discovered in 2004 ( ArribAs 1,500 individuals ( cArbONErO et al. 2016). 2004 a, 2009, 2013 ). The species was not The habitat of I. martinezricai lies in found in other areas more to the west, as the north of the Natural Park of Las previously expected. The batuecan rock batuecas, at medium to high altitudes of the Lizard is considered critically Endangered sierra de Francia mountain range (840 m - (cr, b2ab(v); c2a(ii)) ( ArribAs 2006, 2013; 1,730 m). One subarea is centered around PérEZ -M ELLADO et al. 2009). Despite the the peak Peña de Francia (1,723 m), extend - fact that the entire population occurs inside ing northward to the peak Pico de los the protected area of the Parque Natural de robledos (1,611 m) plus surroundings, to las batuecas y sierra de Francia and is pro - the northeast as far as the sierra del Guindo tected by law, a specific management pro - (Hastiala mountain, 1,735 m; Alto del co - gram or recovery plan to ensure preservation pero, 1,560 m), southward to the Mesa del of this species is still pending, and the lizard Francés mountain (1,640 m) and towards is simply protected along with its wild habitat. the southeast, up to the northern slopes (and Life history parameters such as phe - probably also the southern upper parts) of nology, molting events, thermoregulation, the sierra de la Grajera (rongiero peak, activity, distribution, habitat selection, pop - 1,627 m) with the range ending in the ulation density and sex-ratio are dealt with Extremadura region ( ArribAs 2006, 2013; in ArribAs (2013), growth, allometry, sex - cArbONErO et al 2016). The other subarea ual dimorphism, longevity and an estima - is called Puerto El Portillo (“El Portillo tion of predation pressure in ArribAs Pass”, from 840 m to 1,400 m) and includes (2014a). The most serious deficit in the the heights of the batuecas Valley on the knowledge of this species is its repro- southern slope of the sierra de la Alberca ductive traits, which are described in the where populations of the batuecan rock present paper.

MATEriALs AND METHODs

study sites.- Data about the re- clutches in laboratory .- some productive state of the lizard come from all gravid females ( in the state just over its distribution area. First studies were before egg-laying are rare and difficult to made in the Peña de Francia mountaintop, find) were transported to the laboratory later in the batuecas valley, and finally (located at 1,020 m a.s.l.) to monitor the again in the Peña de Francia slopes at lower oviposition and incubation processes. Fe- altitudes. Fieldwork was done in sporadic males were placed in glass or plastic terraria visits from 1993 to 2014. (base: 30 cm x 20 cm) with peat substratum Gravid females.- Data on fe - and a flat stone for digging underneath. males were collected concerning the fol - Food (small arthropods from the laboratory lowing aspects: i) Activity - inactive (cold area captured with a light-trap) was supplied and immobile under rocks), active (basking ad libitum, although gravid females when or moving). ii) re productive state - copu - very near to oviposition do not feed at all. lated (recent mating scars present), highly Lizards were maintained under natural illu - gravid (oviductal eggs palpable), or short mination and photoperiod conditions (direct after ovip osition (lateral folds present). iii) sun from sunrise to near 12:00 GMT, and Habitat - estimated percentages of rocks, shadowy but warm until sunset). stones, bare ground, grass or shrubs cover - Females were controlled about hourly ing the site (“percent cover”) in a two- during the day, and twice per night, during meter radius around the spot of first local - the entire study of the oviposition process. ization of the . These percent covers Eggs laid were marked, measured and (%) were estimated by eye, comparing with placed in plastic boxes for incubation under graphic surface-calculation scales ( EMbEr- natural temperature conditions (24-30 ºc) in GEr 1983); the inclination of the site was the open air under the conditions described recorded as well. by ArribAs (2004b) and ArribAs & G ALAN Arribas_Iberolacerta_martinezricai_Reproduction:HERPETOZOA.qxd 02.03.2018 17:02 Seite 3

reproduction of Iberolacerta martinezricai (ArribAs , 1996) 189

(2005) for other Iberolacerta species. When hatchlings perforated their egg- These plastic boxes were furnished with shells, hour (GMT) and total duration of peat or vermiculite substrate and a piece of hatching process were recorded, as well as moss to cover the eggs, to provide a humid duration of egg-tooth persistence. From each environment and facilitate easy periodic newborn lizard, snout-vent-length (sVL), inspection. Four perforations in the boxes body mass and the extent (relative to ventral ensured air circulation and prevented from scale rows) of the umbilical scar were noted. mold development. Excessive moisture de - Hatchlings were sexed mainly by the number crease was countervailed by spraying the of trans versal series of ventral scales (males moss and the eggs with water). clutches 27-28, females 28-30)( ArribAs 2014 d). were inspected daily and egg metrics Newborn specimens were successful - (length, width, mass) were taken weekly. ly fed with aphids until release at the site of Egg volume (V) was calculated based on an their mother’s origin. ellipsoid approximation (V = 4 πa2b/3), a and statistical calculations were per - b being half the width and half the length of formed with Ncss-2007 © (HiNTZE 2007). the egg, respectively. Differences were tested using t-tests or One- Length measurements were taken with Way ANOVA, with Tukey-Kramer post-hoc digital callipers (Mitutoyo ®, accuracy 0.1 tests for pairwise comparisons among the mm) and egg-masses with a portable digital group means ( sOKAL & r OHLF 1969; online scale (Tomopol s050 ®, accuracy 0.01 g). help in HiNTZE 2007).

rEsULTs AND DiscUssiON

sexual maturity and dimor - (M < F, males less than females) and femoral phism were studied by ArribAs (2014a). scales (M > F), forelimb length (M > F), The former is most probably reached when hindlimb length (M > F) and pileus length (M lizards are three years old, i.e., in their fourth > F), and at p < 0.05 in the number of collar calendar year (4th cY). The smallest gravid scales (M > F) and longitudinal dorsal scale female studied was 56.7 mm in sVL and rows [“dorsalia“] (M > F) ( ArribAs 2014a) . probably reproducing in the spring of its 5th sex ratio calculated from the cY, i.e., at the age of four years. some male author’s morphological database was 0.74:1 and female specimens may reach maturity (29 males : 39 females), which does not dif - in their third cY, as occurs in I. monticola fer significantly from 1:1 (Multinomial test: (b OULENGEr , 1905) (ArribAs 2014a). The chi 2 = 1.47, Ns), whereas from the clearly biggest male (sVL 68.15 mm) and female higher number of field observations (repeti - (sVL 68.86 mm) conserved had seven tions included) was (1.27 : 1), significantly growth rings (corresponding to two strong favoring males (260 males : 204 females) and five weak growth periods) in the femur (Multinomial test: chi 2 = 6.75, P = 0.009) cross sections. both specimens were most (ArribAs 2013). However, recalculation likely eight years old (in their ninth cY: the based on new field data (357 observations birth year + seven seasons of growth + the of males and 337 of females) resulted in the year of capture) ( ArribAs 2014a). absence of significant differences, showing comparable results are known from I. a balanced sex ratio (1.06:1) (Multinomial monticola which reaches the age of 10 years test: chi 2 = 0.57, P = 0.44, Ns). From 12 in the serra da Estrela (Portugal) ( MOrEirA hatchlings of lab-controlled eggs, six were et al. 1999) and one among hundreds the females and six males. exceptional age of 15 years ( GALáN 2011a). Phenology (largely based on Ar - similarly, a male I. aurelioi (A rri bAs , ribAs 2013).- The lizard’s annual activity 1994) was at least 16 and a female possibly begins at the end of March or, more fre - 14 years old ( ArribAs 2004b, 2007). quently, during April and lasts until the end As to sexual dimorphism, male and of september or beginning of October. A female I. martinezricai differ at p < 0.001 in general pre-oviposition molt is observed in the number of transversal ventral scale rows gravid females during the first half of July. Arribas_Iberolacerta_martinezricai_Reproduction:HERPETOZOA.qxd 02.03.2018 17:02 Seite 4

190 OscAr J. A rribAs

Fig 1: Iberolacerta martinezricai (ArribAs , 1996) from Peña de Francia and batuecas Valley (salamanca, spain). Females showing recent mating scars on belly and tail base. Arrows indicate the areas worst affected. Abb. 1: Iberolacerta martinezricai (ArribAs , 1996) von der Peña de Francia und dem batuecas Tal (salamanca, spanien). Die Weibchen zeigen frische Paarungsnarben auf bauch und schwanzbasis. Pfeile weisen auf die am stärksten betroffenen stellen.

Places occupied by the species (in par - and phenology. in some locations the sun ticular the lower altitudinal and therefore does not reach the ground during the cold usually milder sites) are surrounded and periods of the year. in specimens living protected from direct insolation by moun - under such conditions, the yearly and daily tain spurs that condition the lizard’s activity activity periods are considerably shortened.

______

Fig. 2 (opposite page) / Abb. 2 (gegenüberliegende seite)

A - Iberolacerta martinezricai (ArribAs , 1996) from Peña de Francia (salamanca, spain). Gravid female of the blue morph. Note that contrary to gravid female lizards, the body does not appear very bulky in this species with small clutch size. b - Gravid female of the green morph. c - Two gravid females of the green morph, one reticulated and the other with paravertebral rows of spots. As in A and b, gravid females are not very voluminose. D - comparison between gravid adult females of Iberolacerta martinezricai (ArribAs , 1996) from the sierra de Francia, salamanca, spain and (MüLLEr & H ELLMicH , 1937) from the neighboring sierra de bejar (salamanca, spain). Note the differences in size and bulkiness. A - Iberolacerta martinezricai (ArribAs , 1996) von der Peña de Francia (salamanca, spanien). Trächtiges Weibchen der blauen Morphe. Man beachte die im Unterschied zu anderen trächtigen Eidechsen geringe Massigkeit des rumpfes bei dieser durch geringe Gelegegröße gekennzeichneten Art. b – Trächtiges Weibchen der grünen Morphe. c - Zwei trächtige Weibchen der grünen Morphe, eines mit Netzzeichnung, das andere mit paravertebralen Punktreihen. Wie bei A und b, erscheinen die trächtigen Weibchen nicht sehr füllig. D – Vergleich zwischen adulten trächtigen Weibchen von Iberolacerta martinezricai (ArribAs , 1996) der sierra de Francia, salamanca, spanien, und Iberolacerta cyreni (MüLLEr & H ELLMicH , 1937), aus der benachbarten sierra de bejar (salamanca, spain). Man beachte die Unterschiede in Größe und Körperfülle. 1

9 2A 1 ) 6 9 9 1

, s A b i r r (A

i a c i r z e n i t

r 2B a m

a t r e

c 2C a l o r e b I

f o

n o i t c u d o r p e r

2D Arribas_Iberolacerta_martinezricai_Reproduction:HERPETOZOA.qxd 02.03.2018 17:02 Seite 5 Seite 17:02 02.03.2018 Arribas_Iberolacerta_martinezricai_Reproduction:HERPETOZOA.qxd Arribas_Iberolacerta_martinezricai_Reproduction:HERPETOZOA.qxd 02.03.2018 17:02 Seite 6

192 OscAr J. A rribAs

by this, the total activity cycle of I. Females were observed basking even under martinezricai is only slightly longer (six suboptimal weather conditions during the months in total) than in true high mountain first fortnight of July ( ArribAs unpub - species, such as other Iberolacerta (Pyrene- lished), probably to promote vitellogenesis. saura ), whose annual activity period covers There was no significant difference in slightly less than five months ( ArribAs & body temperature (bT) between gravid GALAN 2005). females of the “blue” and “green” morphs in the lizard’s , not only the (bT green gravid females: 33.24 ± 0.18 ºc, annual but also the daily insolation cycles 29.2-36.4, N = 85 observations; bT blue are relatively short, just a few hours of gravid females: 32.71 ± 0.47 ºc, 18.5-36.8, direct sunlight per day. Due to the relief of N = 50 observations; t = 1.21, P = 0.22) the mountains and the orientation and incli - (Fig. 2A - 2c). Also, there was no signifi - nation of the slopes, the sun reaches the cant difference in bT between gravid habitats late in the morning, especially the (reproductive) and non-gravid (post-repro - lowermost portions of the slopes. Hence, ductive) females (bT gravid females: 32.98 and paradoxically for a lizard living at the ± 2.45 º c, 18.5-36.8, N = 143 observations; edge of the Mediterranean realm, its activi - bT non-gravid females: 33.27 ± 1.84 ºc, ty period seems to be shorter and reproduc - 26.2-36.7, N = 105 observations; t = 1.02, tion activities seem to be delayed in com - P = 0.30). parison with the neighboring high mountain Oviposition occurred during July and (Oro and crioromediterranean) dweller I. in the first days of August. The egg-laying cyreni (MüLLEr & H ELLMicH , 1937), from period spanned from calendar week # 25 the sierra de bejar ( ArribAs , pers. obs.). (first week of July) to calendar week # 29 Mating and egg-laying peri - (first week of August) (average: week # od.- in the first days of April, females 25.5 ± 0.4). From 13 clutches controlled, have not yet copulated (recent mating scars two were laid in the first week of July (cal - are absent). copulations begin at the end of endar week # 25), two during the second (# April (three females with mating scars and 26), none in the third, five during the last five without it in April 30, 1995). There is week of July (# 28), and four in the first no information concerning the period of week of August (# 29). The earliest post- May and June, but it is reasonable to assume oviposition female was found in the first that, depending on the site characteristics week of July (July 6, 2007). and weather, territorial behavior and copula - surprisingly for a mountain lizard in tion occur mainly during these months. in an almost Mediterranean environment, the the first week of July, all the observed phenology of I. martinezricai does not pre - females presented numerous recent mating cede the timing of the seasonal life cycle scars (very dark, almost black) at the belly events of other Iberolacerta . However, as sides and proximal part of the tail, corre - detailed above , the species occupies high sponding to copulatory bite marks received and particularly harsh climate habitats in its during the previous courtship (Fig. 1). range area. The shading capacity of the copulation in the field was observed slope that influences the phenology, the in the first week of July. seven out of 21 weather in late spring and perhaps the age of females with copulation scars on the belly the females (maybe younger females lay had also big marks at the tail base (Fig. 1). their eggs later, as occurs in other small la -

______

Fig. 3 (opposite page) / Abb. 3 (gegenüberliegende seite)

Iberolacerta martinezricai (ArribAs , 1996) from the Peña de Francia (salamanca, spain). A - Freshly laid eggs. b - Eggs during incubation, close to the eclosion. c and D - Two moments of the eclosion in the laboratory. Iberolacerta martinezricai (ArribAs , 1996) von der Peña de Francia (salamanca, spanien). A – Frisch gelegte Eier. b – Eier während der bebrütung, nahe dem schlupftermin. c und D – Zwei Zeitpunkte des schlupfes im Labor. Arribas_Iberolacerta_martinezricai_Reproduction:HERPETOZOA.qxd 02.03.2018 17:02 Seite 7

reproduction of Iberolacerta martinezricai (ArribAs , 1996) 193 3 3 A C 3 3 B D Arribas_Iberolacerta_martinezricai_Reproduction:HERPETOZOA.qxd 02.03.2018 17:02 Seite 8

194 OscAr J. A rribAs

. . l i t -

e e n t l i

r

1

l n a

2

r h .

)

6 o 4

5 3 b t c s o A m

e m 3 1 s 4 5 6 i i

i . 9 9 2 4 6 4 b a

5 3 0 8 “ k u 6 t . 2 . t f r g t . 6 . 0 2 . [ l a 3 1 0 0 . 0 e e 5 2

. a z e . . . 0 . 5 o l

g 6 0 . . 7 2 0 o 5 0 g e r e

. 1 e ) b

0 0 0 0 2 e - ± 8 1 1 0 1 e p ± ± h 1 n c 1 n 6 u - - - - l n w 7 5 ± ± ± 2 ± ± t 1 r

i - -

6 8 o

9 k

e t - 9 1 7 5 o 0 7 5 8 7 7 1 e i . 8 7 f e . 8 . 3 r t = 9 t n 5 6 3 0 6 v 1 s . 6 2 0 . 9

G 7 . . . 7 o v i 0 . . . . 5 . a a n 1 . 1 0 .

e

i 2 0 t - i

. 6 0 . 4 i

t 1 r 0 0 0 1 0 N 9 0 h , r e m 9 1 F r

e 9 3 0 1 ( e 8 r c s e

r a 8 g t 7 n p d A a d p n e u r t

b l j t e u r f i n c t f

r e

u

r

e e n

e h c ) a l

8

1 i r

5 9

h c . 7 .

d

s

a

1 s i

1

c 6 6 8 5 2 l “ r e A

2 6

6 n l n g . . 6 7 3 k . 4 5 3 8 s ( o 0 3 1 o o ä h e

0 6 . 6 ß g 3 0 0 0 . . 0 e t f 5 0 1 . 0 e r m r . . 0 . e b i 0 . 9 . 7 .

e

e 1 3 . 0 0 n e W e i 7 . 0 h o

t 0 0 0 a a 1 1 0 1 1 n l

r

0 ± ± ± ± c b 1 0 1 i 2 - - - - - w V x g c f ± ± ± r t h I

- - -

i 9 6 ± 3 9

o e 1

8 2 5 1 9 n e 3 9 7 r c

u a t r

s 4 1 1

1 1 1 6 0 l e t 5 3 . 0 2 6 s

) d . . 6 4 . . 8 u z n i g 4 . . . . 3 . r A = l . . 0 . c a e . 0 .

n e

6 4 . 4 0 o

o

g 3 0 0 3 0 h a i 0 0 0 e e 3 9 d i n t t 0 8 0 1 1 D d v F e e 3 1 i N i

s 3 n

o

e t 1 7 (

6 d

t r . i 9 e , r d h

r e

. e n 4 a c n h n i

h t n g i s o , c u

m i ä l E a i

a

o

t

s

l

i

a

) s h

2 a w t e o 9

s

s a g s b 5

n 2 5 4

t

t

. 7 4

b 4 o 0 .

2 k n d o g g r e 6 7 2 . ] t r . 6 5 6 5 l A 5 0 3 1 t u e e

2 2 e . 1 n e p g 0 0 . . 0 ” e 0 c

9 . 1 . 9 0

c e 2 . . 0 h . h a

n 5 . 6 . . e s r c . 0 0 1 e

7 1 0 w i 2

c n 0 0 0 e i ± e

8 0 1 0 1 e

- a i w 0 i ± ± ± d 1 1 ß 1 , 2

- - - - u - r l

6 ± ± ± h o - 6 - ( z s e ± 0 9 e 5 s f t 1 e 3 5 6 4 1 o h c 9 9 5 6 t v

r e

8 . 4 1

e i . 2 0 5 t r 3 o e 1 . 9 5 6 a

7 5 . . 7

. e

. b 8 1 . 2 . M n h

r e = 7 . . 1 . u t . 0 0 . t

b s

. 4 9 0 l s c o 0 7 . 2 0

o h b i 7 0 0 0 n t 4 9 i k k u c 0 1 1 I

e 5 0 1 e e t N 6 T u u i 4 e

c

n i

1 r ( l f

h e s d

n d u d c r i o

o

e

r c p

e w

t e

t l p d

h . n e s i

t l i

e e c “ e l ) e e

e u g 9

a t v

7 r s s a 2

v h

d

.

4 l s g

a

0

7 1 Z t o r 9 e r h

g t p 7 . 2 1 )

. 9 5 4 5 9 3 e k

c

h . 1 1 0 3 e e h s .

0 g 1 2 . . 0

T g e 0 0 0 1 6 7

s

. . 4 0 0 . c m . . . . n 5 f e m “ . 2 0 . 0 d m e w n t 7 7 b

d 1 0

1 0 d

e u i 9 0 9 0 1 o - e 0 0 u -

± ± ± r u l 1 o 2 r n - - - - - i r w ± ± ± t l l e a

- 5 z e 1

± 1 9 ± 0 f m a u 1 9 5 7 4 8 d . 4 9 4 c x e i

y

5 3 d o h

5 6 4 9 2

d . 8 0 3 l 5 8 u r e 0 0 s 3 . . . . 6 b l x 8 . . . .

. l t = n . d . 0 . - c . 9 e w a ]

g T 0 7 8 . 3 e a s a 7 0 8 0 1 i e u 9 1 0 t 8 4 ”

t

g

T T 6 0 1 h n 1 N 9 E

s a e 4 a M e “ c 5 ( o t e -

m b i h b n h r i t a h 2 s u

o A m e

h c

a

i 1

l

c t

t ) u b

l

d

c 9

i 2 . . n s u d

3

a ü 8

c g 8 i s

8 8 l n e m 2

. n

g n k 7 . 6 8 6 1

. 4 4 8 5 o n “ 4 i c o . 2 0 f d e 9 8 a . i

a g e [

. 0 0 2 0 0 n 0 3 2 7 6 n r p

6 . 0 . . . o s s

g 4 3 . . . . 4 e

e i i d e 0 1 . i 6 .

u a d 0 0 0 0 e ± e 5 1 0 8 0 r 1 e d ) v n

0 ± ± l 1 2 w e 2 ------l M 2 ± ± ± ± g p

w h t - - o e l e 2 1 ± 1 4 8 4 4 8 O 8

m i e 5 5 7 6 4 e c a

5 3 . t e ; t . 1 2 8 . l t m “ t . 6 1 1 4 5 G u . . 9 4 5 n b s

2 7 . . . . . a e =

4 . 1 2 . . a a o h w . 0

1 6 . e u n 1 0 0 8 0 1

m 1 3 0 1 8 0 O h c c t 2 b G m i 7 0 c s

1 4 r N 1 1 a r

9 m x s a 4

n ( d u e

o i n u a e w n n

f c l d e r w h a e o t l n o m e e

n c

e i l - v e h c t

) i l b d 5

r t

c t s u

r 4

e o ü 4 5

m h e n i l

7 n a t . r e g 8 2

e u 6 8 1 c h o t e i T a . 9 0 . 5 . f t i g

w r M 9 4 n e “

t b 8 0 0 0 E r 0 2 . . m e

p

a d i . .

f

i r o

u e r ± ± 4 1 7 0 s 0 0 0 0 u s e b 0 0 o c 9 n . . . . 2 c l - - - - l e b 9 h 8

e o i - l g t ± ± 4 0 0 0 0 1 n h 1 3 4 3 a ü 6 5 d p b

i

o ü n t . 5 6 T . c i ) 3 7 9 3 m

t

r . f a “ . . . . a = u r 1 3 3 t 1

r l r v s [

7 . ;

5 0 6 0 d

m 1 o 4 n ) e e r

“

) 0 m l O s y 9 1 a N b 3 o v o l e n ( m h s g 2 l m a c r

m m h o e e r

g u ( u t e i L ) f m

e

e l f t g e m z (

l i

g d

e ( s e

h )

s

( r a r t g d d n 3

h s m i a o h m

i r t h n e i i s ) t

t i l d a p ) u n m

g s , w b l

i d l d

r d n e a f m i n n

o v m o r m e u d a n r e o e e l ( t e t l m w v e

) m d a

O i g m

c g r t ( s n

t n g e (

“ e a s g g g g n a

(

o l d n l o i

h g g g g p i

e h m c e ± t e n b s t t t ± - e e e e n s

u l g s u

a

m l G d l b A ä o f f f f a a

i n

n e o i r a , o

m o o o o t t p e l n a ] r c

p t r i l w m v

e i e

s ” e s e n n n n o e t

e s i i i i r g g g g f d o r h h m b e M a a a a

t g g g g n

e p

c

i

h i e n d c o f G G G G E E E E

a t s c

v i t t i o t o e t

n w o e n

v u e i

h y r s e l a

t l

c t e s

n

c a m

n n s g

a ]

b e e

i 6

e h 9 9 8 r l s t n

5 d 3 ] t 1 t ü

. O d 7 l 0 4 5

.

8 6

i

e p . g i u . 8

3 a 4 0 4 7 .

e r - 0 0 1 .

1 d . 4 3 3 a h g 9

g 2 . 1 1

, 0 0 5 6 a 2 b

l m D 0 . . 0 3 3 . i t n . ) c 1 6 9 4 . e ( 6 d 0 0 . .

t

. 9 8 . .

a i

h a 0 0 1 9 0 h i

0 ) * 2 1 l 1 t n 1 0 0 n

± 0 1 8 4 1 y T ( t - s d i e 1 2 , g ± ± ± 1 ± l

a - - - - m e * t ± ± 3 ± ± i r

] - - 1 t - i n 1

7 1 8

r 0 Z o 7 6 5 - 7 . d ( n 7 a ” 9 0 3 4 n 5 4 e ) n 0 0 . d

r a . 5 3 4 s . ( 8

e . . 9 1 0 1 1 t n 9 0 . . 3 . e s f 6 e n g . e d 6 . . . l e i 7 . .

2 . t

n 6 l 6 6 7 4 2 7 6 k c e e

9 i 3 4 9 0 m l e w g 8 . 9 0 a e l 8 9 1 2

w e 1 t 1 5

n m t v 1 e r . 0 9 o o n e 5 0 1 i r [

3 1 r r r o [ a r 3 e l o 0 1 1 y a t n

g 1 e t h 1 e u d l

d

l h k s n c

l n s r r s w

t i

c

e b a o e ,

s k u n - ] ]

l e ß A s n e s r t c o l d n e e n s d d e “ b i

- s r m

A g e

[ h a e e a e

, y e b M r e f m u l

d b c ) m m m m l s )

M c i h h h

l i i a e ) t ) v l u s m u t s s n o o o o

l

c c e a

o

l e E r a 5 u 6 n a

: e r r r r t t V e e

u l i

c v f f f f h r d o :

r n 0

h 9

a a y 1 h

h h

c a l

c n v

1 2 o 0 n

c e 9 n h h c c s s s s

l c

e t m A

i t

t t l a e

e ) ) ) ) e 1

2 d v 1 e t g g g g

u

l h u u . s l l h t i u i

h h ( u u s s s s t l f b

u s a l g t g g g r

h z a l l l b c b u ,

a

t c c e e e e h m r

s t c

a t s l c e c e e e e i i c c c t a a s t l

N r h d e h h h h

i u

n g s g u t c A u m h h t e l d l n T T A A u l c n c c c c y 0 9 9 9 9 e a 1 1 l i n n a o o e t t t t d e l v o L c b a s w w 1 1 4 1 4 4 4 e t i o s i N

s

b

u u u u o

l w m v A t r A

l t m l l l l e ( n r

f f e r e t

- a ======a r a c c c c n e g

l p g g g g o o e r

G t e n

r

)

e s r p c i e e g g g g o o a 1 1 1 1 N N 2 N N 2 N N N A * e e n h r E ( & ( 1 T [ ( ( m r r t [ r D p 1 E ( 1 E ( 1 E ( ( k i ( Arribas_Iberolacerta_martinezricai_Reproduction:HERPETOZOA.qxd 02.03.2018 17:02 Seite 9

reproduction of Iberolacerta martinezricai (ArribAs , 1996) 195

certids; GALAN 1997, 1999; r úA & G ALAN areas of screes and in the proximity of 2003) may determine the final moment of water sources. oviposition. in fact, oviposition of I. mar - Oviposition and egg-laying tinezricai is later than in other high moun - behavior.- The excavation process of tain species, e.g., of the subgenus Pyrene- the egg chamber takes several hours. This saura (ArribAs 2004 b; A rribAs & G ALAN burrow is not immediately placed under a 2005) or I. cyreni from the sierra de bejar stone seated on the ground but a little bit (ArribAs unpublished). Furthermore, fe - below its lower surface, completely dug into males of I. martinezricai are clearly less the ground, in one case under laboratory con- bulky than their congeners when gravid ditions, 4 cm below the surface of the soil. (Fig. 2 D). During the labor to expel an egg, the There is no evidence of more than a female stretches the hind legs spasmodical - single clutch per year and female, regardless ly several times, raising the base and the of its size. Yet, due to lack of information proximal third of the tail for a couple of from May and June one cannot totally dis - seconds. All these actions are repeatedly miss that eggs observed in July could be executed, interrupted by long periods of second clutches of the year. However, the rest. At the same time, she twists the body first appearance of hatchlings in the field (in and tongue-flicks excitedly while moving september) and the lack of different cohorts backwards. The body takes the shape of an of juvenile lizards corresponding to differ - “s”, squirming with the tail a bit raised. ent periods of oviposition speak in favor of When an egg is ejected it remains a unique oviposition per year and female attached to the tip to the cloaca, although (monestrous female sexual cycle, sensu most of it is expelled within a few seconds. GALAN 2009). The female kicks with the feet to detach the in other populations or species of egg that rolls to the ground. in one case, the small sized oviparous lizards (which are kicks counted during the expulsion of the mainly polyestrous), at least the largest egg were 25, and continued increasingly females are able to produce two clutches per spaced after the total detachment of the egg year. but as climatic factors limit the dura - (about 18 seconds in total). These maneu - tion of the reproductive period they seem to vers also move the previously laid eggs and be responsible for the absence of a second cover them with soil. or even multiple clutches as is the case in After completion of the clutch, the the mountain dwelling Iberolacerta , but not female continues with digging movements, in lowland I. monticola (GALAN 2009). scraping soil with the front legs and a few Egg-laying sites.- sites of egg- times but very strongly with the hind legs. laying in nature are almost unknown. With the front legs, she scraps the ground Despite the great number of stones lifted, and pulls back earth, which is pushed to- only a few old eggshells have been found. ward her eggs with the hind legs. This is in part due to the fact that egg-lay - As in other Iberolacerta s. str. and ing sites are inaccessible if lizards inhabit contrary to Pyrenesaura or the oviparous screes where there are rocks on top of each Zootoca , the eggs were not glued together other. However, gravid females near their but remained loose from each other (Figs. egg-laying date are located in the vicinity 3A-3b). of water, a scarce resource in these places Ovipositions detected in the laborato - during the summer. Lizards are seen near ry occurred from 9:00 h to 15:30 h (GMT) fonts and depressions of the terrain where (average = 11.32 ± 0.5 h; N = 22 eggs). boulders accumulate under which water Total duration of the egg-laying process runs. Thus, suitable egg-laying sites repre - from the appearance of the first egg to the sent a compromise between the need for deposition of the last was from 33 to 42 sufficient solar radiation to incubate the minutes (average = 36.57 ± 1.32; N = 7 eggs (thus, near the surface) and the pres - clutches). ence of moisture (hence, near the bottom of characteristics of egg-laying the scree through which water flows). females and clutch size.- snout- both factors can coincide in the lower vent length of reproductive females was Arribas_Iberolacerta_martinezricai_Reproduction:HERPETOZOA.qxd 02.03.2018 17:02 Seite 10

196 OscAr J. A rribAs e g h e c l t b

A e u l G c

l e h h a t

z n n i

A s

/ g

s g e e

h f c o t

u r l e c b

f m o

u r e N b m u

Female sVL (mm) N Number of eggs per clutch / Eizahl je Gelege

Fig.4: Iberolacerta martinezricai (ArribAs , 1996). A – relationship between female snout-vent-length (sVL) and the size (egg number) of her clutch. b – Frequency distribution of clutch size. Abb. 4: Iberolacerta martinezricai (ArribAs , 1996). A – beziehung zwischen Kopf-rumpf-Länge (sVL) des Weibchens und der Eizahl seines Geleges. b – Häufigkeitsverteilung der Gelegegrößen.

61.78 ± 0.93 mm (range: 56.7 - 69.71, N = is intermediate (closer to the lower limits) 10) (Fig. 4 A). The body mass of gravid within Iberolacerta s. str. but higher than in females was 5.2 ± 0.14 g (range: 5.06 - other lacertids such as Podarcis muralis 5.48) (N = 3). After egg-laying, body mass (L AU rENTi , 1768) (0.24 - 0.47), Podarcis lil - was reduced to 3.25 ± 0.13 g (2.63 - 4.00) fordi (G üNTHEr , 1874) (0.25), Podarcis (N = 10). melisellensis (b rAUN , 1877) (0.25), Dalma - The number of eggs per clutch was tolacerta oxycephala (s cHLEGEL , 1831) two to six (average: 4.23 ± 0.23). From 17 (0.23) or Algyroides nigropunctatus (D UMé- clutches checked or gravid females palpated riL & b ibrON , 1839) (0.29) (see summary in by the author, one was composed of two rúA & G ALAN 2003 and ArribAs & G ALAN eggs, two of three, seven of four, six of five 2005). and one of six eggs (see Figs. 4A - 4b). Other Iberolacerta species, such as I. This clutch size is bigger than in monticola or I. aranica have average rcMs Pyrenesaura (ArribAs 2004 b; A rribAs & of 0.54 - 0.56 and 0.55, respectively, higher GALAN 2005), but smaller than in other than in most other lacertid lizards, with the Iberolacerta s. str such as I. monticola (the exception of Zootoca vivipara (L icHTEN- species studied best) in which it varies from sTEiN , 1823) which may reach up to 0.81 two to 11 eggs (average: 7.2 in Estrela, 6.3 (rúA & G ALAN 2003; A rribAs & G ALAN in Galicia lowland localities, 6.2 in Asturias 2005). Iberolacerta (s. str.) horvathi (Mé- or from 5.3 to 6.2 in León) (see ArribAs HELY , 1904) has a slightly lower rcM of 2014b, 2014c, 2014d, 2014e). 0.435 ± 0.028 (range: 0.155 - 0.632) ( LJU - Female reproductive invest - bisAVLJEVic et al. 2012). ment sensu ArribAs & G ALAN (2005) There were no significant correlations (average: 19.03 ± 0.005; range: 16.01 - between female sVL and several parameters 21.4; N = 11 clutches) falls within the limits as clutch size ( r = 0.07; t = 0.29, P = 0.78), of the three Pyrenesaura species ( ArribAs egg length ( r = -0.20; t = 0.16, P = 0.16), & G ALAN 2005) but was not yet calculated egg width ( r = -0.16; t = -1.08, P = 0.29), for other Iberolacerta s. str. clutch mass egg volume ( r = -0.26; t = -1.8, P = 0.07) or relative to the female’s body mass (hence - the total clutch volume ( r = -0.09; t = -0.28, forth referred to as relative clutch mass – P = 0.78 ). The correlations between the rcM, nonsystematically influenced by tail residuals from the regression of log (clutch autotomy and dehydration) was 0.49 ± 0.04 size) on log (sVL of mother) and of log (egg (range: 0.27 - 0.65; N = 10 clutches), which mass) on log (sVL of mother) were also not Arribas_Iberolacerta_martinezricai_Reproduction:HERPETOZOA.qxd 02.03.2018 17:02 Seite 11

reproduction of Iberolacerta martinezricai (ArribAs , 1996) 197

A b ) 3 m m (

) e g s ( a

e s r s c a n i m

e g g m u E l o v

g g E

1 2 3 4 5 6 1 2 3 4 5 Week / Woche Week / Woche

Fig. 5: Iberolacerta martinezricai (ArribAs , 1996). A – increase of egg mass during the incubation. changes in egg volume, not represented, are fully par alleled by that of the egg mass. Note the continuous increase of the mass from the moment of deposition (“week 1”) until a date very near to eclosion (“week 6”), when eggs begin to reduce their turgidity. b – increase of egg volume during the incubation is largely constant, but slightly raised during the first week and reduced in the week prior to eclosion. Outliers in the first week correspond to eggs that died and decayed. Abb. 5: Iberolacerta martinezricai (ArribAs , 1996). A - Zunahme der Eimasse während der inkubation (die Veränderung des Eivolumens, hier nicht dargestellt, entspricht jener der Eimasse). Man beachte die regelmäßige Massenzunahme vom Augenblick der Ablage (“week 1“) bis kurze Zeit vor dem schlupf (“week 6“), als die Eier begannen, ihre Turgeszenz zu verringern. b – Die Zunahme des Eivolumens während der inkubationszeit erfolgt ziemlich gleichförmig; sie ist etwas gesteigert während der ersten Woche und reduziert in der Woche vor dem schlupf. Die Ausreißer der ersten Woche entsprechen Eiern, die abstarben und verfaulten.

significant ( r = 0.05; t = 0.36, P = 0.72). for a determinate female size. in the three clutch size (number of eggs) may be posi - Iberolacerta (Pyrenesaura ) species, clutch tively correlated with the total clutch vol - size was significantly positively correlated ume but this relationship did not reach the with female sVL, whereas egg length was level of significance ( r = 0.58; t = 2.16, P = not. Other parameters such as egg width, 0.06). However, there was a significant egg volume and total volume of the clutch, negative correlation between female sVL were positively correlated with female sVL and the individual egg mass ( r = -0.43; t = in I. aranica only, probably due to small -3.23, P = 0.00) suggesting that bigger fe- sample size in the other two species. males lay smaller eggs, may be combined correlations of the aforementioned residu - with an increase in the number of eggs per als were significant in all three species. clutch, which could however, not be ob- clutch size (number of eggs) was positively served due to the small sample studied. correlated with total clutch volume in the in a closely related species, I. monti - three Pyrenesaura species, (significant only cola , mean egg mass was not correlated in I. aranica , probably due to large sample with female sVL, and negatively correlated size). in conclusion, the bigger a Pyrene- with clutch size ( r = -0.36) ( rúA & G ALAN saura female is, the more and bigger are the 2003), but the total clutch size and mass eggs it lays and the bigger is the total clutch increased significantly along with female volume. This increased egg size in large sVL ( r = 0.53). Furthermore, rcM was not clutches is different from what we find in I. correlated with female sVL in this species, monticola and is suggested in I. martinezri - and the residuals from the regressions of log cai . (clutch size) on log (sVL of mother) and log The distribution of the vitellus (yolk) (egg mass) on log (sVL of mother) showed among the eggs follows different strategies a negative correlation ( r = -0.36). in con - (bAUWENs & D íAZ -U riArTE 1997; b AU- clusion, larger clutches meant smaller eggs WENs 1999): Lizard species which lay large Arribas_Iberolacerta_martinezricai_Reproduction:HERPETOZOA.qxd 02.03.2018 17:02 Seite 12

198 OscAr J. A rribAs ) ) m m A b m m ( (

r r e e t t e e m m a a i i d d

l l a a n s i r d e u v t s i n g a n r t o

l

g g g g E E 1 2 3 4 5 6 1 2 3 4 5 6 Week / Woche Week / Woche

Fig. 6: Iberolacerta martinezricai (ArribAs , 1996). A – Variation of the egg transversal diameter (width) during incubation. “Week 1” corresponds to fresh-laid eggs, “Week 2” to the end of the first incubation week, and so on. Note the steep increase in width during the first third of the incubation period and see text for discussion of this phenomenon. b – Variation of the egg longitudinal diameter (length) during incubation. Abb. 6: Iberolacerta martinezricai (ArribAs , 1996). A – Veränderung des Ei-Querdurchmessers im Verlauf der inkubation. “Week 1” entspricht dem Querdurchmesser frisch gelegter Eier, “Week 2” jenem am Ende der ersten inkubationswoche, usw. Man beachte den steilen Anstieg des Wertes im ersten Drittel der inkubationszeit, der im Text diskutiert wird. b – Veränderung des Ei-Längsdurchmessers im Verlauf der inkubation.

numbers of relatively small-sized eggs (e.g., which all however a are slightly larger in Lacerta s. str.) invest in the increase of the size (see Fig. 2D). Iberolacerta mar - number of eggs, not their size. Those which tinezricai females reach sVL values of lay small numbers of large-sized eggs (e.g., 68.86 mm (average 59.77 mm), whereas I. Podarcis ) invest in the increase of the egg’s cyreni as much as 81.74 mm (average size, not its number. Iberolacerta montico - 65.51 mm), I. galani 84.42 mm (average la (and probably also I. martinezricai ) rep - 64.19 mm) and I. monticola 79.81 mm resents an intermediate situation between (average 61.02 mm). The similar-sized I. these two extremes, increasing both the horvathi (sVL maximum 70.5 mm, aver - number and the size of the eggs ( rúA & age 60 mm) has a comparable clutch size GALáN 2003; G ALAN 2009). in those lacer - (2 to 5 eggs, mode 3) ( ArribAs 2014b, tids with medium egg size, the reproductive 2014c, 2014d, 2014e; DE LUcA 1989, 1992; investment changes throughout their onto - LJUbisAVLJEVić et al. 2012). This is an geny along with the female’s growth. A aspect to keep in mind considering the con - young Iberolacerta female behaves like servation status of I. martinezricai : its low Podarcis in laying few eggs because of her reproductive potential adds another con - small size and limited quantity of vitellus straint to the restrictions imposed to the available for distribution, whereas old and species by climate and habitat. thus large females lay many more and big - Egg characteristics.- Measure - ger eggs due to the increased quantity of ments of fresh, recently laid eggs are shown vitellus available for distribution among in Table 1. There is no data from the embry - eggs. The quantity of vitellus available onic developmental stages as no eggs were varies over the life time of the individual opened for this purpose. and between first and second clutches of the Transformation of the egg year (if a second exists). during incubation.- For metric traits The clutch size of Iberolacerta mar - (length, width, mass, volume, as well as tinezricai is noticeably small (Figs. 4A- weekly increase in these parameters) of 4b), clearly smaller than in the related eggs during the incubation see Table 1 and species I. monticola , I. galani ArribAs , Figs. 5-6. Eggs increase their volume and, cArrANZA & O DiErNA , 2006, and I. cyreni , thus mass constantly during the incubation Arribas_Iberolacerta_martinezricai_Reproduction:HERPETOZOA.qxd 02.03.2018 17:02 Seite 13

reproduction of Iberolacerta martinezricai (ArribAs , 1996) 199

A

b

Fig. 7: Iberolacerta martinezricai (ArribAs , 1996). A – recently hatched specimens (one of them lacking the tail tip) (inset: ventral view of the same specimens). b – A yearling. Note that the bright blue color of the tail fades and disappears during the second calendar year of life. Abb 7: Iberolacerta martinezricai (ArribAs , 1996). A – Kürzlich geschlüpfte individuen, eines ohne schwanzspitze (insert: bauchansicht derselben Tiere). b – Einjähriges Jungtier. Man beachte, daß die leuchtend blaue schwanzfarbe im zweiten Kalender-Lebensjahr verblaßt und schließlich verschwindet.

(Figs. 5A-5b). in the week preceding eclo - gains volume rapidly after laying. To a sion, this increase is very small as eggs re - lesser extent this gain in width is continued duce their turgidity about 24 hours before during the second week of incubation, hatching. being the increase of longitude and width in the first week after deposition, the more synchronized during the third and eggs’ gain in volume and mass is not so fourth incubation weeks. Finally, egg much due to an increase in length (Fig. 6 A) length in creases abruptly while the growth but in width (Fig. 6b). The egg is laid with in width decelerates in the last week before a reasonable length, but the width is unpro - hatching. portionally small as determined by the incubation period.- The incu - opening size of the pelvis and the cloaca. it bation period lasts from 33 to 42 days (aver - is the increase in width from which the egg age 37.75 ± 0.86 days; N = 12 eggs) under Arribas_Iberolacerta_martinezricai_Reproduction:HERPETOZOA.qxd 02.03.2018 17:02 Seite 14

200 OscAr J. A rribAs

the conditions as outlined in ArribAs Dorsum and pileus of the hatchlings (2004b) and ArribAs & G ALAN (2005). are brown, finely spotted with black, in some in other Iberolacerta s. str. species the more pigmented specimens almost finely re - incubation period is of similar length, i.e., ticulated. costal (= temporal) bands with about 46 days in I. cyreni (bArbADiLLO black reticulation, leaving room for brown 1985) (but 32-33 days in two bejar clutch - centered ocelli, and a row of whitish ocelli es – ArribAs unpublished), 45-54 days in I. in their lower part. Legs also reticulated, monticola from the Galician coast at low with bright centered ocelli (Fig. 7A). The altitude ( GALáN 1991) and 37-41 days belly is white, with irregular spots originat - (biscHOFF 1984) or 40-47 days ( LJUbisAV - ing from the anterior edge of the ventral LJEVić et al. 2012) in I. horvathi . in the scales and decreasing in their extent from the subgenus Pyrenesaura , eggs are more external towards the innermost rows. sub - embryonated at the moment of deposition maxillary plates irregular but conspicuously and the incubation period is somewhat spotted (Fig. 7 A, inset). The color of the tail shorter, corresponding to the more extreme base passes gradually from the brown of the high mountain climate at the lizards’ habi - dorsum, across greenish brown, to a bright tat (on average 30, 34 and 36 days for I. turquoise blue that covers the main part of aranica , I. bonnali and I. aurelioi , respec - the tail, also stippled with very small black tively) ( ArribAs & G ALAN 2005). marks (Fig. 7A). The underside of the tail is Eclosion.- in the lab, eclosion also turquoise blue, stippled with black oc curred between 3:00 to 22:00 h (GTM) except the two central scale rows which are (average 9.40 ± 1,71 h; N = 12). The dura - almost immaculate (Fig. 7A, inset). tion of the eclosion, from the egg’s first Egg-teeth persisted from 8 to 36 hours crack until the total disentanglement of the after hatching (average 23.6 ± 2.57 hours; hatchling, lasted from 4.10 to 12.0 hours N = 10). (average 6.9 ± 1.1 hours; N = 6) (Figs. 3c- From 12 individuals hatched under lab 3D). conditions six were females and six males. Hatchling morphology and Iberolacerta martinezricai hatchlings behavior.- Hatchling sVL ranged from were able to autotomize their tail from 24.9 to 27.6 mm (average 26.11 ± 0.26 mm; birth. The hatchlings (1 cY) observed in N = 11) and body mass from 0.37 to 0.48 g nature had intact tails, thus the frequency of (average 0.41 ± 0.008 g; N = 11). New - tail loss in hatchlings must be low. The borns had 27-29 transversal series of ven - bright color of the juveniles’ tail disap - tral scales (average 28.27 ± 0.23; median = peared during their 2 cY (Fig. 7b) and 28; mode = 29; N = 11), the umbilical scar seemed to be an important component of being positioned beginning at ventral scale the antipredator strategy of hatchlings (e.g., rows 19-21 (average 20.09 ± 0.21; median cAsTiLLA et al. 1999; HAWLENA et al. 2006) and mode = 20) and ending at rows 21-24 Hatchlings of the batuecan Lizard (average 23.09 ± 0.28; median and mode = were able to attract the attention of potential 23; N = 11). predators to their tail by a striking whirling There were no significant correlations movement of its distal part, in a fashion that between hatchling and female sVL ( r = - adults are unable to do with their stiffer 0.25; t = -0.81, P = 0.44), or hatchling body tails, which are moved in cases of danger or mass and female sVL ( r = -0.39; t = -1.35, excitement, however only to a comparative - P = 0.21 ). ly limited extent.( ArribAs 2014a).

AcKNOWLEDGMENTs

Thanks are due to Javier carbonero, Miguel provided the corresponding capture permits for the Lizana, isabel Mateos and Pablo Garcia (salamanca, whole study of the species. No specimen was sacrificed spain) for they help when they developed the study for the study of the reproduction, which was entirely about the distribution and status of the species (2007- financed by the author. 2008) for the “Junta de castilla y León”. This agency Arribas_Iberolacerta_martinezricai_Reproduction:HERPETOZOA.qxd 02.03.2018 17:02 Seite 15

reproduction of Iberolacerta martinezricai (ArribAs , 1996) 201

rEFErENcEs

ArribAs , O . (1996): Taxonomic revision of the böHME , W. (Ed.): Handbuch der reptilien und Amphi- iberian ‘Archaeolacertae’ i: A new interpretation of the bien Europas. band 2/i (Echsen ii). Wiesbaden (Aula geographical variation of ‘ Lacerta ’ monticola bOULEN - Verlag). GEr , 1905 and ‘ Lacerta ’ cyreni MüLLEr & H ELLMicH , cArbONErO , J. & G ArcíA -D íAZ , P. & á ViLA , c. 1937.- Herpetozoa, Wien; 9 (1/2): 31-56. & A rribAs , O. & L iZANA , M. (2016): Distribution, ArribAs , O. (2004a): Nuevos datos sobre la dis - habitat characterization and conservation status of tribución de la lagartija batueca: Iberolacerta martinez- Iberolacerta martinezricai (ArribAs , 1996) in the ricai .- boletín de la Asociación Herpetológica Es- sierra de Francia, salamanca, spain.- Herpetozoa, pañola, salamanca; 15 (2): 96-97. Wien; 28 (3/4): 149-165. ArribAs , O. J. (2004b): characteristics of the re - cAsTiLLA , A. M. & G Osá , A. & G ALáN , P. & productive biology of Iberolacerta aurelioi (ArribAs , PérEZ -M ELLADO , V. (1999): Green tails in lizards of the 1994).- Herpetozoa, Wien; 17 (1/2): 3-18. Podarcis : do they influencie the intensity of pre - ArribAs , O. (2007): istòria Naturau e Evolu- dation?- Herpetologica, Lawrence; 55 (4): 530-537. cion dera cernalha Aranesa, Iberolacerta aranica . EMbErGEr , L. [rev. by GODrON , M.] (1983): Huesca (conselh Generau d’Aran; Gráficas Alós), pp. Vade-mecum pour le relevé méthodique de la végéta - 446. tion et du milieu: extrait du: “code pour le relevé ArribAs , O. J. (2013): Thermoregulation, activ - méthodique de la végétation et du milieu”. Paris ity and microhabitat selection in the rare and endan - (cNrs - centre National de la recherche scienti- gered batuecan rock Lizard, Iberolacerta martinezri - fique). 169 pp. cai (ArribAs , 1996).- Herpetozoa, Wien; 26 (1/2): 77- GALáN , P. (1991): Notas sobre la reproducción 90. de Lacerta monticola (sauria, Lacertidae) en las zonas ArribAs , O. J. (2014a): Growth, sex-dimor - costeras de Galicia (Noroeste de España).- revista phism and predation pressure in the batuecan Lizard, Española de Herpetología, salamanca; 5: 109-123. Iberolacerta martinezricai (ArribAs , 1996).- butlletí GALáN , P. (1997): reproductive ecology of the societat catalana Herpetologia, barcelona; 21: 147- lacertid lizard Podarcis bocagei .- Ecography, 173. København; 20: 197-209. ArribAs , O. J. (2014b): Iberolacerta cyreni (L. GALáN , P. (1999): Demography and population MüLLEr & H ELLMicH , 1937); pp. 383-398. in: dynamics of the lacertid lizard Podarcis bocagei in sALVADOr , A. (Ed.): . Fauna ibérica. Vol. 10. Northwest spain.- Journal of Zoology, London, 249: Madrid (Museo Nacional de ciencias Naturales. 203-218. consejo superior de investigaciones cientí ficas GALáN , P. (2009): Ecología de la reproducción (csic)). de los saurios ibéricos.- boletín Asociación Herpeto- ArribAs , O. J. (2014c): Iberolacerta galani lógica Española, salamanca; 20: 2-34. ArribAs , c ArrANZA & O DiErNA , 2006; pp 398-409. in: GALáN , P. (2011): Iberolacerta monticola (can- sALVADOr , A. (Ed.). reptiles. Fauna ibérica. Vol. 10. tabrian rock Lizard). Longevity.- Herpetological re- Madrid (Museo Nacional de ciencias Naturales. view, New York; 42 (3): 430. consejo superior de investigaciones cientí ficas HAWLENA , D. & b OOcHNiK , r. & A brAMsKY , Z. (csic)). & b OUsKiLA , A. (2006): blue tail and striped body: ArribAs , O. J. (2014d): Iberolacerta martinez- why do lizards change their infant costume when grow - ricai (ArribAs , 1996); pp. 409-419. in: sALVADOr , A. ing up?- behavioral Ecology, New York; 17: 889-896. (Ed.): reptiles. Fauna ibérica, vol. 10. Madrid (Museo HiNTZE , J. (2007): Ncss, PAss and GEss. Nacional de ciencias Naturales. consejo superior de Number cruncher statistical systems. Kaysville, Utah. investigaciones cientí ficas (csic)). WWW document and software available at < http:// ArribAs , O. J. (2014e): Iberolacerta monticola www.ncss.com > (last accessed: December 30, 2017). (bOULENGEr , 1905); pp. 419-432. in: sALVADOr , A. LJUbisAVLJEVić , K. & G LAsNOVić , P. & K ALAN , (Ed.). reptiles. Fauna ibérica, vol. 10. Madrid (Museo K. & K rYšTUFEK , b. ( 2012): Female reproductive char - Nacional de ciencias Naturales. consejo superior de acteristics of the Horvath’s rock lizard ( Iberolacerta investigaciones cientí ficas (csic)). horvathi ) from slovenia.- Archives of biological ArribAs , O. J. & G ALAN , P. (2005): repro- sciences, beograd; 64 (2): 639-645. ductive characteristics of the Pyrenean High-Mountain LUcA , N. DE (1989): Taxonomic and biogeo - Lizards: Iberolacerta aranica (ArribAs , 1993), I. aure - graphic characteristics of Horvath’s rock lizard lioi (ArribAs , 1994) and I. bonnali (LANTZ , 1927).- (Lacerta horvathi MéHELY , 1904 Lacertidae, reptilia) Animal biology, Leiden; 55 (2): 163-190. in Yugoslavia.- scopolia, Ljubljana; 18: 1-48. bArbADiLLO , L. J. (1985): Nuevos datos sobre LUcA , N. DE (1992): Notes on biology and ecol - la reproducción de Lacerta monticola (Lacertidae, ogy of the Horváth´s rock lizard ( Lacerta horvathi reptilia) en España central.- Doñana, Acta Vertebrata, MéHELY , 1904, reptilia: Lacertidae); pp 129-135. in: sevilla; 12: 189-196. KOrsós , Z. & K iss , i. (Eds.): Proceedings of the 6th bAUWENs , D. (1999): Life-history variations in Ordinary General Meeting of the societas Europaea lacertid lizards.- Natura croatica, Zagreb; 8: 239-252. Herpetologica, 19-23 August 1991, budapest. bAUWENs , D. & DíAZ UriArTE , r. (1997): MOrEirA , P. L. & A LMEiDA , A. P. & D ELGADO , covariation of life-history traits in lacertid lizards: a H. & s ALGUEirO , O. & c rEsPO , E. G. ( 1999): bases comparative study.- American Naturalist, chicago; para a conservação da lagartixa-da-montanha ( Lacerta 149: 91-111. monticola ). Lisboa (instituto da conservação da biscHOFF , W. (1984): Lacerta horvathi MéHELY Natureza, Ministerio do Ambiente), pp. 68. [Estudos de 1904 – Kroatische Gebirgseidechse; pp. 265-276. in: biologia e conservação da natureza, nº 25.] Arribas_Iberolacerta_martinezricai_Reproduction:HERPETOZOA.qxd 02.03.2018 17:02 Seite 16

202 OscAr J. A rribAs

PérEZ -M ELLADO , V. & M árQUEZ , r. & M ArTí - lizard: Lacerta monticola (squamata, Lacertidae) in NEZ -s OLANO , i. (2009): Iberolacerta martinezricai . in: north-west spain.- Animal biology, Leiden; 53 (4): iUcN 2011. iUcN red List of Threatened species 347-366. 2009. Version 2011.2. WWW document available at sOKAL , r. r. & r OHLF , J. (1969): biometry. The < www.iucnredlist.org/details/full/61516/0 > [last principles and practice of statistics in biological accessed: December 30, 2017]. research. New York (Freeman and company). pp. 776. rúA , M. & G ALáN , P . (2003): reproductive characteristics of a lowland population of an alpine

DATE OF sUbMissiON: December 26, 2016 corresponding editor: Heinz Grillitsch

AUTHOr: Oscar J. ArribAs < [email protected] >, Avda. Fco. cambó 23; 08003 barcelona, spain.