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Journal of Vertebrate Paleontology 23(4):966–970, December 2003q 2003 by the Society of Vertebrate Paleontology

NOTE

VERMIFORM BONES AND THE EVOLUTION OF GIGANTISM IN MEGALANIA—HOW A REPTILIAN FOX BECAMEA LION

GREGORY M. ERICKSON1, ARMAND DE RICQLES2, VIVIAN DE BUFFRENIL2, RALPH E. MOLNAR3, and MARK K. BAYLESS4,1Department of Biological Science, Florida State University, Tallahassee, Florida, 32306-1100, U.S.A.; 2Laboratoire d’Anatomie Comparee, 2place Jussieu, 75251 Paris Cedex 05, France; 3Museum of Northern Arizona, Flagstaff, Arizona 86001, U.S.A.; 41406 Holly St., Berkeley,California 94703, U.S.A.

The largest known terrestrial lizard is Megalania prisca, an extinctanimal that attained lengths twice those typical for its living varanidcousin, the Komodo monitor (Varanus komodoensis) (Fig. 1 left). De-spite competition from mammalian counterparts, it surprisingly came toreign superior as the largest terrestrial carnivorous taxon on the Austra-lian continent during the late Cenozoic era (Flannery, 1991). Did M.prisca achieve great size by simply retaining juvenile reptilian growthrates as in giant extinct crocodylians (Erickson and Brochu, 1998), con-verge on the mammalian condition through accelerated growth as indinosaurs (Erickson et al., 2001), or show a blending of both strategies?We generated the first life history data for this enigmatic animal usingsize estimations based on long-bone dimensions and longevity assess-ments from growth line counts in peculiar, formerly unidentified, dermalbones. The results showed that it attained gargantuan proportions byprolonging the onset of maturity, while utilizing the exceptionally rapid,yet typical, growth rates of the largest varanids living today.

MATERIALS AND METHODS

Dermal Ossicle Identification and Function

Our study focused on several peculiar, unidentified, vermiform bones(Fig. 1 lower right) that were found in direct association with a largeM. prisca skeleton. This particular specimen (Queensland Museum, QMF4452/3) was exhumed from unconsolidated Pleistocene sediments inthe Springsure Rollestone area of Queensland, Australia. Notably, itrepresents one of the few partially complete representatives of this tax-on. During examination it was observed that several of the vermiformelements had been fractured during diagenesis. Subsequent study of thebroken surfaces using a low power (20–903) dissecting microscoperevealed numerous growth lines. Since previous attempts to assess lon-gevity in this specimen using long-bone and rib skeletochronology(5the study of osseous growth line formation, sensu Castanet and Smi-rina, 1990) failed owing to poor preservation and physiological remod-eling (ADR and VDB, unpubl. data), this finding was exciting in thatit rekindled the possibility to reconstruct the life history of M. prisca.

We hypothesized that the strange bones found with QM F4452/3 wereeither osteoderms or gastralia, both of which are known to occur inextant monitor lizards (Dunn, 1927; Smith, 1935; McDowell and Bog-ert, 1954; Romer, 1956; Fuchs, 1977). To test these theories, hundredsof skeletonized, preserved, and study-skin specimens representing twen-ty-five monitor species in the collections of the Florida Museum ofNatural History (UF; Gainesville), American Museum of Natural His-tory (AMNH; New York), and the Yale Peabody Museum (YPM; NewHaven) were examined for vermiform bones. It quickly became appar-ent that the peculiar elements were not gastralia, these bones beingmuch larger and uniform in shape in living monitors. Conversely, os-teoderms found in a minority of taxa (V. komodoensis, V. salvator, V.bengalensis, V. exanthematicus), provided a very close morphologicalmatch, aside from being somewhat smaller (Fig. 1 upper right). It wasconcluded that the strange fossilized bones were in fact osteoderms fromQM F4452/3 scaled to giant size.

The museum survey and subsequent histological preparations andliterature review provided a clearer understanding of the likely devel-opment, distribution, and function of these elements in M. prisca. For

instance, the ossicles are distributed differently among living monitors,being found throughout the body, or locally about the neck, tail, andlegs (also see Smith, 1935; McDowell and Bogert, 1954; Fuchs, 1977;Auffenberg, 1981). The most highly contorted bones were prevalent inregions with high ossicle density, where physical or physiological in-fluence of adjacent bones led to imbrication (and even fusion in V.komodoensis; also see Dunn, 1927). Straighter ossicles were found inregions with low bone density where interelemental influences on mor-phology were negated. Hematoxylin and eosin preparations (H&E stain-ing; Humason, 1979) made from decalcified nape skin from embryonic(near-term) and 5.5-year-old specimens of V. salvator (MKB collection)confirmed Fuchs’ (1977) contentions that these elements form in thedermis, and usually in association with individual scales (Fig. 2 left).Functionally, the strange bones serve as a form of armor in these highlyagonistic animals (Fuchs, 1977) where potentially injurious biting,clawing, and tail slapping behaviors are common (Auffenberg, 1974,1978, 1981; Murphy and Mitchell, 1974). The present survey revealedthat the capacity of these structures for defense is particularly manifestin very old V. komodoensis where hundreds of ossicles will coalesce toform remarkable turtle-shell-like helmets over the snout and supraorbitalregions (Fig. 2 right; also see McDowell and Bogert, 1954).

Establishing the Periodicity of Growth Zone Formation inLiving Monitors

Auffenberg (1981) previously showed that ‘‘osteoderms’’ (presum-ably vermiform) from wild-caught V. komodoensis possess growth lines.To see if such rings exist in captive raised monitors, we made H&Epreparations (Humason, 1979) using ossicles from three known-agespecimens of V. salvator (4.5, 5.5, and 7.5 years old). The analysisrevealed prevalent growth zones and lines of arrested growth (Fig. 3left). Counts of zones in each ossicle were made and contrasted withage at death. The correspondence in numbers suggests an annual genesisof these histological structures (Table 1). These findings, coupled withresults from the aforementioned nape skin preparations showing thatmany osteoderms begin forming prior to hatching (the entire compli-ment appears to have been initiated no later than the first year of life),suggests these bones can be used to assess longevity in monitor liz-ards—even in relatively old individuals.

Assessment of Longevity in Megalania

Given the utility of the vermiform bones to assess life history attri-butes in extant monitors, we turned our attention back to the fossilizedelements from QM F4452/3. Histological preparations were made fromthree of the bones (see methods in Erickson and Tumanova, 2000). Eachelement was sectioned in a region that was particularly straight and thecross-sectional shapes approximated circles. Growth zone counts madeunder polarized microscopy revealed 16 definitive growth zones in eachof the ossicles and thus a longevity estimate for QM F4452/3 of 16years (Fig. 3 left).

Assessment of Megalania Growth Dynamics

In the final stage of our study we sought to reconstruct the growthdynamics of QM F4452/3. This can be done in varanids using annual

967NOTES

FIGURE 1. Left, skeletal mount of a 5.5 m Megalania prisca in the Queensland Museum, Brisbane, Australia. Conservative estimates of totallength for this taxon range from 4.5 to 5.5 m (Anderson, 1927; Dunn, 1927; Rich and Hall, 1979; Rich, 1985). Lower right, dermal ossicle fromM. prisca (QM F4452/3) compared to similar vermiform bones from the skin of a living monitor lizard, Varanus salvator (upper right). Notethat the M. prisca ossicle is incomplete, having been fractured during diagenesis.

FIGURE 2. Left, H&E preparation of nape skin from a 5.5-year-old V. salvator. Note the round, transversely sectioned ossicle deep within thedermis that is associated with an individual scale. Right, fused dermal ossicles that have formed a defensive helmet on the snout and supraorbitalregion of a very old specimen of V. komodoensis (AMNH 74606). Upper right, close-up of fused ossicles in a rosette configuration. A similar‘‘helmet’’ was found on another aged Komodo monitor as well (YPM Q66; not shown).

968 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 23, NO. 4, 2003

FIGURE 3. Inset left, histological section of a dermal ossicle from a known age 7.5-year-old monitor lizard Varanus salvator showing theexpected eight growth zones. Equable findings were made for other ossicles from this specimen and from other individuals aged 4.5 and 5.5years. Each of these specimens had been captured in the wild as neonates and raised in captivity. Left, growth line count revealing 16 growthzones for a thin-sectioned Megalania prisca dermal ossicle (QM F4452/3) viewed with polarizing light microscopy. Previous attempts to ageMegalania using traditional counts of growth lines in long bones and ribs were stymied by poor preservation and remodeling during life,necessitating this alternative means to assess longevity. Right, growth curve for M. prisca (QM F5422/3) based on growth in dermal ossicles. Itwas assumed that linear changes in ossicle size roughly paralleled changes in animal length. Error bars denote one standard deviation centeredabout the mean for measurements made on the three M. prisca ossicles available for study. Age of somatic maturity is noted for QM F5422/3and for several large extant varanid taxa based on data from Auffenberg (1981), Abdul and Abdullah (1987/88), Andrews and Gaulke (1990),Buffrenil et al. (1994), and Andrews (1995).

TABLE 1. Growth-zone counts from known-age Varanus salvator dermal ossicles.

Sample numberNumber of growth zones

(Near-term embryo)Number of growth zones

(4.5 year old)Number of growth zones

(5.5 year old)Number of growth zones

(7.5 year old)

12345678Mean (Std. Dev.)/Expected

000—————

0 (0)/0

55555656

5.25(0.46)/5.0

6766566—

6.0(0.58)/6.0

7889887—

7.86(0.69)/8.0

long bone growth, since radial appositional growth occurs in proportionto whole body growth (e.g., length) throughout ontogeny (Buffrenil etal., 1994; Smirina and Tsellarius, 1998). We posited that similar analysiscould be done using zonal bone formation in varanid dermal ossicles,since they show the same annual growth rhythm and a similar patternwhereby broad bands form early in ontogeny, and the widths decline atthe age of somatic maturity. (We had hoped to test this applicationfurther using two specimens of V. albigularis, MKB personal collection,for which both size and age had been measured throughout life. Un-fortunately our survey revealed that this taxon is barren of vermiformbones.) Given this, we utilized the proportions of annual growth in theossicles to roughly estimate the growth dynamics in QM F4452/3. Meanproportions of annual growth within each ossicle were multiplied bythe estimated amount of post-hatching bodily growth that occurred inQM F4452/3. For our bodily growth measure we chose to use snout-vent length (SVL) rather than total length since there is a strong inter-specific trend of negative allometry in tail length in larger living mon-itors (Mertens, 1942). (Our own sampling showed this to occur beyondSVL of 60 cm [Fig. 4] making it indeterminable whether this trendwould hold true when extrapolated to an animal the size of the giant

extinct monitor.) Regression analysis of the data from Blob (2000)shows that SVL can be predicted accurately in living monitors of allsizes using femoral length and interspecific regression analysis (SVL 5218.297 1 7.6257[femur length in mm], r-squared 5 0.97). In the caseof QM F4452/3, its femoral length of 290 mm produced a SVL estimateof 2.19 m. From this, its approximate hatchling size (0.288 m) basedon regression analyses (SVL 5 47.328 1 0.10980[Adult SVL in mm],r-squared 5 0.78) from data compiled by Thompson and Pianka (2001)was subtracted to reveal that 1.91 m of somatic growth had occurredduring life. Each of the 16 growth-zone proportions was multiplied bythis value, and a growth curve throughout ontogeny was ascertained(Erickson and Brochu, 1998; Fig. 3 right).

RESULTS OF THE GROWTH ANALYSIS

The results of this analysis showed the estimated maximal growthrate of QM F4452/3 was 14 cm/year (Fig. 3 right). Growth rates de-creased following the 13th year of life, consistent with the asymptoticgrowth typical of vertebrates. Despite its great size, the QM F4452/3was still actively growing at the time of death (5% or 10 cm SVL/yr

969NOTES

FIGURE 4. Tail length versus snout-vent length for a diversity of adult varanids. Specimens shown are the largest for each taxon (with completetails) in the UF collection. Note that proportions of tail length to SVL are fairly constant (1.5:1) until a SVL of 60 cm is reached, at which pointtail length exhibits negative allometry. In the absence of an entire skeleton it is difficult to infer reliably the TL of an adult M. prisca. Was itproportioned like the giant living monitor, V. komodoensis (1:1), or did it have an extremely short tail (Hecht, 1975)? Specimen numbers areavailable upon request from GME.

during the last two years of life), a finding that is consistent with un-fused epiphyses of the femora. Although this suggests it may have hadthe potential to reach the upper bounds of size for this taxon, death atthis developmental stage is not unexpected. Only a few adult animalsgo on to have prolonged longevity and attain the very largest propor-tions in the wild (Buffrenil et al., 1994).

DISCUSSION

The results of this study show that the unusual vermiform bones ofvaranids hold great promise for assessing longevity and growth patternsin both fossil and living monitor lizards. However, despite the com-monness of these elements in some taxa (often numbering into the thou-sands), they are perhaps easily missed in the field due to their smallsize and unusual forms that are not easily recognized as bones. Becauseof their possible phylogenetic value (Fejevary, 1918; Mertens, 1942;McDowell and Bogert, 1954) and capacity to reveal life history infor-mation, researchers collecting or examining fossil varanids should lookclosely for them in the future. (The same holds true for preparators ofextant taxa who apparently often throw them out during the skinningof specimens or when discarding refuse from dermestid-cleaned skele-tons.)

From these data it is clear that large Megalania, represented by QMF4452/3, achieved gigantism by sustaining juvenile growth rates for alonger period of time and delaying the onset of somatic adulthood.

Today’s considerably smaller monitors attain similar subadult growthrates in the wild (8–17 cm/yr SVL) but even the largest of these typi-cally acquire the majority of their adult body size within five to eightyears of birth (Auffenberg, 1981; Abdul et al., 1986; Buffrenil et al.,1994; K. Auffenberg, pers. comm.). This evolutionary pattern is thesame seen in giant extinct crocodylians (Erickson and Brochu, 1998)and is evidence for constraint to maximal growth potential in membersbelonging to the living groups of reptiles. The analysis of very largechelonians would be an interesting follow-up to test this theory. (Notethat although there is considerable sexual dimorphism in size amongvaranids, the aforementioned conclusions about M. prisca growth wouldlikely hold true regardless of the sex of QM F4452/3. Growth rates formale specimens of V. komodoensis and V. niloticus, are just 13% greaterthan those for females; Auffenberg, 1981; Buffrenil et al., 1994.)

Monitor lizards have been described as the reptilian equivalent offoxes owing to their unique active foraging techniques that include giv-ing chase to prey and their exceptional mammal-like physiological ca-pacities that include both speed and stamina (Hecht, 1975; Losos andGreene, 1988; Horn, 1999). Varanids also show some of the most rapidgrowth rates among living reptiles (Case, 1978). Given these consid-erations, it is perhaps no accident that a member of this particular lin-eage was able to rise to ‘‘lion-like’’ dominance (Rich, 1985; Losos andGreene, 1988) by delaying maturation to become larger. Further con-vergence on a mammal-like physiology was not required (Hecht, 1975).

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Based on the feats of its living Komodo cousin (Auffenberg, 1981), thelethality of a dinosaur-sized, serrate-toothed monitor lizard to an un-tapped Australian megafauna composed of giant kangaroos and wom-bats, diprotodontid marsupials, and enormous ground birds is unques-tioned (Rich, 1985; Flannery, 1991)—a missed stop in development wasall it took to unleash this ‘‘down under’’ version of the king of beasts.

Acknowledgments We thank Wayne King, Max Nickerson, KennyKrysco, and Kurt Auffenberg of the Florida Museum of Natural History,Jay Cole and Mark Norell of the American Museum of Natural History,Jacques Gauthier and the Yale Peabody Museum, the Queensland Mu-seum, Harry Greene, Rick Blob, Dave Durham, Neil Miner and theEast Bay Vivarium for their assistance with this research. We especiallythank Maureen Kearney and J. Scanlon for their thorough and helpfulcomments that greatly improved this manuscript. This study was fundedby a FYAP grant from the CRC of Florida State University and NSFGrant DBI 97-50190. This study is based upon work supported by theNational Science Foundation under a fellowship awarded in 1997. Anyopinions, findings, conclusions, or recommendations expressed in thispublication are those of the authors and do not necessarily reflect theviews of the NSF.

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Received 13 March 2002; accepted 15 November 2002.