A central role for venom in predation by Varanus komodoensis (Komodo Dragon) and the extinct giant Varanus (Megalania) priscus

Discussion

Bite force has been established as a predictor of prey size in extant mammalian carnivores (16, 17). Moreover, in placental and marsupial carnivores a tendency to take relatively large prey is typically reflected in the skull's ability to withstand the high forces generated during prey subjugation (18). Previous work has suggested weak bite forces in V. komodoensis (2), but whether similar relationships exist among reptiles and their prey has remained unclear. Consideration of gape angle shows that maximal bite forces previously predicted for V. komodoensis by using FE techniques (2) were underestimates (and suggests that future studies should consider this factor). Nonetheless, bite force remains much lower than in a C. porosus of comparable size, suggesting that bite force may not be a reliable indicator of prey size in extant varanid lizards. Our findings suggest that, relative to C. porosus, the skull of V. komodoensis is poorly adapted to resist the erratic forces generated in a sustained bite and hold attack on large prey. Further, it is least well adapted to resist torsion. In contrast, the V. komodoensis skull is best adapted to resist forces generated in pulling on a prey item (or a prey item pulling back). These results are consistent with observational data showing that V. komodoensis opens wounds by biting and simultaneously pulling on prey by using postcranial musculature (4), thereby supplementing relatively weak jaw adductors by recruiting postcranial musculature. Our findings are also in accord with the view that the killing technique of V. komodoensis is broadly similar to that of some sharks and Smilodon fatalis (saber cat). Despite obvious anatomical differences, these unrelated predators kill or are thought to have killed (respectively) large prey by using relatively weak bite forces amplified by sharp teeth and postcranial input (19, 20).

It has been argued that as an alternative or adjunct to direct physical trauma V. komodoensis possesses pathogenic bacteria in its saliva (4, 5) capable of delivering lethal toxic effects through induction of sepsis and bacteremia in its prey (4). Supposedly V. komodoensis tracks the infected prey item or, alternatively, another V. komodoensis specimen benefits from an opportunistic feed. Neither of these scenarios, however, has actually been documented. Regardless, septicemia is popularly accepted as an integral part of the predatory ecology. The feeding behavior of V. komodoensis has also been interpreted within this framework, such as being an altruistic behavior with a group level benefit. Further, it has been speculated that bacterial growth and delivery are facilitated by the production of copious quantities of bloody saliva (4). Although wild-caught individuals have been shown to harbor a variety of oral bacteria, no single pathogen was found to be present in all V. komodoensis studied (5). Moreover, the bacterial species identified were unremarkable in being similar to those identified in the oral cavities of other reptiles or being typical gut contents of the mammalian species on which they prey (21–23).

We also note that the laboratory mouse study (5) that attributed lethal effects from V. komodoensis saliva to the pathogen Pasteurella multocida could not confirm the presence of the pathogen in the majority of donor animals. P. multocida is not typical reptile flora but is prevalent in mammals, especially individuals already under stress from disease or old age (21–23). Because these individuals are often the ones selected as prey items by V. komodoensis, it seems likely that P. multocida, and other bacterial species, are transiently acquired flora of the prey animals and other environmental sources. This would explain the observed variability in bacterial load within and among individuals (5). Such interindividual variability makes it exceedingly unlikely that toxic bacteria could reliably induce sepsis in prey animals to the extent that this would become an evolutionarily successful mechanism on which V. komodoensis could rely on for prey capture. We conclude that there is no compelling evidence for the hypothesized role of pathogenic bacteria in the predatory ecology of V. komodoensis.

Although we dismiss pathogenic bacteria as integral to the feeding ecology of V. komodoensis, we consider that envenomation may play an important role given the presence of venom delivery systems in other varanids (6). Absence of a modified dental architecture such as the delicate, grooved venom-delivering helodermatid teeth is likely one of the reasons that the venomous nature of V. komodoensis has been overlooked. Consistent with the skull performing best in response to pulling forces, V. komodoensis instead uses its robust serrated teeth to cut compliant tissue in an expanded use of the “grip-and-rip” mechanism (24), resulting in 2 parallel extremely deep wounds in prey items (4), which would allow ready entry of the venom.

However, our analyses point to a further feature that distinguishes the feeding ecology of V. komodoensis from other sharp-toothed predators such as sharks or saber cats: venom. Adult specimens (in the range of 1.4–1.6 m and 5–8 kg) of the closely related and known venomous lizard V. varius (6), with their proportionally smaller heads relative to V. komodoensis, yield up 10 mg dry weight material obtained by gentle squeezing of the glands to obtain the major lumen liquid contents or up to 50 mg through the utilization of pilocarpine stimulation (thus obtaining full lumen liquid contents intracellular stored material). Our results show that a 1.6-m V. komodoensis has an internal gland volume of 1 mL and, utilizing the V. varius results as a foundation, we estimate that the total protein (liquid plus storage contents) would be 150 mg, with 30 mg of this in the form of readily deliverable major lumen liquid contents. Because gland size and venom yield increase proportionally with head size in reptiles (25), a full-sized (3 m) adult V. komodoensis would thus potentially yield up to1.2 mL and 200 mg in major lumen liquid contents or 6 mL of liquid and 1 g of dry material (full contents including storage).

We have shown that in the species that have developed secondary forms of prey capture (e.g., constricting) or have switched to feeding on eggs, the reptile venom system undergoes rapid degeneration characterized by significant atrophying of the glands, reduction in fang length, and accumulated deleterious mutations in the genes encoding for the venom proteins (9, 26, 27). This is a consequence of selection pressure against the bioenergetic cost of protein production (28). The robust glands and high venom yield in V. komodoensis thus argue for continued active use of the venom system in V. komodoensis.

Our data thus suggest that V. komodoensis venom potentiates the deep laceration-induced bleeding and hypotension through anticoagulative changes in blood chemistry (PLA₂ toxins) and shock-inducing lowering of blood pressure (CRISP, kallikrein, and natriuretic toxin types), with the prey item further immobilized by the hyperalgesic cramping AVIT toxins (Table 1). Our in vivo studies show that an i.v. dose of 0.1 mg/kg produces profound hypotension whereas 0.4 mg/kg is enough to induce hypotensive collapse (Fig. 4). Thus, a typical adult V. komodoensis prey item such as a 40-kg Sunda Deer would require 16 mg of protein to enter blood circulation to induce complete hypotensive collapse but only 4 mg to induce immobilizing hypotension. This is a realistic amount to deliver as even the weak delivery system of rear-fanged snakes, which may require a degree of mastication for venom delivery, can deliver >50% of the venom available in their glands (29). Such a fall in blood pressure would be debilitating in conjunction with blood loss and would render the envenomed prey unable to escape. These results are congruent with the observed unusual quietness and apparent rapid shock of prey items (4).

The predatory ecology of the V. komodoensis extinct gigantic close relative V. (Megalania) priscus is also unresolved. In particular, whether or not it was primarily a predator or a scavenger has remained an open question (20). Our recent finding of a common origin of the venom system in lizards and snakes (6) and the close evolutionary relationship between V. priscus and the clade of the predatory extant venomous lizards V. komodoensis, V. salvadori, and V. varius (30, 31) lends weight to the hypothesis that V. priscus was a combined-arsenal predator rather than a simple scavenger. Like the other members of this unique varanid lizard clade, the jawbones of V. priscus are also relatively gracile compared with the robust skull and the proportionally larger teeth similarly serrated (Fig. 3). Application of the “extant phylogenetic bracket” comparative approach (32) indicates that V. priscus used the same combined arsenal of large serrated teeth with anticoagulant and hypotension-inducing venom. Maximal body masses exceeding 2,000 kg and 7 m in length have been proposed for V. priscus (although such numbers rely on extrapolation well beyond available data ranges for extant lizards). However, even conservatively assuming geometric similitude (20) with large V. komodoensis suggests that its Pleistocene relative would have achieved at least 575 kg body weight and lengths exceeding 5.5 m. Scaling upward from V. komodoensis, we estimate that a varanid of this size range would produce a total stored venom protein yield (lumen liquid plus storage granules) reaching 6 g, with 1.2 g as readily deliverable major lumen liquid contents.

Our multidisciplinary analyses paint a portrait of a complex and sophisticated tooth/venom combined-arsenal killing apparatus in V. komodoensis and its extinct close relative V. priscus. Thus, despite a relatively weak skull and low bite force, we suggest that the combination of highly and very specifically optimized cranial and dental architecture, together with a capacity to deliver a range of powerful toxins, minimizes prey contact time and allows this versatile predator to access a wide range of prey including large taxa. These results indicate that V. priscus was the largest venomous animal to have ever lived.