Journal of Vertebrate Paleontology 23(4):966–970, December 2003 q 2003 by the Society of Vertebrate Paleontology
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VERMIFORM BONES AND THE EVOLUTION OF GIGANTISM IN MEGALANIA—HOW A REPTILIAN FOX BECAME A LION ´ NIL2, RALPH E. MOLNAR3, and MARK K. BAYLESS4, GREGORY M. ERICKSON1, ARMAND DE RICQLES2, VIVIAN DE BUFFRE 1Department of Biological Science, Florida State University, Tallahassee, Florida, 32306-1100, U.S.A.; 2Laboratoire d’Anatomie Compare ´ e, 2 place 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 extinct animal that attained lengths twice those typical for its living varanid cousin, the Komodo monitor (Varanus komodoensis) (Fig. 1 left). Despite competition from mammalian counterparts, it surprisingly came to reign superior as the largest terrestrial carnivorous taxon on the Australian continent during the late Cenozoic era (Flannery, 1991). Did M. prisca achieve great size by simply retaining juvenile reptilian growth rates as in giant extinct crocodylians (Erickson and Brochu, 1998), converge on the mammalian condition through accelerated growth as in dinosaurs (Erickson et al., 2001), or show a blending of both strategies? We generated the first life history data for this enigmatic animal using size estimations based on long-bone dimensions and longevity assessments from growth line counts in peculiar, formerly unidentified, dermal bones. The results showed that it attained gargantuan proportions by prolonging 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 large M. prisca skeleton. This particular specimen (Queensland Museum, QM F4452/3) was exhumed from unconsolidated Pleistocene sediments in the Springsure Rollestone area of Queensland, Australia. Notably, it represents one of the few partially complete representatives of this taxon. During examination it was observed that several of the vermiform elements had been fractured during diagenesis. Subsequent study of the broken surfaces using a low power (20–903) dissecting microscope revealed numerous growth lines. Since previous attempts to assess longevity in this specimen using long-bone and rib skeletochronology (5the study of osseous growth line formation, sensu Castanet and Smirina, 1990) failed owing to poor preservation and physiological remodeling (ADR and VDB, unpubl. data), this finding was exciting in that it rekindled the possibility to reconstruct the life history of M. prisca. We hypothesized that the strange bones found with QM F4452/3 were either osteoderms or gastralia, both of which are known to occur in extant monitor lizards (Dunn, 1927; Smith, 1935; McDowell and Bogert, 1954; Romer, 1956; Fuchs, 1977). To test these theories, hundreds of skeletonized, preserved, and study-skin specimens representing twenty-five monitor species in the collections of the Florida Museum of Natural History (UF; Gainesville), American Museum of Natural History (AMNH; New York), and the Yale Peabody Museum (YPM; New Haven) were examined for vermiform bones. It quickly became apparent that the peculiar elements were not gastralia, these bones being much larger and uniform in shape in living monitors. Conversely, osteoderms found in a minority of taxa (V. komodoensis, V. salvator, V. bengalensis, V. exanthematicus), provided a very close morphological match, aside from being somewhat smaller (Fig. 1 upper right). It was concluded that the strange fossilized bones were in fact osteoderms from QM F4452/3 scaled to giant size. The museum survey and subsequent histological preparations and literature review provided a clearer understanding of the likely development, 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, and legs (also see Smith, 1935; McDowell and Bogert, 1954; Fuchs, 1977; Auffenberg, 1981). The most highly contorted bones were prevalent in regions with high ossicle density, where physical or physiological influence of adjacent bones led to imbrication (and even fusion in V. komodoensis; also see Dunn, 1927). Straighter ossicles were found in regions with low bone density where interelemental influences on morphology were negated. Hematoxylin and eosin preparations (H&E staining; 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 the dermis, and usually in association with individual scales (Fig. 2 left). Functionally, the strange bones serve as a form of armor in these highly agonistic 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 revealed that the capacity of these structures for defense is particularly manifest in very old V. komodoensis where hundreds of ossicles will coalesce to form remarkable turtle-shell-like helmets over the snout and supraorbital regions (Fig. 2 right; also see McDowell and Bogert, 1954). Establishing the Periodicity of Growth Zone Formation in Living Monitors Auffenberg (1981) previously showed that ‘‘osteoderms’’ (presumably vermiform) from wild-caught V. komodoensis possess growth lines. To see if such rings exist in captive raised monitors, we made H&E preparations (Humason, 1979) using ossicles from three known-age specimens of V. salvator (4.5, 5.5, and 7.5 years old). The analysis revealed prevalent growth zones and lines of arrested growth (Fig. 3 left). Counts of zones in each ossicle were made and contrasted with age at death. The correspondence in numbers suggests an annual genesis of these histological structures (Table 1). These findings, coupled with results from the aforementioned nape skin preparations showing that many osteoderms begin forming prior to hatching (the entire compliment appears to have been initiated no later than the first year of life), suggests these bones can be used to assess longevity in monitor lizards—even in relatively old individuals. Assessment of Longevity in Megalania Given the utility of the vermiform bones to assess life history attributes in extant monitors, we turned our attention back to the fossilized elements from QM F4452/3. Histological preparations were made from three of the bones (see methods in Erickson and Tumanova, 2000). Each element was sectioned in a region that was particularly straight and the cross-sectional shapes approximated circles. Growth zone counts made under polarized microscopy revealed 16 definitive growth zones in each of the ossicles and thus a longevity estimate for QM F4452/3 of 16 years (Fig. 3 left). Assessment of Megalania Growth Dynamics In the final stage of our study we sought to reconstruct the growth dynamics of QM F4452/3. This can be done in varanids using annual
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FIGURE 1. Left, skeletal mount of a 5.5 m Megalania prisca in the Queensland Museum, Brisbane, Australia. Conservative estimates of total length 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 from M. prisca (QM F4452/3) compared to similar vermiform bones from the skin of a living monitor lizard, Varanus salvator (upper right). Note that 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 the dermis that is associated with an individual scale. Right, fused dermal ossicles that have formed a defensive helmet on the snout and supraorbital region 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).
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FIGURE 3. Inset left, histological section of a dermal ossicle from a known age 7.5-year-old monitor lizard Varanus salvator showing the expected eight growth zones. Equable findings were made for other ossicles from this specimen and from other individuals aged 4.5 and 5.5 years. Each of these specimens had been captured in the wild as neonates and raised in captivity. Left, growth line count revealing 16 growth zones for a thin-sectioned Megalania prisca dermal ossicle (QM F4452/3) viewed with polarizing light microscopy. Previous attempts to age Megalania 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. It was assumed that linear changes in ossicle size roughly paralleled changes in animal length. Error bars denote one standard deviation centered about the mean for measurements made on the three M. prisca ossicles available for study. Age of somatic maturity is noted for QM F5422/3 and for several large extant varanid taxa based on data from Auffenberg (1981), Abdul and Abdullah (1987/88), Andrews and Gaulke (1990), Buffre´nil et al. (1994), and Andrews (1995).
long bone growth, since radial appositional growth occurs in proportion to whole body growth (e.g., length) throughout ontogeny (Buffre´nil et al., 1994; Smirina and Tsellarius, 1998). We posited that similar analysis could be done using zonal bone formation in varanid dermal ossicles, since they show the same annual growth rhythm and a similar pattern whereby broad bands form early in ontogeny, and the widths decline at the age of somatic maturity. (We had hoped to test this application further using two specimens of V. albigularis, MKB personal collection, for which both size and age had been measured throughout life. Unfortunately our survey revealed that this taxon is barren of vermiform bones.) Given this, we utilized the proportions of annual growth in the ossicles to roughly estimate the growth dynamics in QM F4452/3. Mean proportions of annual growth within each ossicle were multiplied by the estimated amount of post-hatching bodily growth that occurred in QM F4452/3. For our bodily growth measure we chose to use snoutvent length (SVL) rather than total length since there is a strong interspecific trend of negative allometry in tail length in larger living monitors (Mertens, 1942). (Our own sampling showed this to occur beyond SVL of 60 cm [Fig. 4] making it indeterminable whether this trend would hold true when extrapolated to an animal the size of the giant TABLE 1.
extinct monitor.) Regression analysis of the data from Blob (2000) shows that SVL can be predicted accurately in living monitors of all sizes using femoral length and interspecific regression analysis (SVL 5 218.297 1 7.6257[femur length in mm], r-squared 5 0.97). In the case of QM F4452/3, its femoral length of 290 mm produced a SVL estimate of 2.19 m. From this, its approximate hatchling size (0.288 m) based on 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 occurred during life. Each of the 16 growth-zone proportions was multiplied by this 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 growth rate of QM F4452/3 was 14 cm/year (Fig. 3 right). Growth rates decreased following the 13th year of life, consistent with the asymptotic growth typical of vertebrates. Despite its great size, the QM F4452/3 was still actively growing at the time of death (5% or 10 cm SVL/yr
Growth-zone counts from known-age Varanus salvator dermal ossicles.
Sample number
Number 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)
1 2 3 4 5 6 7 8 Mean (Std. Dev.)/Expected
0 0 0 — — — — — 0 (0)/0
5 5 5 5 5 6 5 6 5.25(0.46)/5.0
6 7 6 6 5 6 6 — 6.0(0.58)/6.0
7 8 8 9 8 8 7 — 7.86(0.69)/8.0
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FIGURE 4. Tail length versus snout-vent length for a diversity of adult varanids. Specimens shown are the largest for each taxon (with complete tails) 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 point tail 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 it proportioned like the giant living monitor, V. komodoensis (1:1), or did it have an extremely short tail (Hecht, 1975)? Specimen numbers are available upon request from GME.
during the last two years of life), a finding that is consistent with unfused epiphyses of the femora. Although this suggests it may have had the potential to reach the upper bounds of size for this taxon, death at this developmental stage is not unexpected. Only a few adult animals go on to have prolonged longevity and attain the very largest proportions in the wild (Buffre´nil et al., 1994). DISCUSSION The results of this study show that the unusual vermiform bones of varanids hold great promise for assessing longevity and growth patterns in both fossil and living monitor lizards. However, despite the commonness of these elements in some taxa (often numbering into the thousands), they are perhaps easily missed in the field due to their small size and unusual forms that are not easily recognized as bones. Because of their possible phylogenetic value (Feje´vary, 1918; Mertens, 1942; McDowell and Bogert, 1954) and capacity to reveal life history information, researchers collecting or examining fossil varanids should look closely for them in the future. (The same holds true for preparators of extant taxa who apparently often throw them out during the skinning of specimens or when discarding refuse from dermestid-cleaned skeletons.) From these data it is clear that large Megalania, represented by QM F4452/3, achieved gigantism by sustaining juvenile growth rates for a longer period of time and delaying the onset of somatic adulthood.
Today’s considerably smaller monitors attain similar subadult growth rates in the wild (8–17 cm/yr SVL) but even the largest of these typically acquire the majority of their adult body size within five to eight years of birth (Auffenberg, 1981; Abdul et al., 1986; Buffre´nil et al., 1994; K. Auffenberg, pers. comm.). This evolutionary pattern is the same seen in giant extinct crocodylians (Erickson and Brochu, 1998) and is evidence for constraint to maximal growth potential in members belonging to the living groups of reptiles. The analysis of very large chelonians would be an interesting follow-up to test this theory. (Note that although there is considerable sexual dimorphism in size among varanids, the aforementioned conclusions about M. prisca growth would likely hold true regardless of the sex of QM F4452/3. Growth rates for male specimens of V. komodoensis and V. niloticus, are just 13% greater than those for females; Auffenberg, 1981; Buffre´nil et al., 1994.) Monitor lizards have been described as the reptilian equivalent of foxes owing to their unique active foraging techniques that include giving chase to prey and their exceptional mammal-like physiological capacities that include both speed and stamina (Hecht, 1975; Losos and Greene, 1988; Horn, 1999). Varanids also show some of the most rapid growth rates among living reptiles (Case, 1978). Given these considerations, it is perhaps no accident that a member of this particular lineage was able to rise to ‘‘lion-like’’ dominance (Rich, 1985; Losos and Greene, 1988) by delaying maturation to become larger. Further convergence 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), the lethality of a dinosaur-sized, serrate-toothed monitor lizard to an untapped Australian megafauna composed of giant kangaroos and wombats, diprotodontid marsupials, and enormous ground birds is unquestioned (Rich, 1985; Flannery, 1991)—a missed stop in development was all it took to unleash this ‘‘down under’’ version of the king of beasts. Acknowledgments We thank Wayne King, Max Nickerson, Kenny Krysco, 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 Museum, Harry Greene, Rick Blob, Dave Durham, Neil Miner and the East Bay Vivarium for their assistance with this research. We especially thank Maureen Kearney and J. Scanlon for their thorough and helpful comments that greatly improved this manuscript. This study was funded by a FYAP grant from the CRC of Florida State University and NSF Grant DBI 97-50190. This study is based upon work supported by the National Science Foundation under a fellowship awarded in 1997. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the views of the NSF. LITERATURE CITED Abdul, J., J. Hamzah, and W. M. W. Abdullah. 1986. Preliminary study on the growth rate and movement of water monitor lizard (Varanus salvator) at Sungai Tembeling Taman Negara. Journal of Wildlife and Parks 5:63–78. ———, and M. Amin bin Abdullah. 1987/1988. Growth rate and behavior of water monitor lizard (Varanus salvator) at SG. Tembeling, Taman Negara. Journal of Wildlife and Parks 7/8:58–66. Anderson, C. 1927. A gigantic extinct lizard. Australian Museum Magazine 3:132–133. Andrews, H. V. 1995. Sexual maturation in Varanus salvator (Laurenti 1768) with notes on growth and reproductive output. Herpetological Journal 5:189–194. ———, and M. Gaulke. 1990. Observations on the reproductive biology and growth of the water monitor (Varanus salvator) at the madras crocodile bank. Hamadrayad 15:1–5. Auffenberg, W. 1974. Combat behavior in Varanus bengalensis (Sauria: Varanidae). Journal of the Bombay Natural History Society 78:54– 72. ——— 1978. Social and feeding behavior in Varanus komodoensis; pp. 301–331 in N. Greenberg and P. H. Maclean (eds.), Behavior and Neurology of Lizards. National Institute of Mental Health, United States Department of Health, Education and Welfare. ——— 1981. The Behavioral Ecology of the Komodo Monitor. University Presses of Florida, Gainesville, 406 pp. Blob, R. W. 2000. Interspecific scaling of the hindlimb skeleton in lizards, crocodilians, felids and canids: does limb bone shape correlate with limb posture? Journal of Zoology, London 250:507–531. Buffre´nil, V. de, C. Chabanet, and J. Castanet. 1994. Donne´es pre´liminares sur la taille, la croissance et la longe´vite´ du varan du Nil (Varanus niloticus) dans la re´gion du lac Tchad. Canadian Journal of Zoology 72:262–273. Case, T. J. 1978. On the evolution and adaptive significance of postnatal growth rates in the terrestrial vertebrates. The Quarterly Review of Biology 53:174–192. Castanet, J., and E. Smirina. 1990. An introduction to the skeletochron-
ological method in amphibians and reptiles. Annales Scientifique Naturelle Zoologie 11:191–196. Dunn, E. R. 1927. Results of the Douglas Burden Expedition to the island of Komodo. I. Notes on Varanus komodoensis. American Museum Novitates 286:1–10. Erickson, G. M., and C. A. Brochu. 1998. How the ‘‘terror crocodile’’ grew so big. Nature 398:205–206. ———, and T. A. Tumanova. 2000. Growth curve and life history attributes of Psittacosaurus mongoliensis (Ceratopsia: Psittacosauridae) inferred from long bone histology. Zoological Journal of the Linnean Society 130:551–566. ———, K. Curry Rogers, and S. A. Yerby. 2001. Dinosaurian growth patterns and rapid avian growth rates. Nature 412:429–433. Feje´vary, Baron G. J. de. 1918. Contributions to a monograph on fossil Varanidae and on Megalanidae. Annales Museum Naturelle Hungarici 16:341–467. Flannery, T. 1991. The mystery of the meganesian meat-eaters. Australian Natural History 23:722–729. Fuchs, H. von Kh. 1977. Histologie und mikroskopische Anatomie der Haut des Bindenwarans. Stuttgarter Beitra¨ge zur Naturkunde Serie A (Biologie) 299:1–16. Hecht, M. K. 1975. The morphology and relationships of the largest known terrestrial lizard, Megalania prisca Owen, from the Pleistocene of Australia. Proceedings of the Royal Society of Victoria 87:239–252. Horn, H. 1999. Evolutionary efficiency and success in monitors: a survey on behavior and behavioral strategies and some comments. Mertensiella 11:167–180. Humason, G. L. 1979. Animal Tissue Techniques, 4th ed. W. H. Freeman and Company, San Francisco, 661 pp. Losos, J. B., and H. W. Greene. 1988. Ecological and evolutionary implications of diet in monitor lizards. Biological Journal of the Linnean Society 35:379–407. McDowell, S. B., and C. M. Bogert. 1954. The systematic position of Lanthanotus and the affinities of the anguimorphan lizards. Bulletin of the American Museum of Natural History 105:1–142. Mertens, R. 1942. Die familie der warane (Varanidae). Parts 1–3. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft 465:1–399. Murphy, J. B., and L. A. Mitchell. 1974. Ritualized combat behavior of the pygmy mulga monitor lizard, Varanus gilleni (Sauria: Varanidae). Herpetologica 30:90–97. Rich, T. H. 1985. Megalania prisca: the giant goanna; pp. 152–155 in P. V. Rich, G. F. van Tets, and F. Knight (eds.), Kadimakara: Extinct Vertebrates of Australia. Princeton University Press, Princeton. ———, and B. Hall. 1979. Rebuilding a giant. Australian Natural History 19:310–314. Romer, A. S. 1956. Osteology of the Reptiles. University of Chicago Press, Chicago, 772 pp. Smirina, E. M., and A. Y. Tsellarius. 1998. Vital bone marking of desert monitor (Varanus griseus DAUD). Russian Journal of Herpetology 5:156–159. Smith, M. A. 1935. The Fauna of British India. Reptilia and Amphibia. Vol. 2—Sauria. Taylor and Francis Ltd., London, 440 pp. Thompson, G. G., and E. R. Pianka. 2001. Allometry of clutch and neonate sizes in monitor lizards (Varanidae: Varanus). Copeia 2001:443–458. Received 13 March 2002; accepted 15 November 2002.