Sociality in lizards: family structure in free-livingKing's Skinks Egernia kingii from southwesternAustraliaC. Mastersr and R. Shine'3PO Box 315, Capel,WA 6271

'�School of Biological Sciences A08, University of Sydney, NSW 2006,Australia.sCorresponding author Prol Rick Shine

ph,� 6 1 2-935 | -3772, tax: 6 l 2-935 l -5609, email: rics@bio.usyd.edu.au

Kingt Skinks Egernid kingii are large yiviparous scin€id lizards from southwestem Australia.Althoughsome other species within the genus Eg€fl?io are known to exhibit €omplex socialir/, with long-termassociations beween adults and their offspring, there are no published records of such behaviourfor E kingt.Ten yeffs' obs€rvations on a single family of lizards (a pair of adults plus six successiveliders oftheir offsprind in a coastal suburban baclgard 250 km sourh of Penh also reveal€d a verystable adult pair-bond in this sp€ci€s.The female prcduced litters of 9 to | | offspring in summer orautumn at intermls of one to thre€ years. In th€ir frst year of life, neonates lived witn the aduk pairand all the lizards basked toSether; in lat€r ye,ars the offspring d'spersed but the €entml shelrer-site€ontained representatives of up to thr€€ annual cohons as well as the par€nts. Adults toleratedjuveniles (especially neonat€s) and their presence may confer direct parental protection: on oneoccasion an adult skink attacked and drov€ away a tigersnake Notechis s€utotus that ventured €lose tothe family's shelter-site.Although olr observations are based only on a single pair of lizards and theirofspring, they provide the most d€tailed evidence yet available on the complex family life of thesehishly social lizards.

FuEFot0

KeI words: behavioun Egemio kingr, I zni parenta caE, rept le, Scinc dae soc a organisat on

lntroductionThe social rystm o{lizanJs have taditionally been viewed asrelative\ sinple, qpically involvins eidrer male territorialiryor dominance hier:rchies (Olsson 1991j Calllerg er al.199?). Indeed, available data (albeit based on only a tinyFaction ofdre > 3,000 livira liad specied suggest thar suchrnating system are the nom anong lizards from a diversearay of phylogenetic lineages. Nonetheles, recmt srurlreshave revealed an ursuspected conplqiry in scial systemswiftin a Gw lirard species, includins individual recognitionofparoen (Olson ald Shine 1998) or offrpring @u1l er al.1994), md long-tem nonogmy @ull 1994, 2010; Buller al. 1998). Most remarkably, sone liads live in stableagcresations of cLoseLy-related individuals (Gmdner er al.2001, 2002). Such aggregatiors may range from "nudear

familis" consisting of an adult pair plus their ofspring(Oconnor md Shine 2003) thJoush to much largerassenblages containing muitiple adults of bodr sexes plustheir ofsprins (Stow et dl. 2001). All ofthe specis frr whichsuch comple,( socialiq' has been described belong to r singlephylogenetic lheage ('dt Egemia Group) comprisingfour genera of large viviparous Austlali:n sliDls (orrcrlqCyclodono4has, Egemra and Titqrl: Geer 1989).

The genus Egemia is of particular interest because(uniquely. "o far a. .. l')ownr ir conrrrN (pe( re, redrndin social sysrcms ftom solitary existence through to theconplex aegregacions described above Gee review byChapple 200 11. I hu.. tud.e. on the.pecre. of r hn genu.

have enormous potential not only to expand the diveEityof social systems kno*n to be *hibited by reptlles, butalso to tesr compering hypotheses on the evolutionarypressures resporuible for social aggregation. Unfortunately,howevei detailed informarion is available for only a smallsubset of taxa, nostly restricted to southeast€m Autralia(E. a"m'/|€h/,ni, E. sal�.dtiljs, E. r.olcsii, E. smbhiu I Gardnererdl. 2001, 2002i Stow€,dl. 2001; Clupple 2003; O'Connorand Shine 2001). Fo odrer taxa we have only limited fieldstudies (E. ruiox E. &'tut , Hickman 1960; Milton 198?,1990; Klinsenbdk et al. 2000) or purely anecdotal reportsGee Chapple 2003) . Hence, we need reliable data on socialorsanization in other Egemtu species, espechlly those 6omdiflerenr geographic areas and phylogenetic eroupings.The present paper provides such data, based on long-terrn(>Io-year) obsel\atiors on a single adult pair of free-livins Egema liryii and then ofGprine.

Methods

Study speciesEgemin kingii is a large (to 244 mm snourvent lengchlSVLll d.rk colou-ed \ iviparoLr \ul.id lxdid cpecieswidely distributed rhrough coastal and near.coastalhabitats in the sourhwesrem comer of Westem Australia(Stor €r dl. 1981). It is nosr abundant on ol{shore islands,where it is pdmarily herbivorous during adult life but

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sometines feeds on invertebrates and seabird eggs (Ston etaI.1981; Arena 1986;tuclurds 199q Langron 2000). Themosr extensive infonation on thls specieJ ecolog comesfrom an unpublished Honou$ thesis b Arena (1986). Hereported that males and femalcs attain similar body sizes,bu nal" . ha ' " larg. r head. . ru1. . u r r ' rn .uru, l m rur i t l. lo0 n,n ,nd len a le. ar l8s n,m SVL, : lu | r . mrrr . rurfixed home ranges in dre field, and adult males ffght e.rchother durnrg the matins seasoni fenales producc smalllilters in autumq and juveniies may associntc $'ifi thefenale parent for several i'eas aftcr birth (Arena 1986) .

Study siteIn 1982 one of us (CM), an amareur naturalist, novedto a nervly.consmrctcd house 300 m frorn the oceanin the snall town of Pcppcrnint Grove Beach, 246 kmsouth of Penh. The sunounding habitat consists of sanddunes nostly vegetrted with peppenrinr fiees Agois

leuosa with a low understorey. Egemd kingi were seenintermittenth bur in 1991 a pile of 23 jarah plaDks(mean length 3.7 nl, width 20 cq left over fmr fence-building) ln the bachard attrac@d a pair of adult lizardswhich hrve lived rhere ever since. The pile of planlc hmbeen left undisturbed rhroughout this period.

ResultsB€ginning in Januaa 1993, CM began takirE photographsand recording sishtings of the skinks. Thc two adults wereeasi\ distinguishable by their body sizcs, thcir tolerance ofclose hum approach, and because one had a re$ownrail. Copulation of fie nvo adults Nas obsened onlyrwice, borh thes near dre plaDls, in l.ttc nomings of rwoconsecutive days in February 2001. Cohons ofnewly-bomskinks have appeared in and aound dre pilc ofplanks atintervals of one to thee years since 1993, ln sunmeror early aurumi (Table 1). Thc nconates were alwaysfi6t discovered when basking with their parents on fteplanlc, and were ncver seen anywhere else in the sardenthrrughout their fint year of life. The group of aduhsplus offspring living in thc pilc of planks typically baskedconnunally (rften, in physical cont.lct with each other)rather than separatelr in tinc or space (Fig. 1). In March2003, for the 6rst timc, rve saw the tlo adLrlts baskrngwith firee senerations of thcir offsprine (one aninal onlyslishtb smaler thm the adults; four abolt half fteir size;a ffve in their lirst year of life).

Table 1 . Reprodlctive oLrtpLrt of a pa r of free-living King sSkinkThe zards prodlced ony sx tters over a ten-yeafperod The Tab e shows the month the neonates werc{rst seen (a n'rost ceaanly wthin a few days ol thefb l1h) and the number of offspr ng in each tten

The nurnbets of ofspring fe sisnificandy over thc ilrstseveral nonths of life, so that Ly the spring {ollowingtheir birth there sere genually about three ro fivesurviving ofApring. Juveniles of diferent ages are readilydis&rsuished by their k y sizes, and typically durinssumner the two adults shared their shelter site with oneor two generations of their ofhpring. In the second and-b.equenr led o ' r \e of f .Dr ins. I ; rhp\ rpre.omcr imc.

seen in other parts of rhe sardel. The tendency for largeroffspring to disperse rnay relate to agonistic behnviourwhereby both aduits vmetines chased and bit fieir larserprogeny Al1 o{ these encountcrs thlt we saw occured inparts of the gardcn away from the cental shelter site.However, the adult skinks tolerated smaller offspring, anddld not retalate even when youngsters took pleces of foodprotrudilg lion the adults' mouths.

Wc have not observed predation nor found carcases ofskinks within the backlard. However, the Lnards respondedrapidly to birds llyiog olerkad, with dr snaller skinlcfleeine first while rhe adults often renained in place onthc r l - . .1 s r re. . T1 e .k 'n t . 'h ' w"d I o rv t r 'e"( ,unto bobtail lizards Tilq!,r rugosa that occasionally movedrhrorgh rh. b. . ( , r rd bur ue u Lne. ed i ne lsu,Uu.interaction wirh another reptile species h April 1999. Thelarger aduft E. kngli was found entwined, and rolling overrnd over wirh, a tigersnake Norechis s*t hrJ only slighdylonger than itseli \X4ien the tvo repnLes separated, thesftrke irled wirh the skink in hot pursuit. The skink laterreappeared with no overt injuries.

DiscussionAlthough our obsewations concern oniy a singie adultpat ofliz.trds, living in the modilied habitat of a suburbangarden, thcy nonetheless provide by far dre most detailedinformation yer available on tbe social system of Egcmialiingn. Despite the facr that rhese large lizards arc aspectacular and sometimes abundant component of rhefauna of southwesrern Australia, they remain vttuallyunsrudied by scieltists. Various facets of their biologyhavc been described ln Honours theses (Arena 1986;

Jones 1988i Richards 1990; Langton 2000), but al1 areas yet unpublished. One paper by Geman reptile-kecperssunnarises Lnnited field data and olxenatiom of captivespecimens (Hauschild and Gasner 1994) .

We have Do geDetic evidence tlLrt the neonates ive saw werethe ofApring of dt resident .rdult pair bur it is very likeb.No other adult E. lingri were sccn jn the baclqard over rheentire period of the study, md copulation between the nroadults was otsened. Thus, although s'e do not know whlchwas rhe rnale and which dre feniale, r'e can be conddentrhar the '!air" coDrained ort adult of each sex. Molecularanalyses of paremage in other Egerria species have revealedoaasional cases of multiplc patemity of Litters, but loqg-term monogamy ls comnon (Gardner et al. 2001, 2002;Stow ct al. 2001; O'Connor and Shine 2t103).

Litt$ s;es recordcd in our srr.rdy (9 to 11: Table 1) werelarger than those gcnerally reported ror E. dnsr ("usuallytrvo" in Bush ct dl. 1995; "2-9 young" ln Hauschild andGasner 1994; "2 a" in Arcna 1986; Cnec 1989). Thisdiference m:y sinpiy reflect the large body sie of our

IYonth Number of offspringt 993 January l

t996 jan'rary

t998 019992002002 March

AustraliSiJoskr voru-e i2 (i) October 2003

Fam ly structure in izards

Figure L Comnruna basking in a fami' grrcup of fr€e- ving Kings Sknk Eger"id kingii n a ,uburban badgard insouthwestern Austra a. Photograph by Les ey lackes.

female; in most lizad species, larger females producelarger litters (Cneer 1989). The intermittent nature ofreproduction is also of interest, with the intewals betweensuccessive lineN ranging 6on one co three years @ble1) . bss.than-annual reproduction is conmon in repriles,especially viviparoN species inhabiting relatively coolclimares (Bull and Shine 1979) .

The only derailed published information on sociaiiq' in E.io4cii consists of a 'Iabte entry in Cardner (1999) notinsthat 'luveniles coexist with parents until they reach sexualmaturity ar approximateb ttfee yean of age', based onpersonal communication. This estimate is consistenr withour ol'n data, as are more general statements (e.g .usually

found livins in colony groups" - Bush et di. 1995). Ir atsoffts well wirh recent scudies on odrr (eastem Austialian)Es€nia species, revealing conplex social sysrens basedaround long-temr associations between adult hzards andtheir offspring. lndeed, rhe genus Eg€mi:ii provides theonly well-docurnented cases of such conplex sociality insquamate reptiies (Chapple 2003).

Unfortunately, available data arc too spa6e to compare the.o.iJ system of E. krl.'a urh tut of.onCenen. specie..Sone Esema species live mostly in "nuclear 6mi1ies" oftwoadults pl6 dreir ofaspring (E. saradn , O Connor and Shlne2003) wheres others live in much larger groups of clce\related individuals (E. amtdwni , Stow et di. 2001; E.stcl,c:n ' Gardret et aL 2001, 2m2). However, we do notyet lcrow the extent of geographic (habitat-associated|\"riation in social systems wid-Iin any sinele speci€s. Basedon the single adult pat that we studied, dr social systenof E. hngn may be intermediare between th€ two dtremes

oudined above. Comidemlle variation is appment in manybehaviotrs: for exanple, both E. strlesii and E. amnrafiarrugroups tend to Etreat en masse into crevices when dangerdueaters (Elller 2001; lanham 2001), whereas in our lizadsit *zs uually only the;uveniles that reheared.

The obsenation of m adut E. /flgii fghting a tigersnakeis paniculady interestins. The snake was roo large forrhe lizard ro ingest (indeed, adult E. lrsri are prinarilyherbivorous: Richards 1990) and rhe lizard was too largefor the snake to ingest. The obvious inlerence is thatthis behaviour comtituted direct parenral protection ofotrsprinc (which wqe ingestible+ized for such a snake,and would be acceptable prey for thid snake species: Shine198?). We are unare of any previous example of suchbeh.qour in lu.:rd. or.nake.. apart 6om an incied.€in aggessive respoNes to an intiudei by postparrumrattlesnakes (Shine t988; Graves 1989; C'.eene e, /,12002; see also anecdotal reporb for other vip€rid snakessummarised by Greene et dl. 2002).

Or:r study dernorxtrates yet again the porencialconffibution that can be nade by amateur naturalists toour understanding of the Australan farna (Geer 1989).This country has an extnordlrury biological diversitybut only a very srnall number of profe$ioml scimtiits toconducr ecological and behavioural research on wtldliG.The inevitable result is dlat our only hope of obtaininginformarion on a broad crcxvsection ofthe Australian faunais through cooperative endeavours between nacuralists andscienrisrs. The complex family life ofKinst Skink providesan extraordinary exarnple of the Lind of phenomenon tharawaits discovery dmugh patient obseration.

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AcknowledgementsVe thank Harold and Gertrude for rheir cooperation overmany years, Bcmie Masrcrs for his assisrance and Lesley

Jackes for fhotosraphy. Manuscript preparatioo wassupported by rhe Afrrali:rn Research Council.

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