AnimalBiology ,Vol.53, No. 4, pp. 347-366 (2003) Ó KoninklijkeBrill NV ,Leiden,2003. Alsoavailable online - www.brill.nl

Reproductive characteristics of alowland population of an alpinelizard: Lacerta monticola (Squamata, Lacertidae) innorth-west Spain

1 MARTA RÚA ,PEDROGALÁ N ¤

Departamentode Bioloxía Animal,Bioloxí a Vexetale Ecoloxía, Facultadde Ciencias,Universidad deACoruña, Campus de AZapateira,s/ n,15071-ACoruñ a, Spain

Abstract—Westudied the reproductive ecology of a populationof the lacertid lizard Lacerta monticola ata lowlandlocation in A Coruña (NW Spain)from 1997 to 2002. The timing of the reproductivecycle was examined based on mark-recapture records of individuallizards in theŽ eld. Thecharacteristics of theeggs and hatchlings were obtained from clutches laid in thelaboratory by pregnantfemales that were temporarily removed from the study area. Our results indicate that mating tookplace between late March and July. The smallest female with signs of sexual maturity had a snout- ventlength (SVL) of52.4mm andthe smallest male was 50.7 mm. Sexualmaturity was attained at theage of 2 yearsby 41% of theindividuals, while the remaining 59% of the lizards matured at the ageof 3years.The laying period occurred between June and the beginning of August considering all years.About 61% of the reproductive females produced a singleclutch annually, while 39% of the femalesproduced two clutches per year. Females that produced two clutches were generally larger (averageSVL 70.9mm) thanthose that laid a singleannual clutch (average SVL 62.6mm). The D D meanclutch size was 6.4 eggs (range 4-9). Both clutch size and clutch mass increased signiŽ cantly withfemale SVL. Themean egg mass in a clutchdecreased signiŽ cantly with clutch size. Hatching occurredbetween August and September. Hatching success in the laboratory was 71.7%. The mean SVL washigher in femalehatchlings than in males.

Keywords: clutches; Lacertamonticola ;Lacertidae;life history; NW Spain;reproduction; reptiles; sexualmaturity.

INTRODUCTION Theecology of reproduction explores the patterns ofcovariation among life his- torycharacteristics suchas the modeand timing ofreproductive events, age and

1E-mail:[email protected] *Correspondingauthor. E-mail: [email protected] 348 M.Rúa, P.Galán size at maturity,frequencyof reproduction, clutch size, size andmass ofeggs and hatchlings,etc. (Dunham,1981, 1994; Gillis andBallinger, 1992;Bauwens, 1999). Rigorousdata are neededto undertakea studyof the generalpatterns ofthe repro- ductiveecology and life history oflizards. Thesedata must include,for instance, clutch characteristics fromeggs laid recently undercontrolled conditions, clutch frequencyfrom marked females inpopulations being monitored, characteristics of the hatchlings,the success rate ofhatching, etc. Also ofutmost importanceis the ability to relate all ofthese characteristics to those ofthe female progenitors.These kindsof studies are scarce inlacertid lizards (Pilorge et al., 1983;Barbault andMou, 1988;Bauwens and Dí az-Uriarte, 1997;Galá n, 1997;Bauwens, 1999; Castilla and Bauwens,2000a, b). Recently,the Iberianrock lizard, Lacerta monticola ,becamea modelorganism forstudies ofbehaviour (Martí n andLó pez, 1999, 2000, 2001), the effect ofcaudal autotomy(Martí n andSalvador, 1995, 1997), and chemical communication(Ló pez et al., 1998;Aragó n et al., 2000).However, these studies address populations inhabitingthe highmountain areas ofcentral Spain(Sierra deGuadarrama) and that belongto the clearly differentiated taxon L. m. cyreni (see below).The northwesternmostpart ofthe IberianPeninsula is knownto have populations of this species, whichare uniquein that theylive in the lowlands(Galá n, 1982), traditionally assigned to the subspecies L.m.cantabrica .Atpresent,very little is knownabout the ecological characteristics anddemography of these animals (Braña et al., 1990;Galá n, 1991). TheŽ rst studies dealingwith the reproductionof L.monticola wereconducted on the subspecies livingin highmountain areas in central Spain, L. m. cyreni (Palacios andSalvador, 1974; Melendro and Gisbert, 1976;Barbadillo, 1985; Elvira andVigal 1985).This taxonis consideredby some authorsto be adifferent species, whichthey denominated L. cyreni (Arribas,1996, 1999; Mayer and Arribas, 1996; Odierna et al., 1996).More recent studies havebeen published on the nominalsubspecies, L. m.monticola ,whichis endemicin the Serra daEstrela, the central mountainrange ofPortugal(Matos, 1988;Moreira et al., 1999).With regardto the forminhabiting the northwest area ofthe IberianPeninsula, L.m.cantabrica ,acertain amount ofinformationhas beencompiled on both the mountain-dwellingpopulations and those livingon the Cantabriancoast whichlive in areas with verydifferent altitudes (Braña, 1983; Brañ a et al., 1990),as well as the populationsinhabiting the low altitude zonesof Galicia (Galán, 1991). Lastly, diverse data onthe reproductive characteristics ofthis species havebeen published in moregeneral studies on the reproductionof Iberian or Palearctic lacertid lizards (Braña et al :; 1991; 1992 I Bauwensand Dí az-Uriarte, 1997;Bosch and Bout, 1998). Ouraim was to describe the reproductivecycle andreproductive characteristics of alowlandpopulation from north-western Spain, belonging to the well-differentiated subspecies Lacerta monticolacantabrica .It is ofutmost importanceto compile informationon the ecological characteristics anddemographic tendencies ofthese Reproductionof Lacertamonticola lowlandpopulation 349 populations,since, owingto their isolation, their small area ofdistribution andthe scarcity ofindividuals, they are consideredto bethreatened(Galá n, 1999a).

MATERIALAND METHODS

Studyspecies

TheIberian rock lizard, Lacerta monticola Boulenger,1905, is adiurnallacertid lizard foundmainly in the rockyhabitats ofhigh altitudes in several mountain rangesof the IberianPeninsula: the Sistema Central mountains,in central Spain (subspecies orspecies cyreni),the Serra daEstrela mountainsin Portugal (sub- species monticola),and the Cantabrianmountains in northern Spain (subspecies cantabrica).Incontrast withits afŽnity for mountains, it is also foundat sea level, fromaltitudes of0 to400-500 m onthe damp,north-facing slopes anddeep river valleys in the northof Galicia andwest ofAsturias, north-westSpain (Elvira and Vigal,1982; Galá n, 1982;Pé rez-Mellado, 1997, 1998, 2002). Recent studies found anunexpectedly close genetic similarity betweenthe populationsof Galicia andthe Serra daEstrela, as well as aconsiderablegenetic differentiation betweenthe Gali- cian andCantabrian populations, both included in the same subspecies, L.monticola cantabrica (Almeida et al., 2001).

Study area

Thestudy area is located at the endof the geographicensemble composedof the lowerbasin ofthe MandeoRiver (Betanzos,Coiró s andPaderne municipalities, A Coruña province,NW Spain,8 ±80W and 43±150N;UTM:29TNJ 79),which forms asteep valley ofuvial erosion.The altitude ofthe area inhabitedby the population of L.monticola rangesfrom 20 m abovesea level (Chelo)to up to 150m (Zarzo). This area is includedin the Wet Oceanicclimatic type,characteristic ofcoastal areas ofthe north-westIberian Peninsula. The annual rainfall andtemperature data from twometeorological stations nearthe studyarea are shownin table 1.

Table 1. Meteorologicaldata from the meteorological stations of Irixoaand Betanzos, 6 and5 kmrespectively fromthe study area. Data from Martí nez-Cortizas et al. (1999).

Meteoro-Longitude Latitude Altitude A verageA verageTemperature T emperature logical annualannual of the of the station temperaturerainfall coldest hottest (±C) month month

Irixoa 8±60W 43±170N 398 m 11.9± 1107 mm 6.7±C 17.6±C Betanzos 8±120W 43±160N 38 m 12.1± 909 mm 7.0±C 16.6±C 350 M.Rúa, P.Galán

Datacollection in the Želd Data onthe annualactivity cycle ofthis populationwere gathered between July 1997and October 1998 and between March and September in 1999,2000, 2001 and2002. These times coincidewith the activity periodof this species. During this period,the studysite was visited oneto four times everymonth, on days with favourableweather conditions, conducive to lizard activity.Oneach visit, weset outto collect, byhandor bynoosing, the greatest possible numberof specimens. Foreach lizard caughtwe recordedsex, age class, snout-ventlength (SVL, to the nearest 0.1mm usingsteel callipers), tail length(including regenerated parts), mass (tothe nearest 0.1g with aPesola dynamometer),dorsal andventral coloration, numberof blue spots onthe ventral scales and anks,as well as the arrangement ofthe cephalic plates. Foreach lizard observedin the Želd wealso recordeddetails ofall reproductiveevents detected,such as courtships andmatings. Eachlizard was markedindividually by toe clippingand was processedquickly ( <5 min) at the capturesite, andreleased immediately. Threeage classes couldbe distinguished, mainly onthe basis ofbody length (SVL)and other external signs (see below):juveniles (lizards bornin the present year),sub-adults (lizards bornin the precedingyear or 2years olduntil theyreached sexual maturity) andadults (after the onset ofsexual maturity). All the results reportedin this study,includingthe timing ofannual activity andof reproductiveevents, were obtained from live specimens, byobserving their behaviourin the Želd andby the successive markingand recapturing of the animals. Thetime ofonset andduration of the mating season was determinedby the presence ofrecent mating scars (copulationmarks) onthe bodiesof the females andby the matingbehaviour observed in the Želd.The gravidity period of the females was evaluatedby ventral palpationto detect enlargedovarian follicles oroviductal eggs. Theegg-laying period was evaluatedfrom the Žrst tothe last clutch ovipositedin the laboratoryand by females observedin the Želd with lateral skin folds,which is indicative ofarecent egg-layingevent. The hatching period was determinedby the juvenile hatchlings inthe laboratoryand by the juveniles, observedin the studyarea, showingan open navel scar, andhaving the hatchlingsize recordedin the laboratory (SVL < 32mm). The hatching period lasted until all hatchlings exhibiteda closed navel scar. Theattainment ofsexual maturity was identiŽed in females byreproductivesigns suchas the presenceof mating scars ontheir bodies,enlarged ovarian follicles oroviductal eggs determined by ventral palpation.Sexually mature males were identiŽed by a developedhemipenes, determined by the enlargedbasal portion ofthe tail. Anothersign of sexual maturity inmales is the brightgreen ventral colorationthat is present onlyin mature individuals.Field observationsof courtship andmating behaviourwere also recordedto determine sexual maturity.Ageat maturity was investigated byreference to recordsof juveniles bornand marked duringtheir Žrst yearof life in1997, 1998 and 1999, and recaptured during 2000, 2001and 2002. Although a large numberof hatchlings weremarked, only 39 were Reproductionof Lacertamonticola lowlandpopulation 351 recapturedduring the following3 years.The reason for this lowrecapture rate is probablythe highmortality rate andthe fact that the youngage classes travel longer distances. Mark-recapturerecords for a numberof females caughtduring the breeding season of1998, 1999, 2000, 2001 and 2002 provided information on clutch frequency.In a small portionof reproductivefemales, it was possible to ascertain successive clutches ofthe same female, as well as to Žndoutif it laid onlya single clutch perseason.

Datacollection in the laboratory BetweenMay and July of 1998, 2000, 2001 and 2002, a numberof pregnantfemales werecollected fromthe studyarea andtemporarily transportedto the laboratory. Inthe laboratorythe females werehoused in terraria withdirect exposureto an artiŽcial light that created athermal gradientfor 12 hours a day(roughly from sunrise to sunset). Foodconsisting ofa variety ofinsects andwater wereprovided adlibitum. Therest ofthe time, gravidfemales wereplaced individually in plastic boxes (25 13 6cm) Žlled with4 cm ofsoil fromthe studysite. Theses boxes wereprovided £ for £ oviposition. The airtight seal ofthe plastic boxesallowed the natural humidityof the soil to bemaintained, thus preventingdehydration of the eggs.These boxes were kept in the laboratoryat roomtemperature (20-25 ±C). We inspected the boxeswith the gravidfemales everymorning. All clutches werelaid in these plastic boxescontaining soil. Followingoviposition, females weremeasured (SVL),weighed and then released at the capturesite. Theeggs were dug up and carefully removed,weighed (to the nearest 0.001g) andmeasured (maximum length andwidth, to the nearest 0.01mm), and their viability judgedby the external characteristics ofthe eggshell.Clutch mass was calculated as the sum ofthe masses ofthe eggs.Egg volume was estimated as V 4=3¼a2b, where a 1=2 of the shortest diameter and b 1=2ofthe largestD diameter.Eggcharacteristics D were in all cases determinedwithin D 8hoflaying. In all cases eachclutch was able to beunequivocally assigned to anindividual female, resulting in the calculation of relative clutch mass (RCM) as the ratio ofthe clutch mass (immediately after laying) to the mass ofthe female after laying.Each clutch was incubatedindividually in the same plastic boxuntil hatching.The eggs were incubated at roomtemperature, but anadditional heat sourcewas providedfor 5 hadayby a 100W light bulbplaced 15cm abovethe boxes,which gave a temperature rangeof 20-29 ±C,just like the oneobserved in the studyarea (unpubl.data). To ensure near-natural conditions of humidity,the clutches werechecked daily sothat anyexcess humidityin the form ofwater that hadcondensed on the coverof the boxescould be removed, and thus preventmould from forming. Immediately after hatching,hatchlings wereweighed ( 0.001g) and measured (SVLand tail length; 0.1mm). The sex ofhatchlings § was determinedby mor- phologicalcharacteristics, § suchas the dorsal pattern andthe numberof transverse rowsof ventral scales (Galán, 1991, 1997). Female hatchlings haveuniformly dark 352 M.Rúa, P.Galán

anksand the numberof transverse rowsis greater than27. Males havea slightly lighter spotted pattern in the ankswhich gives them amorereticulated appearance, andthe numberof transverse rowsis fewerthan 27 (Galán, 1991).After recording the data,hatchlings weremarked individually and released at the studysite. Hatch success inthe laboratorywas estimated onthe basis ofthe ratio ofthe numberof eggsnormally hatched to the total numberof eggs in eachclutch.

Statistical analysis

All statistical analyses weredone with the Statview III,SPSS (version 11.0), andStatistica (version5.97) statistical packages.In the text, wereport mean values 1standarderror (SE). When analysis ofvariance (ANOV A)andother parametric§ statistical tests wereused, we Ž rst conŽrmed normality, independence andhomoscedasticity ofthe data.Multiple comparisonsof the means following the varianceanalyses werecarried outby Scheffé ’s test. Weusedcorrelation and simple regression analyses toexamine the relation betweentwo variables. Whena third variable correlated with both,we usedresidual analysis, checkingstatistically forthe effect ofthe third variable (all variables werelog-transformed prior to the analyses). All statistical tests wereused with asigniŽcance level of p < 0:05.

RESULTS

Annualactivity cycle andreproductive season

BetweenNovember and the beginningof February no individuals were seen at the studysite. This time coincides with the winter inactivity periodduring all the studyyears (1997-2002).The activity season lasted fromlate Februaryto October. BetweenFebruary and late March,lizards wereseen to beactive, butwithout anysigns ofreproductive behaviour .Thesex ratio ofthe lizards observedduring Februaryand March in 1998,2000, 2001 and 2002 did not differ signiŽcantly from one-to-one( Â2 test, p > 0:05in all cases). Themating season lasted fromlate Marchto the beginningof August.The Ž rst females with mating scars wereobserved in late Marchin 1998or early April in 1999,2000, 2001 and 2002, and the last onein mid-July (all the studyyears). The gestation period(females with oviductaleggs, determined by palpation)lasted from early Mayto mid-July (all the studyyears). In the laboratorythe clutches were laid between17 June and 7 Augustin 1998and between 25 June and 19 July in 2002.The incubation period lasted fromlate Juneto mid-September and hatching occurredbetween August and September .Atthe endof September, all hatchlings exhibiteda closed navelscar .Theactivity season ofthe hatchlings lasted from August,when hatching starts, until the endof October. Reproductionof Lacertamonticola lowlandpopulation 353

Sexualdimorphism Althoughsome females attained alarger SVLthanmales, there wereno differences betweenthe sexes in meanSVL (males: 65 :90 0:71 mm, range 50.7-76.5mm, n 59;females: 64 :47 0:56 mm, range 52.4-79.0§ mm, n D118; t 1:522, p D> 0:10). § D D D Dorsal colorationshowed a markedsexual dimorphism.Adult males havea bright greendorsal colorationwhereas females are brown.V entral colorationis also bright greenin adult males, while females are pale green.Older males also havesome blue spots onthe edgesof the external ventral scales.

Sexualmaturity Thesmallest female showingsigns ofsexual activity (oviductaleggs and mating scars) hada SVLof52.4mm, but we observeda female measuring56.0 mm that was still immature. Thereforethe size at whichfemales attain sexual maturity ranges between52.4 and 56.0 mm. Thesmallest male withan enlarged basal portionof the tail (signof adeveloped hemipenes)and bright green ventral colorationhad a SVLof50.7 mm, but we collected animmature male measuring51.8 mm. Thus, the size at whichmales attain sexual maturity varies between50.7 mm and51.8 mm. Recapturedata oflizards markedduring their Žrst yearof life allowedus to ascertain the ageat whichthe minimummaturity size is attained. Overall,41% (n 39)of the individualsattained sexual maturity at 2-yearsold (3rd calendar year)D and the remaining59% do so at 3-yearsold (4th calendar year). The proportionsof individualsmaturing at 2-yearsold or later donotdiffer signiŽcantly betweenthe sexes (  2 0:61, p 0:43). D D Clutch frequency Ofthe 33reproductive females with asufŽcient numberof recaptures fromMay toJuly/ Augustto provideinformation on clutch frequency,20 females (61%)laid onlyone clutch, whereas 13 females (39%)produced two clutches peryear. Females that laid onlyone clutch wereon averagesmaller (SVL:62 :56 0:81mm, range: 55.5-69.7mm) thanthose producingtwo clutches peryear (SVL: §70 :88 1:11 mm, range:65.0-79.0 mm; t 6:18, p < 0:0001).Only the largest females§ (SVL > 65:0mm),that wereat leastD in their 4thcalendar year (3 or moreyears old)appear to beable to lay twoclutches peryear. Recapture records made it possible forus to determine.The Žrst clutch was producedin Juneand the secondclutch in July,after aninterval of20-30days. On the otherhand, females that attain sexual maturity in their third activity season lay onlyone clutch at the endof the layingseason.

Clutch size Therewere no statistically signiŽcant among-yeardifferences inmean female SVL,meanclutch size, meanegg mass, meanclutch mass orrelative clutch mass 354 M.Rúa, P.Galán

Table 2. Reproductivecharacteristics of Lacertamonticola fromthe Mandeo basin (A Coruña). Shown are the mean 1SE, D.S.:the standard deviation, range and sample size (N). § Mean S.E. D.S. Range N § FemaleSVL (mm) 67:28 0:53 3.92 59.70-78.0 54 § Femalemass (g) 4:92 0:09 0.73 3.50-6.90 54 § Clutch size 6:41 0:18 1.34 4-9 54 § Clutchmass (g) 2:631 0:08 0.57 1.493-3.880 54 § Relativeclutch mass 0:539 0:01 0.11 0.325-0.818 54 § Egg mass (g) 0:417 0:01 0.06 0.291-0.554 54 § Egglength (mm) 12:62 0:09 0.68 11.10-14.13 54 § Eggwidth (mm) 7:83 0:06 0.41 6.88-8.80 54 § Eggvolume (mm 3/ 407:62 7:36 54.13 293.64-535.23 54 § HatchlingSVL (mm) Males 25:46 0:08 1.01 23.00-28.10 134 § Females 26:21 0:11 1.26 22.90-29.50 114 § Hatchlingmass (g) Males 0:410 0:004 0.05 0.288-0.625 134 § Females 0:406 0:006 0.06 0.245-0.611 114 §

(ANOVA: p > 0:05in all cases). Therefore,we lumpeddata forthe 4years (1998, 2000,2001, 2002) for further analyses. Consideringall the clutches, the mean clutch size was 6.4eggs, with arangeof four to nineeggs (table 2).Clutch size increased signiŽcantly withthe mother’s SVL,consideringall clutches ( r 0:61, p < 0:0001)(Ž g. 1). D Ina small sample ofreproductive females, wewere able to identifysuccessive clutches fromthe same female (Žrst and/orsecondclutch), as well as to determine whetherit laid onlya single annualclutch (table 3).There were signiŽ cant differences in clutch size amongthe three classes ofclutches (ANOVA, F2;23 17:07, p < 0:0001).The Ž rst clutch was larger thanthe secondannual clutch D (Scheffé’s aposteriori test: F 16:56, p < 0:001),and than the single annual clutch (F 4:14, p < 0:05). D D Clutch characteristics Female reproductivecharacteristics andclutch/ eggcharacteristics, takinginto con- sideration all the clutches studied,are summarised intable 2.Meanegg mass ina clutch was notrelated tofemale SVL( r 0:14, F1 53 1:09, p 0:301) but D ¡ ; D D decreasedsigniŽ cantly with clutch size ( r 0:36, F1;53 7:84, p 0:0072) (Žg. 2).An analysis ofthe relationships betweenD ¡ residuals fromD the regressionD of log(clutch size) onlog (female SVL)andresiduals fromthe regression oflog (meanegg mass) onlog (female SVL)revealeda negativerelation betweenthe twosets ofresiduals ( r 0:36, F1;53 7:86, p 0:007)(Ž g. 3). Hence, larger clutches werecomposed Dof ¡smaller eggsDand this relationD is independentof female SVL.Therewere no signiŽcant differences inegg mass betweenthe single annual Reproductionof Lacertamonticola lowlandpopulation 355 f n i o 6 6 6 6 6 6 6 6 N e h l c t p u l m 0 4 2 6 6 c a s 3 0 3 0 0 0 5 . . e 5 3 5 5 0 l l e 3 . . . . 4 . l g g 7 5 6 3 0 0 1 8 a h n n ------c i a m 0 0 4 3 4 3 0 5 t s s u 0 6 9 2 7 2 5 R . . . . l a 4 3 3 a c 5 4 . . . 2 7 d 6 1 0 0 1 y d i l a n n l o o t c a e d h 6 7 3 2 1 e S E 5 2 8 t 4 2 0 0 3 n S 1 4 0 : : : : : i s : : : 1 1 0 0 0 0 a e 0 0 0 n t l o b a § § § § § § s § § § o m a n 5 1 4 0 3 1 7 3 e e e a 6 5 0 3 8 f s 9 6 7 : : e 1 4 4 : : : w 9 : : : 2 f r 4 4 7 t M e 6 2 0 0 1 o a p h n t s . o e s e w t h a o c 2 2 2 2 2 2 2 2 o l e t N s 1 1 1 1 1 1 1 1 N e u l r . g c e r n e i o w t t d s w e a 0 2 4 7 3 l e e T 0 0 0 6 8 3 1 t r . . e 9 7 7 5 8 a e . . b 9 . . . 4 r h g t 7 6 9 3 0 0 1 8 e e n ------h r n a 0 0 5 0 6 1 0 7 c m i u t 6 1 5 4 0 9 1 t R a . . . . u 9 4 2 h s p l 3 7 8 . . . 1 c a c t 6 1 0 0 1 e c t u h e l s t r r c i e m F d h o t n 2 7 3 2 2 E r 5 1 2 o 8 1 0 0 2 f S d 2 3 1 : : : : : c : : : 1 n s 0 0 0 0 0 e 0 0 0 a e s h § § § § § § h d § § § c t t r n 1 0 8 3 8 n 9 7 3 i u a a 0 1 9 9 4 l 0 6 9 b : : e 0 5 3 t : : : c 1 : : : 2 s 5 7 7 h t M r 7 3 0 0 1 c n Ž a e e r e e r h f t e f t i 6 6 6 6 6 6 6 6 f N n d a e e n d i n e w t s o e s a 0 0 5 0 4 M a e b 4 5 4 5 2 5 9 l C e . . 0 2 5 7 5 e e s g 8 . . . . 3 . R r g n r 5 7 8 6 3 0 0 1 i n ------e e d t r a 0 5 5 0 9 3 7 0 a p n e i 4 5 7 7 4 8 3 a R t . . . . h 7 4 3 w n c 1 3 . . . 1 7 s t e s s 6 1 0 0 1 r u a d l e r f c m a f i z e i d l d l n g 1 5 5 3 7 , E l 5 0 5 a s n l 0 2 0 0 2 S i 2 4 1 : : : : : e a : : : e s 1 1 0 0 0 0 h 0 0 0 z e c i e s t s § § § § § § n u § § § u l a n 8 0 9 3 3 g O 0 7 8 c c a g 8 5 2 4 7 2 1 7 : : e e e 6 6 4 : : : o 5 : : : 2 b 7 4 6 M d 6 2 0 0 1 w , t n h a c g t n h u i l c y t c h a t u l r l d i c n e b s , o r s o c e s e h t s a t f s s ) a a m a d , ) m n ) ) m d d ) a i g m m n g m h ( a ( ( a y l c m ) s r t m ( t s L s g e ( o u a s ( e t a l z h V a i h h z t a c s t t i s r S m . s g s m e d o s a 3 r n i e e v e l b l e h h e i l e m l w t a a a c c h l a l t t t a l g g g b m m u u o e m l l e g g g a e e e h T M t f F F C C R E E E 356 M.Rúa, P.Galán

Figure 1. Relationshipbetween mother’ s bodysize (snout-vent length, SVL) andclutch size consideringall clutches from 1998, 2000, 2001 and 2002.

Figure 2. Relationshipbetween clutch size and mean egg mass. clutch andthe Žrst andsecond subsequent clutch fromthe same reproductivefemale (ANOVA: p > 0:05;table 3). Clutch mass increased signiŽcantly withfemale SVL( r 0:53, F1;53 20:42, p < 0:0001),but relative clutch mass was notrelated to theD lengthof the D female (r 0:12, F1 53 0:774, p 0:383).There were signiŽ cant differences in clutch D ; D D mass (ANOVA: F2;23 3:99, p 0:03)among the single annualclutch andthe Žrst D D Reproductionof Lacertamonticola lowlandpopulation 357

Figure 3. Relationshipbetween residual deviations of clutch size (residual values of theregression oflog-clutchsize on log-mother’s SVL) andresidual deviations of mean egg mass (residual values of theregression of log-eggmass on log-mother’ s SVL).

andsecond clutches ofthe same reproductivefemale. Anaposteriori Scheffétest revealedsigniŽ cant differences betweenthe Žrst andsecond clutches ( F 3:96, D p < 0:05;table 3).Likewise there was asigniŽcant differencein relative clutch mass amongthe three categories ofclutches (ANOVA: F2 23 8:32, p 0:002). ; D D Anaposteriori Scheffétest revealedsigniŽ cant differences in RCMbetweenone single clutch perseason andthe secondclutch ( F 6:59, p < 0:01)and between D the Žrst andsecond clutches ( F 6:53, p < 0:01;table 3). D

Hatchlingsand hatching success

HatchlingSVL andmass, measuredwithin 24 h ofhatching, are shownin table 2. Female hatchlings hada larger SVLthanmales ( t 5:09, p < 0:0001),but there D wereno between-sexdifferences in bodymass ( t 0:47, p 0:64).The sex ratio D D ofhatchlings bornin the laboratorywas 1:0.85(134 males to 114females) anddoes notdiffer signiŽcantly fromone-to-one (  2 1:62, df 1, p 0:20). D D D Themean SVL ofhatchlings in aclutch was positively related tothe meanmass of the eggs (r 0:59, F1 45 24:35, p < 0:0001). D ; D Ofthe 346eggs pertaining to 54clutches that wereincubated in the laboratory, 248eggs hatched successfully, correspondingto ahatchingsuccess of71.7%. In eight outof 54clutches all eggsfailed to hatch. 358 M.Rúa, P.Galán

DISCUSSION Activity cycle Themild, temperate climate in the studyarea allows L.monticola toremain active fromlate Februaryto October.Aconsequenceof this longperiod of annualactivity is alongbreeding season (ca 4months),which enables some individualfemales to producetwo clutches duringthe same reproductiveseason. In this study,mating commencedin late Marchand the last eggswere laid at the beginningof August. Inother studies on L.monticola fromNW Spain,the breedingseason started later (Braña et al., 1990;Galá n, 1991). In populations living in areas with harshclimatic conditions,such as the mountainpopulations of L.monticola andof otherlacertid lizards, the breedingseason starts muchlater thanin coastal populationsand males tendto commencemating as soonas females becomeactive after the winter (Saint- Gironsand Duguy ,1970;Goldberg, 1974; Mellado andOlmedo, 1987; Hraoui- Bloquetand Bloquet, 1988; Brañ a et al., 1990).Females ofthis populationlaid eggsbetween mid-June and the beginningof August.In the mountainpopulations ofcentral Spainthe layingperiod starts later andis shorter,taking place between July andAugust (Pé rez-Mellado, 1982; Barbadillo, 1985). Duringtheir winter activity,bothmales andfemales are equallyactive. Also, the beginningof full activity, at the endof winter, occurs at the same time in bothsexes. Inother lacertid lizard species fromtemperate areas, different authors havereported that the onset ofannualactivity inmales begins2-3 weeks before it occursin females (Nulandand Strijbosch, 1981;Bauwens et al., 1989;Galá n, 1989; Nicholsonand Spellerberg, 1989; Marco et al., 1994).

Sexualmaturity Mark-recapturedata provideprecise knowledgeon the minimumbody size andage at which L.monticola fromA Coruña reachedsexual maturity.Inthis population, individualsbecome sexually mature uponattaining aminimumbody size, rather thana minimum age,as inother lacertid lizard species (Spellerberg,1982; Heulin, 1985;Bauwens and V erheyen,1987; Galá n, 1996a; Bauwens, 1999). Females mature at aminimumbody length (SVL) of52.4 mm andmales at 50.7mm. Inanother coastal lowlandpopulation of L.monticola ,Galán (1991)reported a minimumbody size at maturity that was slightly larger in females (SVL:53.5mm). Bauwensand Dí az-Uriarte (1997)reported a minimumlength at maturity of56 mm for the L.m.cantabrica subspecies. Thereare important differences amongcoastal populationsof L.monticola andthe populationsof the Sistema Central ( L.monticola cyreni).Theminimum body size inadults ofthe latter populationsis 65.8mm SVLin females and61.2 mm inmales (Elvira andVigal, 1985), or 60 mm in females (Bauwensand Dí az-Uriarte, 1997).Unpublished data wouldpoint to the presenceof copulation marks at aminimumSVL of57-59 mm in females in the Sierra deGredos and 58.5 mm in the Sierra deGuadarrama (Oscar Arribas,pers. Reproductionof Lacertamonticola lowlandpopulation 359 comm.).Hence, lowland populations attain sexual maturity at asmaller bodysize, andpossibly at ayoungerage than in the mountainpopulations. Bothsexes ofthe L.monticola populationstudied herereached sexual maturity at 2or3 years old(3rd or 4thcalendar year). Recapture records allowed us to observe that the earliest bornhatchlings (hatchedin early Augustuntil early September) attained sexual maturity beforethe endof the mating season oftheir 3rdcalendar year(mid-June or July) andparticipated in reproduction.Hatchlings that wereborn after mid-Septemberreach the sexually mature size nearthe endof their third activity season,so that theydelay reproduction to the followingspring (4th calendar year). Despite differences inage at maturity dueto the timing ofhatching,differences in ageat maturity betweenindividuals ofthe same cohortmay also beattributed to particular events,such as diseases andinjury ,that woulddelay growth (Galá n, 1996b),and may also cause differences in ageat maturity (Galán, 1996a).

Clutch frequency Aconsiderablefraction (39%)of the females in ourstudy population produced two clutches withinthe same breedingseason. The productionof twoclutches perseason was also documentedin otherlowland populations of L.monticolacantabrica (Braña, 1983; Brañ a et al., 1990;Galá n, 1991), whereas mountain populations ofthe same species (orsubspecies), with ashorter activity period,produced a single annualclutch (Braña et al., 1990,in L.monticolacantabrica ; Moreira et al., 1999,in L.monticolamonticola ;Pérez-Mellado, 1982; Barbadillo, 1985; Elvira andVigal, 1985, in L.monticolacyreni ).Theproduction of multiple clutches per yearhas beendescribed for many other lacertid lizards, mainlyin species livingin areas with aMediterraneanclimate (Saint-Girons andDuguy, 1970; Brañ a, 1983; Chondropoulosand Lykakis, 1983; Barbault andMou, 1988; Castilla et al., 1992; James andWhitford, 1994). The production of single ormultiple clutches within the same season is primarily related tofemale bodysize (Bauwensand V erheyen, 1987;Galá n, 1997)and to the timing ofoviposition (Brañ a, 1983; Brañ a et al., 1990; Galán, 1991, 1997). Large females, whichinitiate reproductiveactivities early in the season,produce two or more clutches annually(Hraoui-Bloquet, 1987; Barbault andMou, 1988; Brañ a et al :; 1990 Galán, 1997),whereas the smallest individuals, whichpostpone reproduction until I the season is well advanced,lay onlya single clutch (Braña, 1983; Hraoui-Bloquet, 1987; Galá n, 1996a, 1997). Hence, female size is amajor determinant ofreproductive investment: larger females lay more clutches peryear and they also producebigger clutches, suchthat theyhave a larger total eggnumber (annual fecundity).

Clutch size andclutch characteristics Ourresults showa meanclutch size of6.41 eggs and a maximumclutch size of nineeggs. These data are similar towhat was reportedby Galán (1991)and Brañ a 360 M.Rúa, P.Galán

(1983)for the same subspecies. Nevertheless, other Lacerta monticola populations fromthe mountainareas ofGalicia (NWSpain)may attain amaximumclutch size of12 eggs (unpubl. data). Mountain populations of L.monticolacyreni present greater meanclutch sizes (Pérez-Mellado, 1982; Elvira andVigal, 1985). This trend is evidentin lizards whichproduce only one annual clutch eachyear and invest the reproductiveeffort in the single clutch (Bauwens,1999). James andWithford (1994)suggest the existence ofphenotypic plasticity in clutch size inuenced by weatherconditions. In the populationstudied here,the productionof two clutches in the same yearis possiblyan adaptation to the favourableweather conditions which permit alongbreeding season. Similarly to the pattern reportedfor other multiple-clutched lizards (Guillette and Bearce,1986; Anderson and Karasow, 1988; Barbault andMou, 1988; Heulin et al., 1994;Galá n, 1997;Olsson and Shine, 1997b; Castilla andBauwens, 2000a; Ji andBrañ a, 2000), the initial clutch of L.monticola is larger thanthe subsequent clutch.So clutch size declines as the reproductiveseason progresses.Another effect is that smaller-sized females, whichproduce fewer eggs, start to breedlater inthe season (Barbault andMou, 1988; Heulin et al., 1994;Galá n, 1996a,1997; Olsson andShine, 1997a). This seasonal variation seems to beinduced by differences in the proximatesource of energy allocated todifferent annualclutches. Material for yolkproduction for the Žrst clutch is mainly derivedfrom fat reserves stored before hibernation,whereas energy shunted to subsequent clutches is mainly derived fromrecent foodintake (Braña et al., 1992;Castilla andBauwens, 2000a). It is noteworthythat L.monticola fromA Coruña didnot lay biggereggs in the later clutch. Anotherphenomenon reported from this studyis that clutch size increases with female size. Several studies havedescribed this pattern forother species like Lacerta vivipara (Pilorge et al., 1983;Heulin, 1985; Bauwens and V erheyen,1987), Podarcis muralis (Barbault andMou, 1988), Lacerta lepida (Castilla andBauwens, 1989), Podarcislilfordi (Castilla andBauwens, 2000a) and others (Reiss, 1989; Bauwensand Dí az-Uriarte, 1997;In Den Bosch and Bout, 1998). Elvira andVigal (1985),Barbadillo (1985)and Galá n (1991)suggest this relation for L.monticola . Several studies havesuggested that clutch size is limited bythe volumeof the maternal bodycavity orby energy availability ,while the eggmass is optimised bynatural selection (Berrigan,1991; Godfray et al., 1991;Roff, 1992; Shine, 1992; Olsson andShine, 1997b). Under the assumption that the amountof energyavailable is limited andegg size is variable,clutch size shouldbe inversely correlated with eggsize in eachparticular clutch becauseof energy and space constraints (Smith andFretwell, 1974;Roff, 1992; Doughty and Shine, 1997; Ji andBrañ a, 2000). Our results showthat among-clutchdifferences in eggmass are negativelycorrelated with clutch size, andthat this relationship is independentof female size. Overall, clutch size is morevariable byfar thanegg size, bothamong females andbetween successive clutches ofthe same female. This pattern is demonstratedby lacertid Reproductionof Lacertamonticola lowlandpopulation 361 lizards exhibitingsteep slopes in the regression ofclutch size onfemale size (Castilla et al., 1992;Ji andBrañ a, 2000).

Relative clutch mass TheRCM valueobtained for L.monticola (average 0.54)is higherthan in most otherlacertid lizards suchas Podarcis muralis ,0.24-0.47D (Brañ a et al., 1991;Brañ a, 1993;Bejakovic et al., 1996a,1996b; Ji andBrañ a, 2000), P. bocagei, 0.33-0.40 (Braña et al.,1991;Galá n, 1997), P. lilfordi,0.25(Castilla andBauwens, 2000a), P. melisellensis ,0.25(Bejakovic et al., 1995b), Lacerta oxycephala ,0.22(Bejakovic et al., 1995a), Algyroides nigropunctatus ,0.29(Bejakovic et al., 1996a);with the exceptionof Lacerta vivipara ,whichmay reach up to 0.81(Bauwens and Thoen, 1981;Bauwens et al.,1986)or even 1.02 (Pilorge et al., 1983).A similarly high RCMvalue(0.56) was foundby Brañ a et al. (1991)in anotherpopulation of Lacerta monticola fromNW Spain(Asturias). Accordingto the roles offoragingtactics and predatorescape developedby Vitt andCongdon (1978), Huey and Pianka (1981) andBrodie (1989), behavioural observations indicate L.monticola tobe a‘widely foraging’lizard, like the great majority oflacertids (Henle,1990, 1991; Bauwens, 1999).In theses species, the primaryescape behaviourinvolves wariness andrapid running(Vitt andCongdon, 1978; Vitt, 1981;Vitt andPrice, 1982).Species utilising this strategy exhibiteda lowerRCM thanspecies usingthe ‘sit-and-wait’strategy . This is whyit is surprising that L.monticola has sucha highRCM value.A similar observationwas madeby Bauwens and Thoen (1981) in Lacerta vivipara and by Braña (1993)in Podarcismuralis ;inthese species, changesoccur in the predator- avoidancetactics from ight to cripsis, whichwould explain this apparentparadox. Asin otherlizard species, ourdata indicate that RCMis notcorrelated with female size.

Hatchingand hatchlings Themean SVL offemale hatchlings was greater thanthat ofmale hatchlings.In L. monticola,females continueto bebiggerthan males in adulthood(Galá n, 1991).In this study,weobservedthat females attain alarger bodysize thanmales, although there wereno differences inmean body size. In L.schreiberi ,females also havea greater bodysize thanmales (Galán, 1984).A higherSVL in female as comparedto male hatchlings has also beenreported for other populations of Lacerta monticola (Barbadillo,1985; Galá n, 1991; Pé rez-Mellado, 1998), and other lacertid lizards, such as Lacerta schreiberi (Galán, 1989; Brañ a, 1996), Podarcismuralis (Ji and Braña, 2000) and Podarcisbocagei (Galán, 1997). In lacertid lizards the larger size offemale juveniles couldbe ageneralphenomenon that couldbe induced by the highernumber of presacral vertebraein females (Barbadillo andSanz, 1983; Barbadillo,1985). HatchlingSVL is positively correlated with the eggmass, suggestingthat the latter maybe a goodestimator ofthe energycontent of an egg (Sinervo, 1990; 362 M.Rúa, P.Galán

VanDamme et al., 1992;Marco and Pé rez-Mellado, 1998). Hatchling SVL does notcorrelate with the mother’s SVLorweight.Such relationships werenot found in Lacerta vivipara (Bauwensand V erheyen,1987), Lacerta agilis (Olsson and Shine,1997b) or Lacerta schreiberi (Marcoand Pé rez-Mellado, 1998) either. Nevertheless, others authorsreported that the meanegg or hatchling mass ofa clutch increases with female lengthin, for instance, Podarcis muralis (Van Damme et al., 1992), Podarcis melisellensis (Bejakovicet al., 1995b), Podarcis bocagei (Galán, 1997) and Acanthodactyluserythrurus (Castilla et al., 1992).Small-sized oviparouslizards that havea small clutch size tendto increase the eggsize rather thanthe clutch size, resulting insigniŽ cant, positive correlations betweenegg size andfemale SVL,whereaslarge-sized lizards tendto increase the clutch size instead ofthe eggsize (Frankenbergand Werner, 1992; Marco et al., 1994).In some species bothcharacteristics (eggsize andclutch size) correlated signiŽcantly with the mother’s SVL(Galán, 1997, 1999b). In this case, Lacerta monticola would appearto adopt a strategy that is similar tothe oneused by bigger lizards with large clutch sizes ( >10eggs), tending to increase the clutch size andnot the egg size, despite the fact their bodysize is small andtheir clutch consists ofless than ten eggs.This andother life historycharacteristics ofthe populationof Lacerta monticola studied,such as the delayand the variability at age(2-3 years) andsize at the onset ofsexual maturity, ahigherRCM thanin other lacertid lizards orthe negligible increase inthe eggmass in the secondclutches with respect tothe Žrst (eventhough the clutch size is lowin the secondclutches), givea highdegree of singularity tothis population,which in itself is uniquebecause, while primarily an alpine species, hereit is foundto inhabit the lowlands.

Acknowledgements Thestudy was performedwith authorisation fromthe regionalgovernment of Gali- cia (Servicio deMedio Ambiente Natural, Consellerí a deMedio Ambiente, Xunta deGalicia). This studywas partially supportedby the Secretaría Xeral deInvesti- gación eDesenvolvementoof the governmentof Galicia, codePGIDT99PXI10301A. This agencyalso grantedthe permits allowingus to collect the specimens onthe Želd andto keepthem temporarily inthe laboratory(user establishment number 15006AE).We would like to thankRicardo Ferreiro, Pablo Serantes, Cristina Brea, andMariá n Gómez fortheir assistance duringthe courseof this study.

REFERENCES

Almeida,A.P .,Rosa,H.D. PauloO.S. &Crespo,E.G. (2001)Genetic differentiation of populations ofIberianrock-lizards Iberolacerta (Iberolacerta )sensuArribas (1999). J.Zool. Syst. Evol. Res. , 39, 1-8. Anderson,R.A. &Karasow,W.H.(1988) Energetics of the lizard Cnemidophorustigris and life historyconsequences of food-acquisition mode. Ecol.Monogr . ,58,79-110. Reproductionof Lacertamonticola lowlandpopulation 363

Aragón, P .,López, P .&Martín, J. (2000)Size-dependent chemosensory responses to familiar and unfamiliarconspeciŽ c faecalpellets by theIberian rock lizard Lacertamonticola. Ethology , 106, 1115-1128. Arribas,O.J. (1996) T axonomicrevision of the Iberian Archaeolacertae I.: Anewinterpretation of thegeographical variation of Lacertamonticola Boulenger,1905 and Lacertacyreni Müller & Hellmich,1937 (Squamata: Sauria: Lacertidae). Herpetozoa, 9, 31-56. Arribas,O.J. (1999) Phylogeny and relationships of the mountain lizards of Europe and Near East (Archaeolacerta Mertens,1921, sensu lato) and their relationships among the Lacertidae radiation. Russ.J. Herpetol. , 6, 1-22. Barbadillo,L.J. (1985) Nuevos datos sobre la reproducció n de Lacertamonticola (Lacertidae, Reptilia)en Españ a central. Doñana. Acta Vert.,12,189-196. Barbadillo,L.J. & Sanz,J.L. (1983) Aná lisis osteomé trico de las regiones sacra y presacrade la columnavertebral en los lagartos ibé ricos Lacertaviridis Laurenti, Lacertalepida Daudin y Lacertaschreiberi Bedriaga. Amphibia-Reptilia ,4,215-239. Barbault,R. &Mou,Y .P.(1988)Population dynamics of thecommon wall lizard, Podarcismuralis , insouth-western France. Herpetologica , 44, 38-47. Bauwens,D. (1999)Life-history variation in lacertid lizards. Nat. Croat.,8,239-252. Bauwens,D. &Díaz-Uriarte, R. (1997)Covariation of life-history traits in lacertid lizards: a comparativestudy. Am. Nat.,149,91-111. Bauwens,D., Heulin,B. &Pilorge,Th. (1986) V ariationsspatio-temporelles des caracteristiques demographiquesdans et entre populations du lé zard Lacertavivipara .In:Centre National de la RechercheScientiŽ que (Eds.), Actesdu Colloque Biologie des P opulations ,pp.531-536. Univ. ClaudeBernard, Lyon. Bauwens,D. &Thoen,C. (1981)Escape tactics and vulnerability to predation associated with reproductionin thelizard Lacertavivipara . J.Anim. Ecol .,50,733-743. Bauwens,D., V anDamme, R. &Verheyen,R.F .(1989)Synchronization of spring molting with the onsetof matingbehavior in malelizards, Lacertavivipara . J. Herpetol.,23,89-91. Bauwens,D. &Verheyen,R.F .(1987)V ariationof reproductive traits in a populationof the lizard Lacertavivipara . Holarct.Ecol. ,10,120-127. Bejakovic,D., Aleksic, I., Crnobrnja-Isailovic,J., Dzukic,G. &Kalezic,M.L. (1995a)Reproductive cycleand clutchsize in femalesharp-snouted rock lizards, Lacertaoxycephala . Amphibia-Reptilia , 17, 73-77. Bejakovic,D., Kalezic, M.L., Aleksic, I., Dzukic,G. &Crnobrnja-Isailovic,J. (1995b)Female reproductivecycle and clutch traits in the Dalmatian wall lizard ( Podarcismelisellensis ). Folia Zool.,44,371-380. Bejakovic,D., Aleksic, I., Tarasjev,A.J. Crnobrnja-Isailovic, J., Dzukic,G. &Kalezic,M.L. (1996a)Life-history variation in a communityof lacertid lizards from the Lake Skadar region (Montenegro). Herpetol J.,6,125-132. Bejakovic,D., Aleksic, I., Crnobrnja-Isailovic,J., Dzukic,G. &Kalezic,M.L. (1996b)Female reproductivetraits in the common wall lizard ( Podarcismuralis )fromthe Skadar Lake region, Montenegro. Rev.Esp. Herpetol .,10,91-96. Berrigan,D. (1991)The allometry of eggsize and number in insects. Oikos,60,313-321. Braña, F.(1983)La reproducció n delos saurios de Asturias (Reptilia; Squamata): ciclos gonadales, fecundidady modalidadesreproductoras. Rev.Biol. Univ .Oviedo , 1, 29-50. Braña, F.(1993)Shifts in body temperature and escape behaviour of female Podarcismuralis during pregnancy. Oikos,66,216-222. Braña, F .(1996)Sexual dimorphism in lacertid lizards: male head increase vs female abdomen increase? Oikos,75,511-523. Braña, F .,Arrayago,M.J., Bea, A. &Barahona,A. (1990)Ciclo reproductor y decuerpos grasos de Lacertamonticola cantabrica .Comparación entredos poblaciones situadas a diferentealtitud. Amphibia-Reptilia , 11, 41-52. 364 M.Rúa, P.Galán

Braña, F .,Bea,A. &Arrayago,M.J. (1991) Egg retention in lacertid lizards: relationships with reproductiveecology and the evolution of viviparity. Herpetologica ,47,218-226. Braña, F .,González, F .&Barahona,A. (1992)Relationship between ovarian and fat body weights duringvitellogenesis for three species of lacertid lizards. J. Herpetol.,26,515-518. Brodie,E.D. (1989)Behavioral modiŽ cation as a meansof reducing the cost of reproduction. Am. Nat.,134,225-238. Castilla,A.M., Barbadillo, L.J. & Bauwens,D. (1992)Annual variation in reproductive traits in the lizard Acanthodactyluserythrurus . Can.J. Zool. ,70,395-402. Castilla,A.M. & Bauwens,D. (1989)Reproductive characteristics of the lacertid lizard Lacerta lepida. Amphibia-Reptilia ,10,445-452. Castilla,A.M. & Bauwens,D. (2000a)Reproductive characteristics of the island lacertid lizard Podarcislilfordi . J. Herpetol.,34,390-396. Castilla,A.M. & Bauwens,D. (2000b)Reproductive characteristics of the lacertid lizard Podarcis atrata. Copeia,2000,748-756. Chondropoulos,B.P .&Lykakis,J.J. (1983) Ecology of the Balkan wall lizard, Podarcisionica (Sauria, Lacertidae)from Greece. Copeia,1983,991-1001. Doughty,P .&Shine,R. (1997)Detecting life history trade-offs: measuring energy stores in capital breedersreveals costs of reproduction. Oecologia,110,508-513. Dunham,A.E. (1981)Populations in a uctuatingenvironment: the comparative population ecology oftheiguanid lizards Sceloporusmerriami and Urosaurusornatus . Misc.Publ. Mus. Zool. Univ . Mich., 158, 1-62. Dunham,A.E. (1994)Reproductive ecology. Introduction. In: L.J. Vitt & E.C. Pianka(Eds.), Lizard Ecology:Historical and Experimental P erspectives ,pp.3-5. Princeton Univ. Press, Princeton. Elvira,B. &Vigal,C.R. (1982)Nuevos datos sobre la distribució n geogrᎠcade Lacertamonticola cantabrica Mertens,1929 (Sauria, Lacertidae). Doñana, Acta Vert., 9, 99-106. Elvira,B. &Vigal,C.R. (1985)Further data on thereproduction of Lacertamonticola cyreni (Sauria, Lacertidae)in CentralSpain. Amphibia-Reptilia ,6,173-179. Frankenberg,E. &Werner,Y .L.(1992)Egg, clutch and maternal sizes in lizards: intra- and interspeciŽc relationsin near-eastern Agamidae and Lacertidae. Herpetol.J. , 2, 7-18. Galán, P.(1982)Nota sobre las Lacertamonticola Boulenger,1905, de las zonas costeras del Norte de Galicia. Doñana, Acta Vert.,9,380-384. Galán, P .(1984)Estudio sobre la biometrí a, folidosis, diseñ o ycoloración de Lacertaschreiberi , Bedriaga,1878 (Sauria, Lacertidae). Alytes, 2, 25-54. Galán, P.(1989)Notas sobre los ciclos de actividadde Lacertaschreiberi Bedriaga,1878, en Galicia. Treb.Soc. Cat. Ictio. Herp. ,2,250-265. Galán, P.(1991)Notas sobre la reproducción de Lacertamonticola (Sauria,Lacertidae) en laszonas costerasde Galicia(Noroeste de Españ a). Rev.Esp. Herpetol. ,5,109-123. Galán, P.(1996a)Sexual maturity in apopulationof thelacertid lizard Podarcisbocagei . Herpetol.J. , 6, 87-93. Galán, P .(1996b)Infecciones externas en una població n naturalde Podarcisbocagei :desarrollo estacionalde la enfermedade incidenciaen la mortalidad,reproducció n ycrecimiento. Amphibia- Reptilia,17,103-113. Galán, P.(1997)Reproductive ecology of thelacertid lizard Podarcisbocagei . Ecography, 20, 197- 209. Galán, P.(1999a)Declive y extincionespuntuales en poblacionesde baja altitud de Lacertamonticola cantabrica. Bol.Asoc. Herpetol. Esp .,10,47-51. Galán, P .(1999b)Demography and population dynamics of the lacertid lizard Podarcisbocagei in NorthwestSpain. J.Zool.(London) ,249,203-218. Gillis,R. &Ballinger,R.E. (1992)Reproductive ecology of red-chinnedlizards ( Sceloporusundulatus erythrocheilus )inSouthcentralColorado: comparisons with other populations of a wide-ranging species. Oecologia,89,236-243. Reproductionof Lacertamonticola lowlandpopulation 365

Godfray,H.C.J., Partridge, L. &Harvey,P .H.(1991) Clutch size. Ann.Rev .Ecol.Syst .,22,409-429. Goldberg,S.R. (1974)Reproduction in mountain and lowland populations of the lizard Sceloporus occidentalis . Copeia,1974,176-182. Guillette,L.J. & Bearce,D.A. (1986)The reproductive and fat body cycles of thelizard, Sceloporus grammicusdisparilis . Trans.Kansas Acad. Sci. , 89, 31-39. Henle,K. (1990)Population ecology and life history of three terrestrial geckos in arid Australia. Copeia,1990,759-781. Henle,K. (1991)Life history patterns in lizardsof thearid and semiarid zone of Australia. Oecologia, 88,347-358. Heulin,B. (1985)Densité et organisationspatiale des populations du lé zard vivipare Lacertavivipara (Jacquin,1787) dans les landes de la région de Paimpont. Bull. Ecol.,16,177-186. Heulin,B., Osenegg, K. &Michel,D. (1994)Survie et incubation des oeufs dans deux populations ovipares de Lacertavivipara . Amphibia-Reptilia ,15,199-219. Hraoui-Bloquet,S. (1987)Le cycle sexuel des femelles chez Lacertalaevis Gray1838 dans la montagnedu Liban. Amphibia-Reptilia ,8,143-152. Hraoui-Bloquet,S. &Bloquet,G. (1988)Le cycle sexuel des mâ les chez Lacertalaevis surla côte du Libanet comparaisonavec les lé zards de montagne. Amphibia-Reptilia ,9,185-195. Huey,R.B. &Pianka,E.R. (1981)Ecological consequences of foraging mode. Ecology,62,991-999. InDen Bosch, H.A.J. & Bout,R.G. (1998)Relationships between maternal size, egg size, clutch size, andhatchling size in Europeanlacertid lizards. J. Herpetol.,32,410-417. James,C.D. &Whitford,W .G.(1994) An experimental study of phenotypicplasticity in theclutch sizeof alizard. Oikos, 70, 49-56. Ji,X. &Braña, F .(2000)Among clutch variation in reproductive output and egg size in the wall lizard (Podarcismuralis )froma lowlandpopulation of northernSpain .J.Herpetol. , 34, 54-60. López, P .,Aragón, P .&Martín, J. (1998)Iberian rock lizards ( Lacertamonticola cyreni ) assess conspeciŽc informationusing composite signals from faecal pellets. Ethology,104,809-820. Marco,A., Pérez Mellado, V .&GilCosta, M.J. (1994) Reproductive strategy in amontanepopulation ofthe lizard Lacertaschreiberi (Sauria:Lacertidae). Herpetol.J. , 4, 49-55. Marco,A. &Pérez-Mellado, V .(1998)In uence of clutch date on egg and hatchling sizes in the annualclutch of Lacertaschreiberi . Copeia,1998,145-150. Martín, J. &López, P .(1999)Nuptial coloration and mate guarding affect escape decisions of male lizards Psammodromusalgirus . Ethology,105,439-447. Martín, J. &López, P .(2000)Chemoreception, symmetry and mate choice in lizards. Proc.R. Soc. Lond. B.,267,1265-1269. Martín, J. &López, P .(2001)Repeated predatory attacks and multiple decision to come out from a refugein an alpine lizard. Behav. Ecol.,12,386-389. Martín, J. &Salvador,A. (1995)Microhabitat selection by theIberian rock lizard Lacertamonticola : effectson density and spatial distribution of individuals. Biol.Conserv .,79,303-307. Martín, J. &Salvador,A. (1997)Effects of tail loss on the time budgets, movements, and spacing patternsof Iberian rock lizards, Lacertamonticola . Herpetologica ,53,117-125. Martínez-Cortizas, A., Castilla-Rodríguez, F .,Pérez-Alberti, A., Dí az-V alcarcelM. &Blanco-Chao, R. (1999) AtlasClimá tico de Galicia. Xuntade Galicia,Santiago de Compostela. Matos,A. de(1988) Contribuç ão parao conhecimentoda biologia da lagartixa serrana ( Lacerta monticola Boul.)da Serrada Estrela (Portugal). Arq.Mus. Bocage, Nova Sé rie ,1,213-218. Mayer,W .&Arribas,O.J. (1996) Allozyme differentiation and relationship among the Iberian- Pyreneanmountain lizards. Herpetozoa, 9, 57-61. Melendro,J. &Gisbert,J. (1976)Contribució n alestudiode Lacertamonticola enla Sierrade Gredos (Ávila,Españ a). Doñana, Acta Vert., 3, 89-92. Mellado,J. &Olmedo,G. (1987)Actividad invernal en poblacionesde lagartosde lazonasubtropical. Mediterránea Ser .Biol. , 9, 5-13. 366 M.Rúa, P.Galán

Moreira,P .L.,Almeida, A.P .,Rosa,H.D., Paulo O.S. &Crespo,E.G. (1999)Bases para a conservaçao dalagartixada montanha, Lacertamonticola . Estudosde Biología eConservaçao da Natureza , 25, 1-68. Nicholson,A.M. & Spellerberg,I.F .(1989)Activity and home range of thelizard Lacertaagilis L. Herpetol.J. ,1,362-365. Nuland,G. J.van& Strijbosch,H. (1981)Annual Rhythmics of Lacertavivipara Jacquin and Lacerta agilisagilis L.(Sauria,Lacertidae) in theNetherlands. Amphibia-Reptilia , 2, 83-95. Odierna,G., Aprea,G., Arribas, O.J., Capriglione, T .,CaputoV .&Olmo,E. (1996)The karyology of theIberian rock lizards. Herpetologica ,52,542-550. Olsson,M. &Shine,R. (1997a)The seasonal timing of oviposition in sandlizards ( Lacertaagilis ): whyearly clutches are better. J.Evol. Biol .,10,369-381. Olsson,M. &Shine,R. (1997b)The limits to reproductive output: offspring size versus number in the sandlizard ( Lacertaagilis ). Am. Nat.,149,179-188. Palacios,F .&Salvador,A. (1974)Primeros datos sobre la reproducció n de Lacertamonticola en Iberia. Bol.R. Soc.Españ ola Hist. Nat .,72,243-244. Pérez Mellado, V .(1982)Datos sobre Lacertamonticola Boulenger,1905 (Sauria, Lacertidae) en el oestedel Sistema Central. Doñana, Acta Vert.,9,107-129. Pérez-Mellado, V .(1997) Lacertamonticola Boulenger,1905. Lagartija serrana. In: J.M. Pleguezuelos (Ed.), Distribución yBiogeografía delos AnŽ bios y Reptilesen Españ a yPortugal.Monografí as deHerpetología , no3,pp.225-227. Editorial Universidad de Granada& Asociación Herpetológica Española, Granada. Pérez-Mellado, V .(1998) Lacertamonticola Boulenger,1905. In: A. Salvador(Ed.), FaunaIbé rica, vol.10: Reptiles ,pp.207-215. Museo Nacional de CienciasNaturales. CSIC, Madrid. Pérez-Mellado, V .(2002) Lacertamonticola Boulenger,1905. Lagartija serrana. In: J.M. Pleguezue- los,R. Márquez & M.Lizana(Eds.), Atlasy LibroRojo de los AnŽ bios y Reptilesde Españ a , pp. 227-229.Direcció n Generalde Conservació n dela Naturaleza-A.H.E., Madrid. Pilorge,T .,Xavier,F .&Barbault,R. (1983)V ariationsin litter size and reproductiveeffort within and betweensome populations of Lacertavivipara . Holarct.Ecol. ,6,381-386. Reiss,M.J. (1989) TheAllometry of Growth and Reproduction. CambridgeUniversity Press, Cam- bridge. Roff,D.A. (1992) TheEvolution of Life Histories .Chapman& Hall,New York. SaintGirons, H. &Duguy,R. (1970)Le cycle sexual de Lacertamuralis enplaineet enmontagne. Bull.Mus. Natl Hist. Nat. (P aris) ,42,690-695. Shine,R. (1992)Relative clutch mass and body shape in lizardsand snakes: is reproductiveinvestment constrainedor optimized. Evolution,46,828-833. Sinervo,B. (1990)The evolution of maternal investment in lizards: an experimentaland comparative analysisof egg size and its effects on offspringperformance. Evolution,44,279-294. Smith,C.C. &Fretwell,S.D. (1974)The optimal balance between size and number of offspring. Am. Nat.,108,499-506. Spellerberg,I.F .(1982) Biologyof Reptiles.An Ecological Approach. Blackie& SonLtd, London. VanDamme, R., Bauwens,D., Brañ a F.&Verheyen,R.F .(1992)Incubation temperature differentially affectshatching time, egg survival, and hatching performance in the lizard Podarcismuralis . Herpetologica ,48,220-228. Vitt,L.J. (1981) Lizard reproduction: habitat speciŽ city and constraints on relativeclutch mass. Am. Nat.,117,506-514. Vitt,L.J. & Congdon,J.D. (1978) Body shape, reproductive effort, and relative clutch mass in lizards: resolutionof aparadox. Am. Nat.,112,595-608. Vitt,L.J. & Price,H.J. (1982) Ecological and evolutionary determinants of relative clutch mass in lizards. Herpetologica ,38,237-255.