Mateguarding,intrasexualcompetition andmatingsuccessinmales
ofthenon-territoriallizardLacertaschreiberi
A.MARCO andV.PÉREZ-MELLADO
Departamentode BiologíaAnimal, Universidadde Salamanca,SalamancaE-37071, Spain(E-mail:)
Received30July 1998,accepted18January1999
Schreiber’sgreenlizardLacerta schreiberishoweda highdegreeof overlap in individualhomerangeswhichthe malesdid not activelydefend.The number of matesandestimatedmatingsuccessof maleswerenot relatedto the size of malehomeranges.The populationsexratiowas skewedtowardsmales andapro- miscuousmatingsystemwas detected;individualmalesmatedwith0-4 females. Matingfrequency,numberofmates,andmatingsuccessofmaleswerepositively correlatedwithsnout-ventlength.Moreover,therewas assortativematingbysize. Malesguardedindividualmatedfemalesfor severalhours, keepingin physical contactwiththem,andattackingapproachingmales.Male contestsuccesswas relatedto bodysize, butnot to homerangesize. The winningmalesmatedmore oftenwithmorefemalesandprobablyhadhigherreproductivesuccess. However, malescouldnot guardmorethanone femalesimultaneouslyandthey rarely monopolizedindividualfemaleswhichwerepolyandrous.
KEY WORDS: intrasexualcompetition,Lacerta schreiberi,mateguarding,mating success,territorialism.
Introduction.. / . / . / . / . / . / . / . / . / . / . / . / . / . / . / . / 279Materialandmethods / . / . / . / . / . / . / . / . / . / . / . / . / . / . / 280
Results... / . / . / . / . / . / . / . / . / . / . / . / . / . / . / . / 281
Homerangeoverlap / . / . / . / . / . / . / . / . / . / . / . / . / . / 281
Matingsuccess. / . / . / . / . / . / . / . / . / . / . / . / . / . / . / 281
Intrasexualcompetition / . / . / . / . / . / . / . / . / . / . / . / . / 283
Discussion.... / . / . / . / . / . / . / . / . / . / . / . / . / . / 284
Acknowledgments.. / . / . / . / . / . / . / . / . / . / . / . / . / . / 285
References.... / . / . / . / . / . / . / . / . / . / . / . / . / . / 285
INTRODUCTION
In polygynousandnon-territorialmatingsystems,malecompetitioncan invol- veintrasexualselectionwheremalesfightamongstthemselvesto matewithfemales
(HALLIDAY 1992, COOPER VITT 1993, ANDERSSON 1994).For speciesthatexhibit intrasexualselection,successin competitionover matesis crucialfor the fitnessof malesandtraitsthatimprovesuccessin fightsare favouredin the competingsex (ANDERSSON1994).However,in non-territorialmatingsystemsmalesthatmatewith severalfemaleshaveless timeto allocateto eachone,andinferiorcompetitorscan occasionallyhaveaccessto femalesby avoidingcontestswithsuperiorrivals.Males thatmatewithfewerfemalesmay monopolizethe matingsoftheirmates, preventing opportunisticmatingby othermales.In thiscontext,gametheory(ENQUISTLEI- MAR 1983)suggestsa trade-offfor malesbetweenmatesearchandmateguarding. Manylacertidlizardsshowagonisticbehaviouramongmalesandmalechoice (KRAMER1937, KITZLER1941, MOLINABORJA1981, OLSSON1992).However,intrasexu- alselection andmatingsystems havebeenrarelyinvestigatedinlacertidlizards.
Westudiedthe matingsystemandintrasexualcompetitioninanaturalpopula- tionofLacerta schreiberifor 3years.Wedocumentthe relationshipsamongnumber ofmates,matingsuccess, contestsuccess, homerangesize andbodysize ofindivid- ual males.
MATERIALANDMETHODS
Lacerta schreiberiisamedium-sizedlacertidlizardthatinhabitshumidareasnearrivers andmountainstreamsin the NorthernandCentralIberianPeninsula(SALVADOR 1984, MARCO
1997).Malesmature on averageone yearearlierthanfemales(snout-ventlengthrangefor adultmales:72-116mm;SVL rangefor adultfemales:86-115mm;MARCO 1995),andhave longer,widerheads,andbrightercolourationon the backandbelly. Furthermore,duringthe matingseasonmalesdevelopa prominentbluecolourationon the throat.Femaleshaverela- tively longerabdomens(BRANA 1996).Femalesare sexuallyreceptivefor approximately 3 weeksandthey layonly one clutchwithinabreedingseason(MARCOetal.1994).
For 3 years(1990-1992)we studieda L. schreiberipopulation in the Sierrade Béjar (provinceof Salamanca, Spain,U.T.M.co-ordinates:30TTK653691),in a humidHolmoak (Quercuspyrenaica)forest.The studysite has an altitudeof 1250 m anda temperateclimate characterizedby the existenceof frequentfrostsfromOctoberto May andfrequentsnowfalls between DecemberandMarch.
Dataweregatheredon a 0.25 ha (50 x50 m) experimentalplot for threebreedingsea- sons(April throughMay).Atthe beginningofthe breedingperiod,all the adultlizardsobser- ved insidethe plot (108 individuals)werecaptured,markedbytoe-clipping,andpaintedon the backwithtwo spotson combinationsoffourbodysites(head,neck,midback,andamonglegs) andfivecolours.Snout-ventlength(SVL), weight,andreproductivestate(oviductalor vitellog- eneticeggs, copulationmarks,andlateralskin folds for females,andbluesexualcolourationof throatfor males)wererecordedfor eachlizard.Age was determinedfor somelizardsfrom markedhatchlings.Behaviourwas observedduringalldayswhenthe lizardswereactiveinthe breedingseason.The studyplot was checkedseveraltimesevery day by an observerwalking slowlythrough it, recordingeachlizardseen.The observerwas usuallyatleastat5 m away fromlizardsandalwaysusedbinocularsto identifyindividuals.We recorded764 observations ofindividuallizardsincluding30agonisticinteractionsbetween known males and116 matings between known males andfemales.
To estimatehomerangesizes,we recordedthe XandYcoordinatesof a lizardon the plot atevery observationwithaprecisionof0.5 m (thereferenceswerestakeson ameasured grid).Weonly recordedhomerangedatawhenthe observationwas madeatleast1hrafterthe previousobservationof the sameindividual.We haveestimated62 adulthomerangesduring the matingperiodandhomerangeoverlapswiththe programRangesIV(KENWARD1987).The homerangewas estimatedwiththe convexpolygonmethodusingthe arithmeticaverage with
the 100% of the observations(AC100) andthenexcludingthe 10% mostexternalones(AC90) (SCHOENER1981).Homerangeoverlapwas the percentageof a lizardhomerangethatwas overlappedbythe homerangesofanotherlizards.
The sex ratiowas calculatedfor eachyearbydividingthe numberofadultmalesbythe numberof adultfemalesfoundon the studyplot.Matingfrequencywas calculatedfor each yearas the quotientbetweenthe numberof observationscorrespondingto a matingandthe totalnumberof observationsfor eachlizard.The matingsuccessof eachmalewas estimated for eachyearconsideringthe numberofmates,the relativenumberofeachfemalematinglead bythatmaleandthe estimatedclutchsize ofeachfemaleinvolved(STAMPS1983),usingthe for- mula
nj
MSj=[(Nji/Nti)*CSi]
i=1
whereMsj =matingsuccessofmale“j”;nj =numberofmatesofmale“j”;Nji =numberofmat- ings betweenfemale“i”andmale“j”;Nti =total numberofmatingsoffemale“i”;andCsi =esti- matedclutchsize of female“i”.Clutchsize was estimatedusinga linearregressionobtained fromfemalesofan adjacentpopulationduringthe sameyears(r=0.79; F=53.5; P0.001;N
=26,SE =2.152;MARCO etal.1994).
RESULTS
Homerangeoverlap
The sex ratioduringthe matingperiodwas on average1.92:1(males:females). Malesoverlappedtheirhomerangeson averagewith5.9 males(SD =3.23; range=
0-12). Femalesoverlappedtheirhomerangeson averagewith6.6 males(SD =2.8;
range=2-12). Malesoverlappedtheirhomerangeson averagewith3.1 females(SD
=1.9; range=0-6), butonly matedon averagewith0.9 females(SD =1.1; range=
0-4; N =71). The numberof femalehomerangeswhichoverlapwitha malehome rangewas correlatedwithhis numberofmates(Spearman correlationr=0.36; P=
0.03; N=43) butwas not correlatedwithmalebodysize (Spearmancorrelationr=
0.01; P0.05; N=43).
Matingsuccess
Malesguardedindividualmatesfor severalhoursafterthe initialapproach, havingphysicalcontactwiththemandattackingapproachingmales.Of adultfe- malesobservedduringthe matingperiod76.8%wereguardedbyan adultmale.We neverobservedone malewithmorethanone femalenormorethanone malewith one female.Malesrarelymonopolizedallthe matingsofany female.Femalesmated on averagewith2.5males(range=1-5;N=22).
Matingfrequency(Pearsoncorrelationr=0.775;P0.001;N =70), average size ofmates(Pearsoncorrelation r=0.536;P0.001;N=35), andmatingsuccess (Pearsoncorrelationr=0.721;P0.001;N=70; Fig. 1) werepositivelycorrelated withmaleSVL. Male homerangesize was not relatedto matingsuccess(Spearman correlationr=0.25; P=0.108).
282A.MarcoandV.Pérez-Mellado
Fig. 1.—RelationshipbetweenmatingsuccessandSVL ofLacerta schreiberimales.The line indicatesthe linear regression.Openpointscorrespondto lizards thatwere neverobservedtomate.
The matingfrequencyofmaleswithfourmateswas higher thanthatofmales withfewermates(one-wayANOVAF=55.612;P0.001;df =4, 55), butpost-hoc comparisonsshowedno differencein averagematefrequencyamongmalesthathad three,two or one mate.On average,maleswithfourmateshadthe highestmating success(one-wayANOVAF=63.98;P0.001;df=4,65; Fig. 2). However,post-hoc comparisonsshowedno differencein averagematingsuccessamongmalesthathad three,two orone mate.Someindividualswithonly one matehadhighermatingsuc- cess thansomemaleswith two orthreemates.
Fig. 2. —Relationshipbetweennumber of matesandmatingsuccessin a populationof Lacerta schreiberi.Columnsindicatemean±SE andlinesindicaterange.
Male matingsuccess inLacerta schreiberi
Intrasexualcompetition
283
Ofthe adultmaleobservationsmadeduringthe matingperiod9.95%involved agonisticcontests.Malesperformedritualisticdisplaysthatcould escalateintophys- ical fights.Inmanycontests,winningmalesthreatenedlosinglizardswithaggressive andfast bodymovements,withoutactualphysicalcontact.The losingmaleusually escapedandwas chasedfor 1-2 m. In 16% of the observedmale-maleinteractions, they usuallyperformedritualisticdisplays.In the displays,bothmaleswereoriented inoppositedirections,withthe headofone lizardatthe level ofthe fore limbsofthe other.They stoodhighon theirlegs, raisingthe bodyfromthe groundandbending the vertebralcolumntoforman verticalarc. Maintainingthisposture,they appeared to watchone anotherfor severalsecondsto severalminutes.If neitheranimalwas broughtto submission,the ritualcouldescalateto multipleaggressivebitesto the head.Thesefightsresultinblackmarksinthe pileus andsubmaxilaryareas.
The averagesize ofmalesthatwereinvolvedin agonisticinteractions,butdid not performritualisticdisplays,was 93.37 mm(SE =1.681).This averagewas higher thanthe averageSVL ofadultmalesthatwereneverobservedin an agonisticinter- action(88.49mm;SE =1.637) andlowerthanthe averageSVL of malesthatper- formedritualistic fights(101.68mm;SE = 1.912)(one-wayANOVA F = 7.96; P
0.001;df =2, 68). Malesthatperformedritualisticfightswere5or moreyearsold. The numberof victorieswas positivelyrelatedto the bodysize of males(Pearson correlationr=0.45; F=17.49;P0.001;N=70). The averageSVLofwinningmales (99.24mm;SD =7.57) was significantlyhigherthanaverageSVL of losingmales (91.35mm;SD = 8.52) (Studentt-testt= 4.19; P0.001).The SVL difference betweenwinningandlosingmalesof eachcontestwas in average7.86 mm(SD =
11.798)andrangedbetween–12.5 to 37.5 mm.These contestsoccurredthroughout the entirematingperiodandmalescontinuouslydefendedtheirindividualmates. We detectedseveralfightsbetweenthe samemaleswithdifferentresults.Therewas apositiverelationshipbetweenthe numberof victoriesin contestsandthe number of mates(Spearmancorrelationr=0.814;P0.005)andalso betweenthe number of victoriesin contestsandmatingsuccess(Spearmancorrelationr= 0.821;P
0.005;Fig. 3).
Fig. 3. —Matingsuccess(mean± SE) of Lacerta schreiberimalesthat wona differentnumberof male-malecontests.
284A.MarcoandV.Pérez-Mellado
DISCUSSION
Largermaleshadmoremates,largermates,highermatingsuccess,andprob- ably greaterreproductivesuccess.Toimprove malematingsuccessinanon-territorial specieswithfemalemultiplematings,thereis a trade-offfor malesamongmating withlargerfemales, increasingthe numberofmatesandincreasingthe timeallocat- ed to eachone (ENQUIST LEIMAR1983).LargeL. schreiberifemaleslay moreeggs per clutchthan smallfemales(MARCOet al. 1994).Thus,malescan get a potential advantageifthey matewithlargerfemales.Ifmalespreferlargerfemalesas mates, intrasexualcompetitionamongmalestomatewithlargefemaleswouldbehighand, consequently,the costsofmatingwithlargefemaleswouldalso be higherthanmat- ing withsmallones.On the otherhand,if malesmatewithseveralfemales,they wouldhaveless timeto allocateto eachone andthe probabilityof paternityin the progenyof eachmatedfemalewouldbe lowerthanif malesmatewithfewerfe- males.In ourstudy,matingsuccessofthe mostsuccessfulmales(highestMS=38.2) was higherthanthoseof a hypotheticalmonogamousmale[maximumclutchsize recorded=24eggs (MARCO etal. 1994)].Thus,the polygamicstrategyoflargemales couldbe advantageousin thisnon-territorial speciesif the matingsuccessreflects the probabilityof paternity. OLSSON et al. (1994)pointedout thatneitherordernor timebetweenmultiplefemalecopulationshadan impacton the reproductivesuc- cess offirstor last malesin L.agilis. Furthermore,sandlizardfemalesmatingwith manypartnerslay clutchesbothsiredby differentmalesandwithhigherhatching success(OLSSONMADSEN 1995).We believethatthe spatialconcentrationoflarge femalesinsmallareasofhighhabitatquality couldexplain why inourlizardpopula- tiontherewas assortativematingbysize andalso thatlarger malesmatedwithmore femalesthan smallmales.However,a moresuccessfulstrategyfor mediumsize malescouldbetoguaranteehighpaternityofthe clutchofone materatherthantry- ing to matewithas manymatesas possible.In ourstudy,somemaleswithonly one partnerhadhighermatingsuccessandprobablyhigherreproductivesuccessthan maleswithtwo or threemates.This situationmay be commonin suboptimalareas wherefemaledensityis low andthe cost for malesof matingwithseveralfemales may behigh.
In the L.schreiberipopulation studied,therewas no relationshipbetweenmale homerangesize andmalereproductivesuccess.However, male-femalehomerange overlapratewas correlatedwithmalematingsuccess.An increasein malehome rangesize couldincreasethe numberofmatesbutthe malewouldallocateless time to eachone,andthus,the probabilityofpaternitycouldbe lower(STAMPS 1983).In spiteofthis,the strategyoflargeadultmalesto increasetheirreproductivesuccess couldbe relatedto the homerangesite selectionin the matingseason.Anincrease in the adultfemaledensityor the proximityamongthemwouldpermitan increase in the reproductivesuccessof males.Femalesof L. schreiberihavesmaller home rangesthanmalesandselectspecificareaswitha highavailabilityof refugesand baskingsiteson openandstonyareas(MARCO 1996).Atthesesites,thereis a high densityofadultfemales(MARCO 1996)whichfavoursthe polygamicbehaviourofthe largemales.Malesmay haveahighhomerangeoverlap withfemalesat the selected areas.Largenon-territorial malesselectareaswitha highdensityof females.This trendhas also beenshownin territoriallizardsby SCHOENERSCHOENER(1982)in speciesofAnolis,andbyPÉREZ-MELLADOetal.(1988)inLacerta monticola.
Intrasexualcompetitionwas observed andsomemalescontrolledthe accessof otherstoindividual mates,byphysicalherdingofthe mateandphysicalexclusionof
Male matingsuccess inLacerta schreiberi
285
males.Usuallylargermaleswon contests.Whenmaleswerematchedin size, they usuallyperformedritualisticdisplayswhichcouldculminatein aggressivebitesto theirheads.The stereotypedfightsbetweenmalesweresimilarto behaviourrecord- ed for sandlizards(OLSSON1992)andotherlizardfamilies(CARPENTERFERGUSON
1977).Contestswereobservedthroughout the matingseasonwithoutthe establish- mentofdominancehierarchies.Winningmaleshadmoremates,morematingswith themandhighermatingsuccess.
Malesmature 1 year earlierthanfemales, andat a smallerbodysize. Young males(3year old) overlappedtheirhomerangeswithbothlargemalesandfemales butthey hadlow matingsuccess.Incontests,the younglizardsusuallylost andesca- ped.This earlymaturity acquisition(MARCO1995)couldbe relatedto the existence of opportunitiesfor a relativelyhighmatingsuccessfor youngmales.In situations withhighmalemortalityratesor low malesdensity,the opportunisticstrategyof youngmalescouldbe advantageous.Moreover,given thatpolygamic malescannot monopolizethe accessofothermalesto theirindividualmates,inferiorcompetitors may occasionallymatewithsolitaryfemales.The costsin growthderivedfromthe early maturityinyoungmalescouldbecompensatedinnon-territorialmating systemsbythe possibilityofmatingwithtemporarilysolitaryfemalesandbythe low risk ofphysical damageincontestswithcompetitors(ANDERSSON1994).
ACKNOWLEDGMENTS
WethankDirk Bauwens,AndrewR.Blaustein,DougP.ChiversandJosephM.Kiesecker for theirhelp.This studywas partiallysupportedby the grantEX95-16796691of the SEUID andthe grantPB94-1408ofthe CICYTofthe MinistryofEducationandCultureofthe Spanish Government.
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