function and evolution of the frill of the frillneck lizard, chlamydosaurus kingii (sauria:...

8/14/2019 Function and evolution of the frill of the frillneck lizard, Chlamydosaurus kingii (Sauria: Agamidae)

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Biological Journal of the Linnean Society (1990), 40: 11-20. With 2 figures

Function and evolution of the frill of thefrillneck lizard, Chlamydosaurus kingii (Sauria:Agamidae)RICHARD SHINE


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12 R. SHINEevolutionary origin: a structure may have originally evolved for some reasonother than its present function, or have arisen through general allometricrelationships rather than specific selective pressures (Huxley, 1932; GouldLewontin, 1979). These issues may be clarified by the study of extremeelaborations of display structures, such as the renowned antlers of the Irish Elk(Gould, 1974). The present study examines the functional significance, andprobable adaptive significance, of the largest and most dramatic displaystructure seen in any reptile: the frill of the Australian frillneck lizard,Chlamydosaurus kingii This large (to 90 cm total length) agamid lizard of tropicalAustralia and southern New Guinea possesses an enormous frill, a fold of skinattached to the neck, supported by hyoid cartilage and covered with large keeledscales. Ordinarily the frill is kept folded back against the body, but it can beerected to a diameter more than four times that of the lizards body (Fig. 1) . Frillerection is commonly seen as a defensive response to human interference, but thelack of information on behaviour of Chlamydosaurus in the field means that otherpotential uses for the frill remain entirely speculative. The frill has been variouslyinterpreted as an adaptat ion for gliding (Fenner, 1933), food storage (Bacchus,1939), increasing auditory acuity (De Vis, 1883), thermoregulation (Worrell,1963; Frith Frith, 1987), predator deterrence (Kent, 1895), or courtshipdisplay (Daan , 1972). Other possibilities, such as camouflage or male territorialdisplay, seem not to have been discussed.

MATERIAL AND METHODSBody length, head size and frill size were measured on preserved specimens at

the Australian Museum. Sex was determined by midventral incision andinspection of the gonads. Body length was measured from the tip of the snout tothe vent, and head length from the tip of the snout to the posterior extremity ofthe lower jaw. Frill length was measured inside the frill, from the attachmentpoint closest the end of the lower ja w to the furthest extremity of the frill in a lineparallel to the main axis of the lizards body.

Observations of free-ranging Chlamydosaurus kingii were carried out in KakaduNational Park, 250 km east of Darwin in Australias Northern Territory. Mostwork was centred on the Four-gates Road, which runs along the western sideof Magela Creek downstream of Magela Crossing. Kakadu lies within the wet-dry tropics, with high temperatures year-round (daily maxima a t the nearesttown, Jabiru, average 31C in July, 39C in October: Brennan, 1986), bu t withannual rainfall highly seasonal (over 90 in the months December to March).Chlamydosaurus is abundant in savannah woodland in this region, especially in theopen forests dominated by Eucalyptus tetrodonta and E iniata Most of theinformation reported in the present paper comes from observation of 11 adultfrillnecks in which miniature temperature-sensitive radiotransmitters weresurgically implanted in November-December 1986. These data weresupplemented by observations on other animals during the same period, anddata from seven other telemetered lizards in other years. This work was part of alarger study on habitat use, food habits, movements and thermal relations of thisspecies (Shine Lambeck, 1989).

Lizards were initially located by surveillance from a vehicle driving slowlythrough suitable habi tat. Th e animals were captured by hand , and returned to


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DISPLAY STRUCTURES 13

Figure 1 Threat display by adult male frillneck lizard.the laboratory. Small radiotransmitters 50 20 mm, 15 g; TT-IU-080,J StuartEnterprises) were surgically inserted in the peritoneal cavity under coldanaesthesia. The incisions were sutured closed, and all lizards were releasedwithin 24h of the surgery, at the exact site of their original capture. Thetransmitters weighed from 2 to 6 of lizard body mass, and did not preventsubsequent movement, social interactions, foraging or oviposition (see below and


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14 R. SHINE

Snout-vent length cm)Figure 2. Measurements of preserved frillneck lizards reveal sexual dimorphism in jaw lengthrelative to body length (le ft) , but not in frill length relative to body length (r igh t) . See text fordefinitions. methods and statistics.

Shine Lambeck, 1989). Effective reception range for the telemetry signalaveraged 500 m.Lizard behaviour was monitored during daylight hours over the followingthree weeks. In the November-December 1986 study, observers satapproximately 20 m from the lizards in portable hessian hides (2 x 1 x 1 m), withbinoculars inserted through a small slit cut in the front of the blind. A total of

>300 hours of observations was carried out; details of methodology andmonitoring schedules are given in Shine Lambeck (1989).RESULTS

Museum dataMeasurements of preserved Chlamydosaurus kingii showed that males attainmuch larger body sizes than do females (Nor thern Territory specimens only:mean male snout-vent length (SVL) 254.2 mm, s.d. 21.9, n 56; meanfemale SVL=206.4, s.d.= 16.6, n = 16; t=8.08, 70d.f., P < O . O O l ) . Males alsohave larger heads than do females at the same body length (Fig. 2: analysis ofcovariance, slopes F1,213.32, n.s.; intercepts F1,22=3.06, P


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DISPLAY S T R U C T U R E S 15evidence of frill erection. On a priori grounds, the frill seems too small and fragileto be significant as a parachute.(2) Food storage. The idea that frillnecks may store food items within the foldsof their frill (Bacchus, 1939) has no empirical support from this study. Mostlizards that we captured contained food items in their stomach, and some lizardswere so full of prey that food items fell from their mouths when they gaped todisplay at us. None contained prey items within the frill and, as in the case of theprevious hypothesis, it is difficult to imagine this phenomenon on a priorigrounds.

(3) Auditory enhancement. De Vis (1883: 301) speculated that one function ofthe hood might be that of conducting sound to the tympanum, an officeapparently aided by the channels formed by its converging folds. His dissectionof the frill gave no support to his hypothesis, and we did not observe frill erectionin response to unusual auditory stimuli. Most cases of frill erection (see below)were clearly inconsistent with enhancement of auditory capability.

(4) CamouJage. Although the frill is very obvious when erect, it is inconspicuouswhen at rest, folded back along the body (Fig. 1) . The folds of the frill resembleloose shreds of bark or d ry leaves, and to some extent break up the outline of thelizard. Although this enhancement of camouflage may be of advantage to thelizards, it is most parsimoniously interpreted as a secondary consequence of thefrill rather a selective pressure for the evolution of this large erectile structure.5 ) Thermoregulation. Because the erect frill has a large surface area, there is thepotential for it to serve as a device for collecting radiant energy, dissipatingexcess heat to the air, or perhaps shading the lizards body to reduce exposure tothe suns rays (Worrell, 1963; Frith Frith, 1987). The first of these hypothesespredicts that frill erection should be seen when the lizard is basking, whichtypically occurs early in the morning (Shine Lambeck, 1989). Frill erectionwas never observed in this context: basking lizards were able to elevate bodytemperatures rapidly without erecting the frill. In any case, it would beremarkable to see the evolution of a structure to facilitate heat uptake in a reptileliving in this very warm climate: lizard temperatures average close to 40C(similar to ambient temperature) in the mid-afternoon (Shine Lambeck,1989). Th e highly seasonal activity patterns of Chlamydosaurus also mean that it israrely active in cooler times of the year (Shine Lambeck, 1989). Overheatingmay be a more significant problem, but we saw no evidence of frill erection forthis purpose even on very hot days. Experiments in which the frill was surgicallyremoved (and subsequently taped back in place) suggested that it had little or noeffect on the rate at which body temperatures increased in tetheredChlamydosaurus exposed to a heat source (G.J W. Webb, personalcommunication).

(6) Predator deterrence. This is the function most often attributed to the frill. Alllizards except one juvenile erected the frill when they were captured, and alsowhenever we handled them in captivity. It seems likely that similar responses aregiven to naturally occurring predators, such as hawks (D. Curl, personalcommunication), varanid lizards (Shine, 1986), and elapid and boid snakes(Shine, unpublished observations). We observed partial frill erection by lizardsin response to the close approach of birds (orioles, kookaburras). One lizarddisplayed full frill erection in response to a motor vehicle travellingapproximately 50 m away.


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16 R. HINE(7) Social interactions. Many agamid lizards show complex social behaviour,including assertion displays by territorial adult males. Within the AustralianAgamidae, such displays have been reported in the genera Amphibolurus,Ctenophorus and Pogona (e.g. Carpenter, Badham Kimble, 1970; Greer, 1988).In the bearded dragon Pogona) the beard is used in social contexts as well asin predator deterrence (Carpenter t al., 1970). It is thus surprising that littleattention seems to have been given to the potential role of the Chlamydosaurus frillin social interactions. Our observations suggest that intraspecific communicationis the primary function of the frill. The most common contexts in which we sawfrill erection in free-ranging lizards were (a) displays by adult male lizards, and(b) interactions between lizards.(a) Male displays. All adul t males ( n= 5 telemetered, 8 non-telemetered)observed in November-December 1986 engaged in frequent and spectaculardisplays. These displays were not directed to other specific individuals. Displayswere seen throughout the day, but with a higher incidence in the early morning:33 of all records were obtained between 0600 and 0800 hours, and only 16%

in the much longer period between 1100 and 1800 hours. Thus, these displaysmay be broadly comparable to the non-directed territorial defence seen in thedawn chorus of many bird species. Of 21 display sequences, lasting from a fewminutes to > 1 hour, five were on the ground, rocks or small fallen logs whereasthe remainder were in trees. Most commonly (14 of 16 arboreal cases), malesshowed this behaviour while they were clinging, head upwards, to relativelyslender vertical trunks of standing trees. I n the other cases, males were head-downwards during t he. display. The heights of trees used for displays(mean= 12.7 m, s.d.=3.67, n = 1 7 ) were significantly greater than the meanheight of 341 trees measured in transects through the study area (mean 8.3 m,t=4.88, 16d.f., P30 mdistant. Th e lizard then raised the forepart of its body slightly from the treetrunkby means of simultaneous extension of both forelimbs (as in a push-up display:act system No. 73 of Carpenter Ferguson, 1977). This was followedimmediately by a series of partial frill erections (generally, one-third to one-halfof full erection) with simultaneous head-bobbing and slight opening of themouth (act systems No. 75 and 6) . Each display sequence comprisedan average


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DISPLAY S T R U C T U R E S 7of 9.25 frill erections (s.d. =6.77, n=5 7, range= 1 to 29), and lasted an averageof 11.3 seconds (range 5 to 30). The lizard would then wait for 1 to 40 minutes(n 72, mean 7.3 minutes, s.d. 8.10) before commencing another display. Inabout one-third of displays, limb circumdiction (waving of one foreleg) was alsoevident. Frill erections were usually, but not always, simultaneous with head-bobs and gaping. These assertion displays were generally associated withrelocation of the lizard, with males often moving up, down or around the trunkbetween successive displays. Less frequently, displaying males left their tree andmoved bipedally across the ground, reverting to a quadrupedal posture todisplay. Often, such displays were performed on rocks or logs, or at the base ofother trees (sometimes, clinging approximately 1 m up the t runk). However, thetime spent on the ground rarely exceeded a few minutes.(b) Male-male interactions. Frillnecks mate in November-December, and battlesbetween males are common. Males fight by lunging at each other head-on andinterlocking their jaws (observed on 19 November 1986). Mouths are openedwidely in displays prior to combat, and the frill is fully erected. As a consequenceof this mode of fighting, injuries to the jaws are common in adul t males duringthe breeding season. Of 29 adult males examined during November-December1986, 26 (90 ) had obvious scarring, mostly recent (seven with fresh bloodevident on the wounds). Of these 26 animals, injuries to the jaws were seen in 18(69 ), ranging from missing teeth to actual breaks in the mandible. I n contrast,scarring was recorded in only one of four immature males (25%), and one ofeight adult females (12.5 ). These data reveal a significantly higher incidence ofinjuries in adult males than in either females (x2=20.6, 1 d.f., P


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18 R . SHI NEto have any thermoregulatory significance, and its contribution to camouflage ismore likely to be a secondary consequence of frill morphology than a selectivepressure for the evolution of the structure. Both of the remaininghypotheses-anti-predation and intraspecific display-are supported by ourdata. By far the commonest use of the frill, at least during the mating season, is indisplays by males and in interactions between adult lizards.

The apparent lack of frill displays by solitary females and juvenile malessuggests, by analogy with studies on other agamids (e.g. Carpenter Ferguson,1977), that the male display functions in territorial defence. Structures used bymales in this way often show strong sexual dimorphism (e.g. antlers and tusks inmale ruminants), but relative frill size is not dimorphic in C. kingii (Fig. 2 ) . Thedimorphism documented in relative head sizes of this species is similar to thatreported in many other lizards, in which it has been attributed to sexualselection for success in male-male combat (e.g. Carothers, 1984; Vitt Cooper,1986). The lack of dimorphism in frill size can be explained in at least two ways.

(i ) Females also use the frill for intraspecific communication and deterrence ofpredators (and perhaps for other purposes). Unless there is some selectivedisadvantage to large frill size in females, sexual selection for large frills in maleswould also increase the size of the structure in females (Fisher, 1930).

(ii) Even if large frill size is disadvantageous to females, high geneticcorrelation between the sexes may prevent the evolution of sexual dimorphism(Lande, 1980). This hypothesis is difficult to reconcile with the observeddimorphism in relative head sizes.

The obvious question remaining is: why is the display structure of this speciesso much larger, relative to body size, than in any other reptile (and virtually anyother animal)? Th e dramat ic assertion display of male Chlarnydosaurus, and theelaboration of the frill for that display, are extreme developments of tendenciesthat are widespread in other lizard species. The combat between rival males, andthe consequent serious injuries (especially, mandible breakage in adult malesduring the breeding season) are also more exaggerated than the situation in mostother lizards. Why should frillnecks be extreme in these respects? Several factorsmay increase the potential variance in reproductive success among males andhence, the opportunities for sexual selection. Sexual competition between malesis likely to be most intense when a single male can potentially inseminate severalfemales. Such a situation may arise from: ( i ) the relatively extended season overwhich receptive females may become available (as judged by the timing ofoviposition of captured gravid females, and the seasonal distribution of suchfemales: Shine Lambeck, 1989); (ii) the high abundances of this species insuitable habitats; (iii) the open nature of the habitat, coupled with the highvisual acuity of the lizards, so that lizards can interact with conspecifics over awide area; and (iv) the high mobility of individuals of this species (ShineLambeck, 1989). These characteristics may increase the variance in malereproductive success and the intensity of sexual selection. This in turn mayfacilitate the extreme development of sexually-selected morphology andbahaviour.

An alternative hypothesis for the extreme elaboration of the frill involves theconcept of allometry. Frills are small in hatchlings, and relative frill size increaseswith body size (e.g. Fig. 2 ) . Similar positive allometry of display structuresoccurs both intraspecifically and interspecifically in many other types of animals


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D IS P LA Y S T R U C T U R E S 19(e.g. Gould, 1974), including other agamid lizards (Moody, 1980). Hence, thelarge relative frill size in Chlamydosaurus may result simply from the unusuallylarge body size of this species. Body size is much larger in Chlamydosaurus than inany related genus (e.g. Lophognuthus: Moody, 1980). Given the putatively shorttime-span of the Australian agamid radiation (based on molecular data:P. Baverstock, personal communication), average body size may have increasedrelatively rapidly in the lineage leading to Chlamydosaurus If so, the relative sizeof the frill may have similarly increased through adherence to this generalpositive allometry, rather than through specific selective pressures for anunusually large display structure. The evolution of the spectacular frill inChlamydosaurus kingii may reflect both allometry and adapta tion. Given that theseare not mutually exclusive alternatives, i t may be impossible to test between thetwo hypotheses.

A C K N O W L E D G E M E N T SField assistance was provided by R . Lambeck, T. Pople, T. Press, R. Hore andD. Houston. Logistical support came from Pancontinental Mining Co., the

Office of the Supervising Scientist, and the Australian National Parks andWildlife Service. G.J W. Webb and D. Curl provided unpublished data , and T.Pople, C. James and D. Houston provided comments on the manuscript. Thestudy was funded by the Australian Geographic Scientific Research andExploration Fund.

R E F E R E N C E SBAC CHU S, J., 1939. Notable Australian lizards. Walkabout, 5: 53-60.BRENNAN, K., 1986. Wildflowers of Kakadu. Jabiru, N. T.: Privately published.C A R O T H E R S , J. H., 1984. Sexual selection and sexual dimorphism in some herbivorous lizards. AmericanNaturalist, 124: 244-254.CA RP EN TER , C. C. FER GU SO N, G. W., 1977. Variat ion and evolut ion of s terotyped behavior inreptiles. In C. Gan s D. W . Tinkle (Ed s), Biology ofthe Reptilia, 7: 335-554. New York: Academic Press.C A R P E N T E R , C. C., BADHA M, J. A. KIMBLE, B., 1970. Behavior patterns of three species ofAmphibolurus (Agamidae) . Copcia, 1970: 497-505.D U N , S., 1972. Family Agamidae. In B. Grzimek (Ed.), Animal Lqe Encyclopedia: 205-227. New York: va nNostrand Reinhold Co.DARWIN, C. , 1871. Th e Descent of Man and Selection in Relation to Sex. London: Murray.DE VIS, C. W., 1883. Myology of Chlamydosaurus kin gii . Proceedings of the Linnea n Society of New South Wales, IFENNER, C. , 1933. Runyips and billabongs. Sydney: Angus Robertson.FISH ER, R . A, , 1930 . The Genetical Theory of Natural Selection. Oxford: Oxford University Press.FR IT H , C . FR IT H , D . , 1 98 7. Australia n Tropical Reptiles and Frogs. Townsville: Tropical Australia Graphics.G O U L D , S. J., 1974. T he origin and function of 'bizarre' structures: antler size and skull size in the IrishG O U L D , S. J . LE W ON TI N, R . C. , 1979. Th e spandrels of San Marco and the panglossian paradigm: AGR EE R, A. E., 1988. Australian Lizards. Sydney: Surrey B eatty Co.HARV EY, P . H. , KAVA NAGH , M. J C L UH U X L E Y , J. S., 1932. Problems of Relatiue Growlh. London: Methuen.K E N T , W . S., 1895. Observations on the frilled lizard, Chlamydosaurus ki ngi . Proceedings of the


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20 R. SHINESHINE, R ., 1986. Food hab its, habitats and reproductive biology of four species of varanid lizards in tropicalSH IN E, R . LAM BECK , R ., 1990. Ecology of frillneck lizards, Chlzmydosaurus kingii Aga mid ae) in tropicalVITT, L . J. COOPER, W. E., 1986. Skink reproduction and sexual dimorphism: Eumeces far ciat us in theWOR RELL, E . , 1963. Reptiles of Australia. Sydney: Angus Robertson.

Australia. Herpetologica, 42: 346-360.Australia. Australian Wi ld Research, in press.southeastern United States, with notes on Eumeces inexpectatus. Journal of Herpetology, 20: 4084 15

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