Wroe, 2002

P u b l i s h i n g

Australian Journal of Zoology Volume 50, 2002 Š CSIRO 2002

A journal for the publication of the results of original scientific research in all branches of zoology, except the taxonomy of invertebrates All enquiries and manuscripts should be directed to: Australian Journal of Zoology CSIRO Publishing PO Box 1139 (150 Oxford St) Collingwood, Vic. 3066, Australia Telephone: +61 3 9662 7622 Fax: +61 3 9662 7611 Email: publishing.ajz@csiro.au Published by CSIRO Publishing for CSIRO and the Australian Academy of Science

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Australian Journal of Zoology, 2002, 50, 1–24

A review of terrestrial mammalian and reptilian carnivore ecology in Australian fossil faunas, and factors influencing their diversity: the myth of reptilian domination and its broader ramifications S. Wroe Centre for Research into the Evolution of Australia’s Total Ecosystems, Mammal Section, Australian Museum, 6–8 College Street, Sydney, NSW 2000, Australia, and Vertebrate Palaeontology Laboratory, School of Biological Sciences, University of New South Wales, Sydney, NSW 2052, Australia.

Present address: Institute of Wildlife Research, School of Biological Sciences A08, University of Sydney, NSW 2006, Australia.

Email: swroe@bio.usyd.edu.au

Abstract The notion that Australia’s large, terrestrial carnivore faunas of the middle Tertiary to Pleistocene were dominated by reptiles has gained wide acceptance in recent decades. Simple but sweeping hypotheses have been developed seeking to explain this perceived ecological phenomenon. However, a review of the literature does not support these interpretations, which are based on largely speculative and, in many cases, clearly erroneous assumptions. Few size estimates of fossil reptilian taxa are based on quantitative methodology and, regardless of method, most are restricted to maximum dimensions. For species of indeterminate growth, this practice generates misleading perceptions of biological significance. In addition to misconceptions with respect to size, much speculation concerning the lifestyles of large extinct reptiles has been represented as fact. In reality, it has yet to be demonstrated that the majority of fossil reptiles underpinning the story of reptilian domination were actually terrestrial. No postcranial evidence suggests that any Australian mekosuchine crocodylian was less aquatic than extant species, while a semi-aquatic habitus has been posited for madtsoiid snakes and even the giant varanid, Megalania. Taphonomic data equivocally supports the hypothesis that some Australian mekosuchines were better adapted to life on land than are most extant crocodylians, but still semi-aquatic and restricted to the near vicinity of major watercourses. On the other hand, the accelerating pace of discovery of new large mammalian carnivore species has undermined any prima facie case for reptilian supremacy regarding pre-Pleistocene Australia (that is, if species richness is to be used as a gauge of overall impact). However, species abundance and consumption, not richness, are the real measures. On this basis, even in Pleistocene Australia, where species richness of large mammalian carnivores was relatively low, available data expose the uncommon and geographically restricted large contemporaneous reptiles as bit players. In short, the parable of a continent subject to a Mesozoic rerun, wherein diminutive mammals trembled under the footfalls of a menagerie of gigantic ectotherms, appears to be a castle in the air. However, there may be substance to some assertions.

Traditionally, erratic climate and soil-nutrient deficiency have been invoked to explain the perception of low numbers or relatively small sizes of fossil mammalian carnivore taxa in Australia. But these arguments assume a simple and positive relationship between productivity, species richness and maximum body mass and either fail to recognise, or inappropriately exclude, other factors. Productivity has undoubtedly played a role, but mono-factorial paradigms cannot account for varying species richness and body mass among Australia’s fossil faunas. Nor can they explain differences between Australian fossil faunas and those of other landmasses. Other factors that have contributed include sampling bias, a lack of internal geographic barriers, competition with large terrestrial birds and aspects of island biogeography unique to Australia, such as landmass area and isolation, both temporal and geographic.

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Introduction In 1887 Richard Owen, by then pre-eminent among students of Australian palaeontology for half a century, made the following statement: ‘The picture of [Pleistocene] mammalian life in the Australian continent paralleled, of old, that still manifested in Asia and Africa: © CSIRO 2002

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huge herbivorous quadrupeds were kept in check by large and powerful carnivorous ones …’. However, in recent decades, perception of the composition of Australia’s terrestrial Pleistocene carnivore faunas has changed, culminating in the suggestion by Esmee Webb (1998) that ‘The only carnivores known to have preyed on the very largest extinct marsupials were poikilotherms’. Thus, by the end of the 20th century, the ‘large and powerful’ marsupial predators envisioned by Owen (1887), had been completely displaced by reptiles. Lately, this concept of reptilian domination of Australia’s large terrestrial carnivore niches has been predated to encompass the entirety of Australian prehistory back to at least early Miocene times (Flannery 1991, 1994). Reinterpretations of the relative significance of reptilian and mammalian carnivores in pre-Holocene Australia are not of purely academic interest, but have been promoted as central to broad hypotheses attempting to explain a range of ecological phenomena in Australia. The context, history and validity of the science behind this apparent reversal of opinion since Owen’s time are the subjects of the following essay.

Origins of the debate: resurrected carnosaurs and marsupial pussy cats Owen’s interpretation of Australia’s Ice Age ecology stood for decades. The most readily identifiable catalyst for this change was a long time coming and, surprisingly, was not based on the discovery of any new fossil species. The evidence in question was drawn from a study of the giant varanid, Megalania prisca, forwarded by Max Hecht in 1975. At the crux of Hecht’s investigation was an estimation of the maximum size of M. prisca. He produced figures of 7 m for total length and 600–620 kg for body mass. The estimate of maximum length was based on rather incomplete material and his methodology for estimating maximum mass was perhaps inappropriate. Specifically, maximum length was deduced on the basis of extrapolation from a single phalanx. The mass of the animal to which this phalanx belonged was determined as follows: a hand-fitted graph of mass versus length for an unknown number of unidentified lizard species that grew to around 3 kg, as supplied by Pough (1973), provided a basis; on to this was plotted the hypothetical body mass of a 3-mlong Varanus komodoensis, as estimated by Auffenberg (1972); Hecht, having calculated a maximum of 7 m, extrapolated further in order to obtain a corresponding figure for mass.

At this point he had exceeded Pough’s original data range by more than two orders of magnitude. While this method might have seemed reasonable at the time, it is unlikely that it would be widely accepted today, but these results still figure prominently in discussion over the role of reptiles in Pleistocene Australia.

As it turns out, the phalanx that formed the basis of Hecht’s deductions was probably not from Megalania prisca (R. Molnar, personal communication).

Apparently with a view to cementing the position of Megalania prisca as the apical predator of its day, Hecht (1975) further determined (p. 247) that the ‘bizarre’ Thylacoleo [marsupial lion] ‘… certainly could not have filled the big felid niche’ and strongly implied that M. prisca could, although no supporting arguments were tendered. Neither were estimates of minimum or average total lengths and masses.

It seems unlikely that Owen, who described both Thylacoleo carnifex (Owen 1859) and Megalania prisca (Owen 1860), would have agreed with Hecht (1975) on the question of Pleistocene marsupial lion ecology (see Owen 1887). It may be that Hecht’s interpretations were influenced by prior arguments for herbivory in T. carnifex (Flower 1868; Cope 1882).

At any rate, more recent studies have concluded that not only was T. carnifex a large, hypercarnivorous, felid-like predator (Wells et al. 1982), but that, among felids, its closest ecomorphological equivalents were machairodont sabre-tooths. Members of this felid

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subfamily are widely recognised as specialist hunters of very big prey, including juvenile mammoth (Janis 1994; Wroe et al. 1999; Wroe 2000).

In subsequent investigations that have supported the hypothesis of reptilian domination, Hecht’s (1975) maximum estimates of size for Megalania prisca are typically cited (Diamond 1992; Webb 1998). Others have provided still larger estimates: Flannery (1994, p. 113) describes M. prisca as reaching ‘up to a tonne in weight’ and being ‘about the size of a medium-sized Allosaurus’, Flannery (1998) states that M. prisca ‘… must have weighed several tonnes’, while Webb (1998) evidently misquotes Hecht (1975) in describing M. prisca as a monitor lizard weighing 1000 kg (Hecht 1975)’. On the basis of overall similarity in shape with a hypothetical 10-ft (3.04 m), 250-kg V. komodoensis, Auffenberg (1981) suggests that 4.5-m M. prisca would have weighed up to 2200 kg. But this assumed that the animal had just eaten 80% of its own body mass and seems to have been further marred by miscalculation. Using Auffenberg’s (1981) method and the body mass of 102 kg he gives for a 10-ft (3.04 m) ‘empty’ V. komodoensis, my estimate for a 4.5m M. prisca is 331 kg. Refreshingly, Burness et al. (2001) have recently provided an estimate of mean adult body mass for the giant varanid of 380 kg. Unfortunately, they provide neither the raw data nor the methodology used to determine it.

However, although Hecht (1975) did not provide mean total lengths or masses for Megalania prisca, he did give estimates of minimum and average head–body length. If Hecht’s methodology is applied to these data, the total length of the smallest mature M. prisca is less than 2.20 m and the average is around 3.45 m. Among living varanids the closest comparisons that can be made for M. prisca are with the Komodo dragon (Varanus komodoensis). As with M. prisca, size in this species appears to be subject to considerable hyperbole. In the course of an extensive 13-month field study, the heaviest wild-caught specimen obtained by Auffenberg (1981) was 54 kg and it seems likely that this specimen had recently consumed a large meal, as similar-length specimens (actual lengths not given) weighed as little as 35 kg. The largest verifiable mass recorded for a wild-caught Komodo dragon remains 54 kg. Auffenberg (1981) notes that captive animals can be much heavier, but that it is likely that these are overweight. Ciofi (1999) alludes to a robust male V. komodoensis of about 2.5 m long weighing 54 kg. A very large male captive individual at Taronga Park Zoo is 2.75 m and 80 kg (Taronga Park Zoo, unpublished). Using these figures, on the basis of geometric similtude the average 3.45-m-long M. prisca weighed 118–158 kg. Recent independently derived estimates have placed the maximum length of M. prisca at 4.67 m and mean adult length at 3.3 m (R. Molnar, personal communication).

Using this latter figure, the mean adult body weight would have been between 103 and 138 kg. Alternatively, assuming an average snout–vent length of 2.3 m for M. prisca, as given

by Hecht for mature individuals and using the equation provided by Blob (2000) for predicting mass in varanids, including V. komodoensis, the mean adult body mass of the giant varanid was 96.98 kg.

As with all estimates, there are problems with these. Megalania prisca may or may not have been as robust as Varanus komodoensis and its tail may or may not have been relatively short, as in this biggest living lizard. Animals often become more heavily built as they get larger. If this applies to M. prisca, then the mean masses derived on the basis of geometric similtude that I present here are underestimates. But tempering this is the likelihood that the higher figures are derived using a captive animal that is likely to be overweight. The prediction based on Blob’s (2000) equation does require some extrapolation, although relatively little compared with that of Hecht (1975); however, it has the advantage of not incorporating guess work for tail length, which is highly variable among varanids. At any

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rate, I’d argue that on the basis of the limited data available, at present, a best estimate for average adult body mass in M. prisca is between 97 and 158 kg. To give some standard for comparison, a 3.4-m Crocodylus porosus weighs about 155 kg (Webb and Manolis 1989).

Concomitant with the apparent up-sizing of the giant monitor has been a down-sizing of Thylacoleo carnifex. Owen (1859) unambiguously interpreted T. carnifex as lion-like with regard to both size and habit. The average body masses of male and female Panthera leo are around 150 and 170 kg respectively (Van Valkenburgh 1990). Martin (1984) gives an estimate of 200 kg. However, successive predictions have seen Australia’s largest marsupial carnivore reduced from parity with P. leo as follows: 75–100 kg (Murray 1984), 50–70 kg (Flannery 1991), 40–60 kg (Flannery 1994), 40 kg (Flannery 1998) and 20 kg (Webb 1998).

In the course of 14 years, the marsupial lion has shrunk by as much as an order of magnitude, but in no instance have these estimates been based on any quantitative or defined methodology. This spiraling trend may have stalled, with Burness et al. (2001) providing a mean body mass estimate of 73 kg, although, as with M. prisca, method and data are not supplied.

Of particular importance here is that while studies subscribing to the notion of reptilian domination commonly cite only the maximum estimated dimensions of Megalania prisca, the size of Thylacoleo carnifex is typically given as a range or compared with a living species (Murray 1984; Rich and Hall 1984; Flannery 1994). Apples are compared with oranges and the result is misleading. The same is also typically true with respect to sizes given for large or gigantic living reptiles (Pope 1962). Assessing the ecology of species on the basis of absolute maxima generates gross misconceptions, especially where the subjects are of indeterminate growth (Pope 1962). For example, the verifiable maximum for the saltwater crocodile (Crocodylus porosus) is about 6.7 m and some have doubtless grown larger still (Webb and Manolis 1989). Such animals may have weighed 1.5 tonnes or more, but, even in historical terms, individuals of these dimensions have always been extremely rare (Webb and Manolis 1989). While it may be reasonable to speculate on the upper limits of prey size that such giants were capable of taking, it is not reasonable to portray such limits as within or even approaching the normal range. Male C. porosus rarely exceed 5.2 m in length and a body mass of 500 kg, while females rarely exceed 3.4 m and 155 kg (Webb and Manolis 1989). And these figures again are maxima, not means.

Given that no complete skull of Megalania prisca is known and that the postcranial skeleton is very poorly represented (Molnar 1990), it is worth reiterating that any estimates of size in this species must be taken with a grain of salt. But if comparisons are to be made then estimated averages are of more value. The only mean body mass estimates for Thylacoleo carnifex based on published data and quantitative methodology are 101 and 130 kg (Wroe et al. 1999). These figures place the marsupial lion below the averages of the two largest living cats (Panthera leo and Panthera tigris), but significantly above the third heaviest (Panthera onca). Even the lesser of these two averages for T. carnifex is more than twice that of Panthera pardus, with which it has often been compared in recent times (Wroe et al. 1999).

These results suggest that while the very largest Megalania prisca were probably much heavier than the largest Thylacoleo carnifex, on average M. prisca ranged somewhere between parity with T. carnifex and 50% heavier. Given this turnaround with respect to relative sizes, the question of which was the more significant predator in terms of impact on Australia’s Pleistocene faunas bears revisiting. A conclusive response can not be given without accurate data pertaining to the actual biomasses, ranges and habits of the species in question.

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Of the two, only for T. carnifex is there convincing evidence for active hunting of megafauna (Scott and Lord 1924; Wroe et al., in press). As mentioned above, the closest extant analogue to M. prisca is the Komodo dragon, and while Varanus komodoensis can be a very effective predator, able to kill prey much larger than itself, carrion constitutes a significant proportion of its diet (Auffenberg 1981). As a scavenger it is highly efficient and known to eat almost 90% of a carcass, including hooves and hides (Ciofi 1999). Auffenberg (1981, p. 222) observes ‘When finished with a carcass an ora [Komodo dragon] leaves only a few traces – a smudge of blood, the intestinal contents, and often a few tufts of hair from the hide’. Large felids are more fastidious and tend to leave 25–30% of a kill (Ciofi 1999).

On the basis of tooth structure, T. carnifex is even less well suited to scavenging than are extant cats (Wroe et al.1999). The Komodo dragon is indisputably the top predator within its community – hence there are few carcasses left by other taxa for it to feed from, excepting those killed by conspecifics. This was not so in Pleistocene Australia and because T. carnifex was, on anatomical grounds, singularly inadequate as a processor of bone, it probably left significant parts of any large kill untouched. Large varanids are particularly well adapted to a scavenging role (Teaford et al. 2000), and results of the only relevant study performed to date suggest that in Australia carrion may dominate their diet (Guarino 2001).

Consequently, I posit that much of the diet of M. prisca probably consisted of carrion in the form of unused marsupial lion kills and that rather than standing over T. carnifex, the giant varanid was more likely to have subsisted on the predatory marsupial’s table scraps.

Among fossil faunas, Australia’s other prominent and speciose mammalian carnivore taxon, Thylacinidae, was also bereft of bone-cracking taxa and this includes the recently extinct Thylacinus cynocephalus (Wroe and Musser 2001). Even following the ascendancy of dasyurids in the mid–late Miocene, relatively few species of large marsupial bonecruncher are known to have evolved.

Consumption is another pertinent issue. Being ectothermic, Megalania prisca would certainly have required much less per kilogram of body mass than the marsupial lion. A 1.0kg dasyurid requires about 13.6 times the energy and 11.2 times the water needed by a varanid of the same size (King and Green 1999). This subject is treated in more detail below, but how this disparity might translate to the respective requirements of a 97–158-kg varanid and 101–130-kg thylacoleonid is unclear. Still, most would accept that unless M. prisca was far more common and widespread than the marsupial lion, its direct impact on prey populations would have been significantly less, even if we assume that it was equally predacious.

But Megalania prisca was probably rare (Rich and Hall 1984). For example, of 28 Pleistocene fossil sites considered Australia-wide by Roberts et al. (2001), only one contained remains of the giant varanid. Of these same sites, nine contained Thylacoleo carnifex. This is despite the fact that dentitia are the most commonly preserved part of either species and that M. prisca had far more teeth. Moreover, in the varanid these, unlike those of T. carnifex, were replaced throughout life. Varanus komodoensis is known to live for decades (Auffenberg 1981). The giant varanid almost certainly could live longer still and would likely have produced scores of teeth within a lifetime (M. Thompson, personal communication). So, if M. prisca was as common as T. carnifex we would expect to find far more specimens instead of far less. Some unknown taphonomic phenomena may have biased against M. prisca but, at present, the most parsimonious conclusion is that the animal was very uncommon.

In a study of some relevance to this debate conducted between 1991 and 1993, Varanus gouldi were removed from two dunes from the Simpson Desert west of Birdsville, while the

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marsupial carnivore Dasycercus cristicauda was expunged from another two. No measurable impact was observed on small mammal populations in those areas denuded of V. gouldi, but populations increased dramatically in the areas where D. cristicauda was no longer present (C. Dickman, unpublished).

A final point of interest here, pertaining to the question of which taxon was the dominant terrestrial predator, is that lateral compression of the sagittal crest in M. prisca supports the interpretation that it was semi-aquatic (Molnar 1990).

The role of other Pleistocene reptiles in the development of the parable: ‘giant’ snakes and ‘terrestrial’ crocodiles Perceptions of the respective sizes of Thylacoleo carnifex and Megalania prisca have not been the only bases for hypotheses of reptilian domination of large terrestrial carnivore niches in the Australian Pleistocene. The inferred habits and dimensions of more recently described fossil reptiles have further buttressed the argument in the eyes of many.

The giant snake In an article intriguingly entitled ‘Small fossil vertebrates from Victoria Cave, Naracoorte, South Australia.’, Smith (1976) described a new Pleistocene species of fossil snake and named it Wonambi naracoortensis. On the basis of more complete material Barrie (1990, p. 148) observed that ‘Wonambi was a large, heavy-bodied snake, though its skull, teeth and anterior vertebrae are relatively small and delicate.’ As with Megalania prisca, only an estimated maximum length was provided. This was calculated at between 5.39 and 6.13 m on the basis of analogy with the python Morelia spilota. However, as noted by Scanlon (1997), pythons are relatively long snakes and calculations based on a pythonine paradigm are likely to be overestimates. Scanlon (1997) considers that such an overestimate is not likely to be great. However, relatively small increases in length translate into considerable differences in mass (Wroe 2000). For example, assuming geometric similtude, a 6.13-m snake would be about 47% heavier than a 5.39-m one. In addition to an estimate of maximum length, Barrie (1990) further speculated that a 6-m-long individual could have weighed 250 kg, although how this estimate was arrived at is unclear. Subsequently, W. naracoortensis has been described as being ‘over 50 kilograms’ (Flannery 1991, p. 728) and ‘over 100 kg in weight’ and up to 6 m long with a head ‘… the size of a shovel’ (Flannery 1994, p. 113). More recently, Scanlon and Lee (2000) diagnosed W. naracoortensis as having a ‘… total length estimated to exceed 5 m’.

Although Wonambi naracoortensis was a heavily built snake, it was less so than the heaviest of living snakes, Eunectes murinus, the green anaconda or water boa (J. Scanlon and R. Shine, personal communication). No estimates are available for the body mass of W. naracoortensis based on quantitative analyses. Body mass data even for living snakes is hard to come by (Ernst and Zug 1996). A big female E. murinus, 5.04 m in length, is recorded as being 54 kg by Rivas (1999). No complete skull is known for W. naracoortensis.

The reconstructed skull based on fragments of the largest known specimen of W. naracoortensis from the type locality is 135 mm long but, on the basis of mandibular fragments, Scanlon and Lee (2000) estimate a maximum of 160 mm. This is significantly shorter than the 168 mm recorded for the largest of a sample of 560 adult specimens of Sumatran reticulated python (Python reticulatus), measured by Shine et al. (1998). The longest of these wild-caught individuals was about 6.8 m, while the mean length for mature females was 4.13 m. The heaviest among this sample was 75 kg and the mean body mass for adult females was 17.639 kg, or 0.235 of the maximum. The mean for adult males was

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5.899 kg or 0.079 of the maximum (Shine et al. 1998). Of these 560 adults, only two exceeded 30 kg. I have been unable to find a record of mean body masses for adult E. murinus. However, I suggest that, on the basis of information at hand, and assuming that W. naracoortensis was as robust as E. murinus and that it grew to 5 m in length, then a rough estimate of mean adult body mass for the species would be between 4.27 kg (54 kg × 0.079) and 12.69 kg (54 kg × 0.235).

That this estimate is inexact is accepted; it may also be that selective predation on Python reticulatus by humans has produced a skewed distribution, with large specimens underrepresented (M. Archer, personal communication). If so, then the average calculated here would be an underestimate although the use of the massive green anaconda as a template for extrapolation would offset this. Additionally, it is unlikely that the known sample of W. naracoortensis comprises examples of the very largest individuals, but then this applies to all fossil taxa and in the absence of more comprehensive studies it meanwhile represents an honest attempt to provide an average value.

With respect to the ecology of Wonambi naracoortensis, Flannery (1994) suggests that the animal probably specialised in taking wallaby-sized prey. Wallaby species range in average body mass from about 5 to 15 kg (Archer 1985). But the conclusion of Flannery (1994) appears to have been founded on two erroneous deductions, the first being that W. naracoortensis had a shovel-sized head (Scanlon and Mackness, in press) and the second being that the average length of the species was 6 m. Barrie (1990, p. 148) argues that ‘… large prey capable of struggling vigorously are unlikely to have been taken, since Wonambi’s jaws were rather weak’ and that ‘… reduction in lateral flexion would limit its ability to constrict animals, thus implying that it subsisted mainly on small prey’. In fact, at present there is no reason to believe that W. naracoortensis (or, for that matter, any madtsoiid), was a constrictor by habit. The presence of a large number of relatively small, weak teeth in this species led Barrie (1990) to further posit that ‘It is possible that Wonambi had feeding habits similar to those of Acrochordus [aquatic file snakes], fish being available in the lagoons of its habitat’. Scanlon and Lee (2001) suggest that Yurlunggar, another large madtsoiid was semi-aquatic. In addition to weak jaws, small teeth and limited lateral flexion, it is also now clear that W. naracoortensis lacked the ability to fully disarticulate its jaws in the fashion typical of all modern snakes (Scanlon and Lee 2000). This would have limited the size of potential prey. Wonambi naracoortensis may have been adapted to a rockclimbing lifestyle (J. Scanlon, personal communication). Given that the species is typically found in cave deposits, a diet consisting largely of bats is an obvious possibility. Finally, while W. naracoortensis had a relatively wide distribution in southern and eastern Australia, it was apparently uncommon throughout this range (Scanlon 1992): in the 28 Pleistocene sites examined by Roberts et al. (2001) only one contained W. naracoortensis.

The terrestrial crocodile The third large Pleistocene reptile commonly invoked in arguments for reptilian domination of Pleistocene Australia is the allegedly terrestrial Quinkana fortirostrum. Distinctive ziphodont teeth possibly belonging to this species were first noted by Plane (1967). Hecht and Archer (1977) described a Pleistocene ziphodont crocodylian from the Texas Caves of south-eastern Queensland later referred to Quinkana sp. by Molnar (1981). In the same paper Molnar formally described Q. fortirostrum based on the rostral portion of a skull from Tea Tree Cave, north Queensland. Molnar gave no estimate of size for Q. fortirostrum based on this material, and no more complete specimen has been described since. Nonetheless, several estimates have been forthcoming in subsequent years. Flannery (1994) and Webb

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(1998) settle on a body mass of over 200 kg and a length of 3 m. How these estimates were arrived at, or whether they represent estimated averages or maxima, was not stated.

Regardless, such a body mass seems unlikely for a 3-m-long crocodylian. At this length, the very robust Crocodylus porosus averages 94 kg. If this is a maximum length then the average body mass was probably much less. A 2-m C. porosus weighs about 25 kg and at 1.5 m average body mass is 9.5 kg (Webbs and Manolis 1989).

Regarding the status of Quinkana fortirostrum (and other fossil reptiles) as a terrestrial species, I have been unable to find any clear definitions in the literature, but suggest the following: terrestrial species are those that hunt and feed on land, at no stage in their ontogeny live in water and can reproduce and thermoregulate indefinitely in the absence of permanent water sources; semi-aquatic taxa are those that may hunt and feed on both land and in water, but cannot reproduce and sustain thermoregulation indefinitely in the absence of permanent water sources (this includes all living crocodylians).

The issue of whether reptilian taxa are terrestrial, semi-aquatic or aquatic is an important one. The reasons at a semantic level are obvious. Reptiles did not dominate large terrestrial carnivore niches if they were aquatic. Unless species are truly terrestrial and not tied to major water sources in an obligatory sense for any aspect of their biology, then their potential impact has to be qualified in line with the very significant range restrictions that such dependence entails. Still, semi-aquatic and aquatic species can influence terrestrial biotas where they take terrestrial prey and clearly this is a complicating factor. But, if we are to include aquatic and semi-aquatic species, then it must be borne in mind that on all continents excepting Antarctica and Europe, the largest extant predators of terrestrial prey are crocodylians. Full assessment would require comparisons based on mean body masses, generally unavailable in the literature, but North America and Asia are each home to least two crocodylian species growing to lengths exceeding 5 m that include terrestrial prey in their diets (Alderton 1991). In South America, with eight species of crocodylian, the three that grow to 5 m or more are also known to take terrestrial quarry, as are most of the remaining taxa (Alderton 1991). As well as a diverse crocodylian fauna, South America is home to two gigantic snakes, the terrestrial Boa constrictor and the semi-aquatic Eunectes murinus. Also of relevance is the fact that large ‘terrestrial’ crocodylians are also known from the middle–late Tertiary of South America (Busbey 1986). Even in Africa, famous for its diverse large mammalian carnivore fauna, perhaps the biggest predator of terrestrial prey is the formidable Crocodylus niloticus, but, again, no mean values are available.

The image of Quinkana fortirostrum as a terrestrial crocodylian has been widely accepted. Flannery (1994, p.113) asserts that it ‘probably had hoof-like feet’ and that we ‘know it was terrestrial because it has been found in cave deposits far from water associated with an entirely terrestrial fauna’. Yet, no direct anatomical data support the hypothesis of a terrestrial habitus for this species. Historically, for Q. fortirostrum and all other supposedly terrestrial Cainozoic crocodylian taxa, in Australia and elsewhere, anatomybased arguments for a terrestrial lifestyle have been founded largely on the basis of cranial and dental similarity (but not necessarily close relationship) with an Early Tertiary European taxon, Pristichampsus (Molnar 1981; Salisbury 2001). Rossmann (2000) has recently reargued the case for a terrestrial habitus in this animal, but this view is not accepted by all specialists in the field (S. Salisbury, personal communication).

In addition to a ziphodont dentition, common features shared by Pristichampsus and other allegedly terrestrial crocodylians are laterally compressed teeth, a deep snout and laterally directed orbits. Willis (1993) further observes that a tendency to hold the head above the body is another feature that might be associated with a terrestrial habitus.

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Pristichampsus was interpreted as a land-living animal largely because of its hoof-like unguals and evidence for a rounded tail (Molnar 1981). However, the hooves of Pristichampsus are an artefact of preservation (Rossmann 2000; S. Salisbury, personal communication), while Willis (1993) observes that at least three extant, semi-aquatic crocodylian taxa have deep heads with laterally directed orbits. Laterally compressed teeth are also present in at least one of these living taxa, Paleosuchus (Salisbury and Willis 1996).

Ouboter (1996) observes that in this genus the head is held high.

The extant Paleosuchus possesses four of the five cranial and dental attributes typically used to sustain arguments for a terrestrial habitus in fossil crocodylians. While it has been suggested that Paleosuchus may spend more time on land than most other living crocodylians, the evidence is not clear-cut (Paolillo and Gorzula 1985; Magnusson and Lima 1991; Oboter 1996; C. Stevenson, personal communication). In one study, Paleosuchus trigonatus was shown to eat significantly more terrestrial prey than its congeneric, P. palpebrosus (Magnusson et al. 1987), although the diet of this second species did not differ from that of Caiman crocodilus and Melanosuchus niger. Moreover, the study of Magnussan et al. (1987) was restricted. Ouboter (1996) determined that in other habitats the diet of P. trigonatus contained no more terrestrial species than were found in other crocodylians, while Salisbury and Frey (2001) conclude that the locomotor behaviour of Paleosuchus is essentially that of a generalist.

At present, while available evidence suggests that Paleosuchus trigonatus is an adaptable species that may, under some circumstances, spend more time on land than other crocodylians (including its congeneric), it is still semi-aquatic. Finally, although it is true that Paleosuchus lacks one characteristic present in Pristichampsus and other supposedly terrestrial crocodylians, serrated teeth, as noted by Molnar (1981) the presence of a ziphodont dentition suggests only that an animal took relatively large prey and says nothing about whether it was aquatic or terrestrial. Serrated teeth, as found ziphodont crocodylians, are also present in species ranging from great white sharks (Carcharodon carcharias) to Varanus komodoensis.

Only for one other Cainozoic crocodylian is there postcranial evidence that has been interpreted as indicative of a terrestrial lifestyle. Features present in unpublished fossil material referred to Mekosuchus inexpectatus (from late-Pleistocene New Caledonian) have been interpreted as adaptations to life on land (P. Willis, personal communication).

However, critical appraisal must await publication of a detailed analysis. Furthermore, at the very least, the presence of M. inexpectatus on an island 1477 km east of Brisbane might suggest that it, or its ancestral species, was more likely semi-aquatic. Although some terrestrial reptiles, varanids in particular, are strong swimmers, this represents an extraordinary distance even for island-hopping Varanus komodoensis. So, even if M. inexpectatus was shown to be terrestrial, there is good reason to believe that this may have been a local adaptation. A final point to be considered here concerns the small (<1 m) late Oligocene mekosuchine, Trilophosuchus rackhami. From the position of muscle insertion points in its skull, Willis (1993) determines that this species may have held its head above its body and that this might indicate a terrestrial habit, but, as noted above, this morphology is also present in the semi-aquatic Paleosuchus. Ouboter (1996) notes that this ability is typical of small or juvenile crocodylians in general and Salisbury (2001) concludes that all extant crocodylians are able to hold their heads above their bodies and parallel to the ground, except Gavialis gangeticus.

Taphonomic evidence for a terrestrial habitus in Quinkana fortirostrum is no more definitive. Molnar (1981) found that although some Q. fortirostrum had been found in cave

10

S. Wroe

deposits, including two associated with terrestrial faunas, most were unambiguously associated with aquatic tetrapods and all were found within 10 miles of a major watercourse. As noted by Molnar (1981) this neither supports nor refutes the hypothesis that this crocodylian was terrestrial, as semi-aquatic extant crocodylians are known to travel extensively overland on occasion. Additionally, populations of at least one living species are known to live in caves (Bohme and Koenig 2000). No other Australian crocodylian species for which a terrestrial lifestyle has been suggested are known from cave or fissurefill faunas (P. Willis, personal communication). Willis (1997) notes that a high degree of regional endemism among mekosuchine crocodylians of the late Oligocene–Miocene diminishes the argument that such species were terrestrial. Perhaps some mekosuchines spent more time on land than most living species, but certainly the balance of evidence suggests that these were still biologically dependent on major watercourses, at least with respect to reproduction and thermoregulation.

To conclude on the question of whether Quinkana fortirostrum or, for that matter, any other fossil Australian crocodylians were terrestrial, the term itself may be a misnomer.

Some semi-aquatic fossil taxa probably spent more time on land than do most living species, but this does not mean that they were terrestrial. However, it does mean that their ranges and distributions would have been limited when compared with those of terrestrial mammals.

Reptilian domination in the middle to late Tertiary?

Hecht’s (1975) assessment of the role of Megalania prisca along with interpretations of the ecology of Wonambi naracoortensis and Quinkana fortirostrum resulted in wide acceptance of reptilian domination in Pleistocene Australia (Archer and Bartholomai 1978; Molnar 1981). Flannery (1991, 1994) has contended that this phenomenon may have extended back to the early Miocene.

In the early 1990s there was little evidence to suggest the presence or absence of diverse guilds of either large reptilian or mammalian carnivores in pre-Pleistocene Australia. The

Table 1.

Large pre-Pleistocene reptile species of Australia for which a terrestrial habit has been proposed

Species

Family

Age

Baru darrowi Baru wickeni Baru huberi Quinkana babarra Quinkana fortirostrum Quinkana timara Quinkana meboldi Mekosuchus whitehunterensis Trilophosuchus rackhami Nanowana godthelpi Nanowana schrenki Wonambi naracoortensis Wonambi barriei

Crocodylidae Crocodylidae Crocodylidae Crocodylidae Crocodylidae Crocodylidae Crocodylidae Crocodylidae Crocodylidae Madtsoiidae Madtsoiidae Madtsoiidae Madtsoiidae

Yurlunggur camfieldensis Morelia riversleighensis

Madtsoiidae Pythonidae

mid Miocene late Oligocene late Oligocene Pliocene Pleistocene mid Miocene late Oligocene late Oligocene early Miocene early Miocene early Miocene Pleistocene late Oligocene, early Miocene mid Miocene late Oligocene

Estimated length ~4 m (Willis 1997) ~4 m (Willis 1997) <1.5 m (Willis, pers. comm.)

– 3 m (Flannery 1994) – <1.5 m (Willis, pers. comm.) <1 m (Willis 1997) <1 m (Willis 1993) <1.5 m (Scanlon 1997) <1.5 m (Scanlon 1997) ≤5 m (Scanlon 1997) <2.5 m (Scanlon and Lee 2000) – –

Ecology of Australian fossil carnivores

11

fossil record was largely silent on the issue. But, since 1989 at least 12 new species of mekosuchine crocodylian, madtsoiid and pythonid snake have been described from deposits ranging in age from the latest Oligocene to Pliocene (Table 1). Some have interpreted this as further evidence for reptilian dominance with respect to middle–late Tertiary terrestrial carnivore niches (Willis 1997; Scanlon and Mackness, in press). On the other hand, advances in the field of marsupial carnivore palaeontology have been construed

by Wroe (1999a, 2001, in press; Wroe et al., in press) as contra this assertion. Around 15 new species of marsupial carnivore from pre-Pliocene deposits have been added to the previously somewhat lacklustre tally (Table 2).

However, despite these finds, gaping holes in relevant data sets for both reptiles and mammals continue to impede the elucidation of terrestrial ecology in Tertiary Australia.

Table 2. Australian fossil carnivorous marsupial fossil species not represented in modern faunas Estimated average body weights for dasyuromorphians are from Wroe (2001) or as determined in Table 3, following the methodology of Myers (2001). Estimates for body weight in W. vanderleurei and T. carnifex from Wroe et al. (1999) Species

Family

Age

Estimated body weight (kg)

Barinya wangala Ganbulanyi djadjinguli Dasyurus dunmalli Glaucodon ballaratensis Sarcophilus moornaensis Sarcophilus laniarius Muribacinus gadiyuli Badjcinus turnbulli Wabulacinus ridei Thylacinus macknessi Thylacinus megiriani Thylacinus potens Ngamalacinus timmulvaneyi Nimbacinus dicksoni Nimbacinus richi Mutpuracinus archiboldi Tjarrpecinus rothi Maximucinus muirheadae Priscileo roskellyae Priscileo pitikantensis Wakaleo oldfieldi Wakaleo vanderleurei Wakaleo alcootaensis Thylacoleo hilli Thylacoleo crassidentatus Thylacoleo carnifex Ekaltadeta ima Ekaltadeta jamiemulvaneyi Jackmahoneyi toxoniensis Propleopus oscillans Propleopus wellingtonensis Propleopus chillagoensis

Dasyuridae Dasyuridae Dasyuridae Dasyuridae Dasyuridae Dasyuridae Thylacinidae Thylacinidae Thylacinidae Thylacinidae Thylacinidae Thylacinidae Thylacinidae Thylacinidae Thylacinidae Thylacinidae Thylacinidae Thylacinidae Thylacoleonidae Thylacoleonidae Thylacoleonidae Thylacoleonidae Thylacoleonidae Thylacoleonidae Thylacoleonidae Thylacoleonidae Hypsiprymnodontidae Hypsiprymnodontidae Hypsiprymnodontidae Hypsiprymnodontidae Hypsiprymnodontidae Hypsiprymnodontidae

early–mid Miocene mid–late Miocene Pliocene Pliocene Pliocene Pleistocene mid Miocene late Oligocene late Oligocene to early Miocene late Oligocene to early–late Miocene late Miocene late Miocene early Miocene late Oligocene to early–late Miocene mid Miocene mid Miocene late Miocene mid Miocene mid Miocene late Oligocene early Miocene to early–late Miocene mid Miocene to early–late Miocene late Miocene Pliocene Pliocene Pleistocene late Oligocene to mid Miocene early–late Miocene Pliocene Pleistocene Pleistocene Pliocene–Pleistocene

0.4 3.6 1.7 7.5 9.1 23.6 1.6 2.4 5.3 9.2 57.3 38.7 5.7 5.0 4.9 1.1 5.4 18.4 – – – 44–56 – – – 101–130 – – – – – –

12

S. Wroe

Assertions that any of the eight, pre-Pleistocene mekosuchine crocodylians were terrestrial remain speculative in the absence of supportive postcranial and taphonomic data. As already noted, no pre-Pleistocene crocodylians have been described from cave or fissurefill deposits. Similarly, the palaeoecology of each of the four new madtsoiid snake species remains conjectural.

Again, especially with respect to reptiles, information on size has generally been either restricted to estimates of maximum dimensions, limited to educated guesswork, or some combination of the latter two. Flannery (1991, 1994) treats mammalian carnivores as big as, or bigger than, the living dasyurid Dasyurus maculatus as large. Large males of this species can exceed 5 kg in body mass, but the average is closer to 2.5 kg (Wroe, in press).

For reptiles, this would probably exclude at least the two Tertiary crocodylians under 1 m and two snakes under 1.5 m, leaving a total of nine species (Table 1). At around 4 m, the largest of Tertiary reptiles for which a terrestrial lifestyle seems possible was Baru darrowi.

But Willis (1997) describes this species as semi-aquatic. The only published estimates currently available for any other pre-Pleistocene crocodylians are estimates of less than 1 m for Mekosuchus whitehunterensis and Trilophosuchus rackhami (Willis 1997). But of the nine remaining, all are much smaller than B. darrowi excepting B. wickeni (P. Willis, personal communication).

For marsupial carnivores, Wroe (2001) gives body mass estimates for the 12 prePleistocene thylacinids described to date, largely on the basis of equations derived by Myers (2001). Using the same methodology, estimates for a number of other fossil dasyuromorphian taxa are given in Table 3. The largest pre-Pleistocene marsupial carnivores for which estimates based on quantitative methodology are known are the thylacoleonid Wakaleo vanderleurei at 44–56 kg (Wroe et al. 1999) and the thylacinids Thylacinus megiriani and T. potens, considered to have weighed about 57 and 39 kg respectively by Wroe (2001). At least two other pre-Pleistocene marsupial lions are larger than W. vanderleurei on the basis of dental dimensions: Wakaleo alcootaensis and Thylacoleo crassidentatus (Clemens and Plane 1974; Archer and Dawson 1982). Of the 12 Tertiary thylacinids, nine are at least twice the size of D. maculatus (Wroe 2001). For marsupial carnivores, using the criterion of Flannery (1991), at least four species among the 27 pre-Pleistocene taxa featured in Table 3 would be excluded, but there can be little doubt that all thylacoleonids and propleopine kangaroos weighed 2.5 kg or more on average.

To date, the number of described late Oligocene–Pliocene terrestrial reptilian predator species exceeding approximately 2.5 kg in average body mass ranges between one and nine,

Table 3.

Body weight estimates for six fossil marsupial carnivore taxa based on methodology of Myers (2001) Length is in millimetres. Weight is in grams

Species Barinya wangala Ganbulanyi dadjinguli Glaucodon ballaratensis Sarcophilus laniarius Sarcophilus moornaensis Dasyurus dunmalli

Specimen no. Variable Dimension QM F31408 QM F24537 P16136 M1261–64 NMV P28268 QM F739

UMRL 1UML LMRL LMRL LMRL LMRL

12.7 6.7 34.6 49.4 36.7 21.7

Source

Body Percentage weight error

Wroe 1999c 429.1 Wroe 1998 3645.0 Stirton 1957 7528.9 Stirton 1957 23605.2 Crabb 1982 9096.0 Bartholomai 1971 1684.8

14 22 13 13 13 13

Ecology of Australian fossil carnivores

13

depending on which, if any, mekosuchine crocodylians and madtsoiid snakes were terrestrial. With respect to marsupials the count is 23. Relevant Oligocene–Pliocene material that is undescribed or not allocated to a species includes Megalania sp. (significantly smaller than M. prisca), a python (Scanlon and Mackness, in press), at least two thylacoleonids (A. Gillespie, personal communication) and two dasyuromorphians.

Broader ramifications: factors that influence maximum body mass and species richness While I have argued that the case for reptilian domination of large terrestrial carnivore niches among fossil faunas in Australia is weak or groundless on the basis of respective sizes, abundance and ecomorphology, other related contentions appear to be on firmer footing. Relative to other continents, Australia has been depicted as having both low species richness and small maximum body mass for large mammalian carnivores (Lee and Cockburn 1985; Flannery 1994; Diamond 1998).

Milewski (1981) posited that low soil-nutrient levels, characteristic of arid and semi-arid Australia, resulted in relatively low productivity that favoured reptiles over endotherms. In 1985, Lee and Cockburn stressed the importance of erratic climate as a constraint on productivity that similarly limited the evolution of large endothermic meat-eaters. Morton and James (1988) considered that both erratic climate and infertile soils had facilitated the invasion of mammalian niches by reptiles, including carnivorous ones in inland Australia.

Most recently, Flannery (1991, 1994) translated this theme to the Pleistocene fossil record, stressing the role of intense variability in the El Niño Southern Oscillation (ENSO) and soil-nutrient deficiency in particular. He further speculated that this regime might have extended back to early Miocene times.

Crucial to these interpretations is the acceptance of the primacy of productivity as an influence on mammalian species richness and body mass, as well as a simple and positive relationship between these variables. Also implicit is a simple relationship between productivity and energy transfer between plants and animals.

Productivity and maximum body mass Maximum body mass in animals is often linked to the productivity of the environments they inhabit. The work of Burness et al. (2001) is particularly relevant on this issue. These authors compared the sizes and consumption of the largest mammalian carnivores, herbivores and selected reptiles against landmass area. All continents and various islands were included. They found a general correspondence between maximum body mass and landmass area, but concluded that in the late Pleistocene, Australia’s largest endemic mammalian carnivores and herbivores were too small to be explained by this factor alone and low productivity was invoked as a sister constraint.

If the estimates given in Wroe et al. (1999) and the present paper are considered, then the conclusion of Burness et al. (2001) regarding the size of Australia’s largest mammalian carnivores is undermined and the mean body mass of its largest mammalian predator may be entirely consistent with landmass area. Moreover, for Diprotodon optatum, Australia’s biggest mammalian herbivore, the estimate of Burness et al. for mean body mass of 1175 kg was evidently derived on the basis of educated guesswork. This applies to many other fossil taxa included in their study. Wroe et al. (in press) recently estimated the body mass of the only available specimen of D. optatum currently held at the Australian Museum using the methodology of Anderson et al. (1985) and obtained a figure of over 2.7 tonnes. This

14

S. Wroe

may represent exceptionally large or small D. optatum, but it is more likely to approximate the average (Berger 2000). If this is so, then the size of Australia’s largest mammalian herbivore conforms with that expected on the basis of continental area alone (G. Burness, personal communication) and special pleading in the guise of alleged low productivity is unnecessary.

Burness et al. (2001) rightly observe that ultimately it is not maximum body mass, but mean consumption rates that constitute a real basis for ecological comparisons among carnivores. On the basis of methodology supplied by Nagy (2001), Burness et al. (2001) predicted food consumption for a 380-kg Megalania prisca and a 73-kg Thylacoleo carnifex and concluded that they were comparable. Substituting figures for mean body masses provided in the present article would profoundly affect this result. But there are other reasons for skepticism. As observed by Nagy (2001), his own equations are unreliable predictors where the taxa involved are larger than the largest specimens used in their derivation. Underwood (1997) treats extrapolation beyond the data range as a fundamental error with respect to such predictions. Reliability further diminishes with increasing phylogenetic distance and difference in lifestyle and habitat.

Phylogenetic and behavioural differences between Megalania prisca and the largest reptile (Varanus komodoensis) included by Nagy (2001) may not have been great, but around eight-fold extrapolation is required. Whether this might produce over- or underestimates is uncertain, but, in one aspect, underestimation seems probable. Nagy incorporated few varanids, but these lizards have relatively high metabolic rates (King and Green 1999). However, extrapolation far beyond the data range is perhaps the most serious problem and it detracts from the validity of most conclusions drawn by Burness et al.

(2001).

The suggestion by Burness et al. (2001) that differences in area alone do not account for the lesser maximum size of Australia’s largest marsupial carnivore and herbivore relative to those of other continents is also based on low predicted consumption for Australian marsupials relative to placentals elsewhere. To estimate feeding requirements in Thylacoleo carnifex, Burness et al. (2001) apply Nagy’s (2001) equation derived using metabolic rates for marsupials, the largest of which was a 44.5-kg grazing kangaroo (Macropus giganteus).

Again, the value of this equation is debatable with respect to elucidating consumption in a fossil species that so greatly exceeds the original data set. This is particularly so given that the largest marsupial carnivore incorporated by Nagy (2001) was a 63-g marsupial mouse (Antechinus swainsonii). As a more extreme example, the largest herbivore used to derive Nagy’s (2001) equation for estimating food intake in placentals was a 43-kg springbock (Antidorcus marsupialias). This was used by Burness et al. (2001) to estimate the food requirements of a 6000-kg Columbian mammoth (Mammuthus columbi).

Lastly, pinnipeds constituted over 10% of the species used by Nagy (2001) to develop his general equation for the prediction of consumption in placentals. However, Williams et al. (2001) demonstrate that marine mammals have a basal metabolic rate up to 2.3 times that of similar-sized terrestrial placentals. With this in mind, Nagy’s (2001) equation may greatly overestimate consumption in land-living placentals and produce an exaggerated differential between these and the exclusively terrestrial marsupial taxa.

Productivity and species richness among carnivorous mammals At most, seven carnivorous marsupial species the size of Dasyurus maculatus or larger (including D. maculatus and Sarcophilus harrisii) are known from Australia’s Pleistocene faunas (Table 3). Such species richness (number of species) is certainly poor if compared

Ecology of Australian fossil carnivores

15

with arbitrarily defined, similar-sized areas within â&#x20AC;&#x2DC;Ice Ageâ&#x20AC;&#x2122; North America or present-day east Africa.

As mentioned above, fundamental to explanations for perceived low species richness among mammalian carnivores in Australia is an assumed simple and positive relationship between productivity, species richness and species abundance (number of individuals). This assumption is not necessarily safe. The relationship may be complex and can be positive, negative or unimodal (Ritchie and Olff 1999; Kondoh 2000). The reasons for this are not well understood, although a contributing factor is likely to be variable energy transfer between plants and animals in different biomes. Inefficient energy transfer often occurs in areas of high productivity because primary production is locked into inaccessible woody plants (Glazier 1991). Janis et al. (in press) observe that in savannah ungulate faunas, species richness increases with rainfall to around 800 mm per annum, but then levels off.

This suggests that productivity may be limiting species richness in much of present-day Australia, but this does not apply throughout the entire Pleistocene and in Miocene times very extensive tracts of Australia received far more rain than today (Archer et al. 1998).

Further complicating the issue is the fact that other variables, such as soil-nutrient levels, are not necessarily critical to productivity (Jordan and Herrara 1981).

From what we do know of marsupial carnivore palaeontology in Miocene Australia, the data are contradictory. On the one hand, species richness is higher and consistent with the proposition that productivity affects diversity; on the other, maximum body masses were less, eating into the proposition that productivity is primary with respect to this factor.

Factors other than productivity influencing body mass and species richness Productivity is undoubtedly a significant factor with respect to both body mass and species richness. The island continent is certainly dry, and wild fluctuations in the ENSO index certainly place stresses on its biota and large tracts of inland Australian, especially, are characterised by poor soils. However, the continent has not always been dry, there is no evidence for ENSO prior to around 40 000 years ago (Kershaw et al. 2000), and we know next to nothing about Australiaâ&#x20AC;&#x2122;s palaeo-soils. In addition to grounds for skepticism already discussed, this gives reason to believe that the role of productivity has been overestimated.

Many other factors affect species richness and body mass and these need to be considered in more detail.

Basic principles of island biogeography predict that an island biota will support fewer species than that of an area of identical size within a larger continental mass because of increased extinction and decreased immigration rates (MacArthur and Wilson 1967; Ternborgh et al. 2001; Whittaker et al. 2001). Thus, it is inappropriate to directly compare species richness for any Australian taxon with arbitrarily defined areas within other continents. Both the distance from the nearest continental landmass and temporal isolation are critical factors. The shape of a landmass may also be significant (Williams 1997).

Australia is by far the smallest continent and, excepting Antarctica, it is the only one that has remained isolated through to the present day. The full extent of this disconnection remains debatable, but it may include the entire Cainozoic (Godthelp et al. 1999), making Australia easily the most isolated continent regarding both distance from other continental landmasses as well as temporal separation (again excepting Antarctica). As observed above, related biogeographical phenomena include the demonstration that maximum mammalian body size and continental area are positively correlated (Marquet and Taper 1998; Burness et al. 2001). Another is that the maximum size of mammalian taxa tends to increase over time, at least with respect to genera (Alroy 1998). Climatic stability over

16

S. Wroe

geologically significant periods and its effect on habitable area, as well as equatorial and latitudinal exposure, are other relevant factors (Berger 2000). Large size in many taxa may be an adaptation to low-productivity environments (Owen-Smith 1988) and increased aridity (Wheeler 1992).

One influence that is very interesting, but difficult to test, is the role of historical constraint. It has been argued that this latter factor can be discounted because in South America borhyaenoid marsupials also dominated terrestrial carnivore niches and achieved greater species richness (Flannery 1994). Complicating any comparison is the role of predatory phorusrhacoid, or â&#x20AC;&#x2DC;Terror Birdsâ&#x20AC;&#x2122;, which became increasingly significant in late Tertiary South America (Marshall 1994). However, in addition to great differences in habitable area, equatorial exposure, geographic relief and latitudinal spread, sampling disparity means that the comparison with Australia was never fair. From results presented

by Cione and Tonni (1995) and Savage and Russell (1983), there are about three times as many mammal-bearing deposits of Miocene age known from South America as from Australia. The discrepancy is greater still with respect to older faunas. Similarly, the contention that low productivity might explain the lack of large mammals in New Guinea (Burness et al. 2001) overlooks the fact that very few fossil sites are known from this island and that most of these are at high altitude. The largest mammals are not typically present at elevation.

When this constellation of mitigating factors are considered, it is reasonable to posit that, productivity aside, we would not expect fossil marsupials to have been as diverse in Australia as in South America. Nonetheless, advances in Australian palaeontology now place the comparison on a more equal footing. At present, about 16 Australian marsupial carnivores of Miocene age are estimated at a mean body mass of about 2.5 kg and over. The total count for Miocene Borhyaenoidea of all sizes is approximately 30 (C. Muizon, personal communication) and it is likely that some of these would have weighed less than 2.5 kg (although this must be balanced against the existence of a number of didelphoids that may have exceeded this mark). In addition, while it is true that some borhyaenoids were larger than the heaviest of Australiaâ&#x20AC;&#x2122;s known marsupial carnivores, the largest were restricted to Oligocene deposits (Marshall 1978; Cione and Tonni 1995). Among marsupials of late Tertiary South America, the closest ecomorphological equivalent of Thylacoleo carnifex was the marsupial sabre-tooth Thylacosmilus atrox. Using the methodology of Anyonge (1993), Wroe et al. (1999) predict that the largest known individual T. atrox was about 116 kg. Applying the same technique, the largest Thylacoleo carnifex weighed over 160 kg.

Also to be considered is the possibility that historical constraint may have imposed limitations on the maximum size and species richness of marsupial herbivores in Australia.

For example, the heaviest of megaherbivores are characterised by highly specialised, loadbearing feet (Owen-Smith 1988), a feature that might have been limited by the marsupial mode of reproduction. Maximum prey size is certainly one factor influencing the maximum body mass of predators. In South America herbivore niches were occupied by placentals.

Other indirect influences on marsupial carnivore diversity include characteristics unique to the Australian flora. Fluoroacetatate (1080) is a toxic compound used in many countries to control vertebrate pests. It naturally occurs in three African and one South American plant species. In Australia, 35 widely distributed taxa produce 1080 and native species display variable tolerance (Twigg and King 1991). The effects of this poison on the evolution of mammalian herbivores in Australia have not been the subject of major investigation, but Twigg and King (1991) argue that, where present, it produces a regime

Ecology of Australian fossil carnivores

17

that advantages reptiles over mammals and birds. Similarly, the highly successful species of Eucalyptus also contain toxins and this has undoubtedly constrained the evolution of marsupial herbivores on the continent to some degree (Hume 1999).

Our limited understanding of palaeo-ecomorphology continues to hamper comparisons between Australia’s mammalian carnivore faunas and those of other continents. However, while additional work is needed, it is probable that most larger taxa were hypercarnivorous (sensu Van Valkenburgh 1989). Of the four higher taxa to be considered, only propleopine kangaroos were clearly omnivorous (Ride et al. 1997; Wroe et al. 1998). However, the species richness of mammalian carnivores in Australia has typically been contrasted with that of all Carnivora (e.g. Flannery 1994), an order in which many, if not most, are generalist feeders. In a study of 89 carnivorans with an average body mass of 2.5 kg or more, Gittleman (1985) lists only 26 as species in which flesh constituted 60% or more of the diet. The rest were classified as omnivores, frugivores/herbivores and insectivores. Four were piscivores. In this context a far more pertinent question with respect to mammalian ecology in Australia than ‘why so few large carnivores?’ is ‘why so few large omnivores, frugivores and herbivores?’. To be contemplated in response is the role of large terrestrial birds. At least eight dromornithid and four casuariid species have existed in Australia since the late Oligocene (W. Boles, personal communication). These range in size from about 20 to 500 kg (Boles 1997; Wroe 1999b). Extant casuariids are omnivores and it is reasonable to speculate that this was also true of fossil species. With respect to dromornithids, an omnivore–scavenger role has been suggested for at least one species (Rich 1981) and Wroe (1999b) posits that some may have been significantly carnivorous.

The higher extinction rates to be expected on the smallest, driest and most isolated inhabited continent may have reduced the available time required for the evolution of larger species. A lack of land bridges with other continents means that immigrants could not replace large taxa extinguished by local events, as was often possible on other continents.

Novacek (1999) observes that it took millions of years for large herbivorous mammals to evolve following the extinction of non-avian dinosaurs. Studies such as that of Marquet and Taper (1998) have demonstrated the relationship between area and maximum body size; a further complicating factor is that the already greater area of other continents relative to Australia understates the real discrepancy (Wroe et al., in press). To varying degrees, all other inhabited continents have been contiguous with neighbours at times during the Cainozoic. During the Pleistocene they have occasionally formed a single landmass. Given that area is of demonstrable significance, this must be considered, as must the fact that wildly fluctuating climate in Australia has, at times, massively restricted available habitats to a degree exceeding that of at least some, if not all, other landmasses (Martin 1998; Wroe et al., in press).

Among continents, another uniquely Australian factor that may have constrained the species richness of mammalian carnivores, as well as of other terrestrial taxa, is a lack of geographical barriers. Obstacles to immigration and migration, such as mountain ranges and rivers, are fundamental to allopatric speciation models. As both the flattest and driest inhabited continent, Australia offers little in the way of such impediments.

An interesting hypothetical to ponder is whether Australia would have supported the largest of Asian mammals had Australia not remained geographically isolated? I would argue yes, although such taxa may have become smaller or even extinct during times of reduced habitable area. Isolation and taxonomic composition are likely to be of particular importance with respect to Australian biogeography. Consideration of the Pleistocene fossil

18

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record of Flores may shed some light. Three fossil elephants are the largest known taxa on this relatively small Indonesian island, two dwarf and one large species of Stegodon. Yet the largest carnivore was the Komodo dragon (Morwood et al. 1999; Morwood 2001). Both elephants and Varanus komodoensis are superior swimmers over distance. Although area is likely a significant factor with respect to such biological phenomena, it is difficult to dismiss the role of historical accident as an explanation for both maximal body mass and the relative significance of reptiles and mammals in this instance. The absence of tigers (Panthera tigris), historically found on many smaller Indonesian islands, is most easily explained on the basis of sweepstakes dispersal and the fact that V. komodoensis is a better swimmer (Sondaar et al. 1994).

Conclusions The contention that reptiles dominated Australiaâ&#x20AC;&#x2122;s large terrestrial carnivore niches since the early Miocene is brought into question. With respect to Pleistocene faunas, the ecology of the three Australian ectotherms traditionally invoked to sustain proposed reptilian supremacy is poorly understood. The degrees to which the crocodylian Quinkana fortirostrum and particularly the varanid Megalania prisca were actively predaceous are unknown. Regarding the giant snake Wonambi naracoortensis, evidence to hand suggests that it was weak-jawed, its numerous but small teeth were ill suited to the role of securing large prey, it lacked postcranial features common to constrictors, and it was unable to fully disarticulate its jaws. It has also yet to be established that these three reptiles were terrestrial.

Only estimates of maximum size are provided in the literature for two of these reptiles and only for one of these, Megalania prisca, has any estimate been provided using quantitative methodology. Some predictions for M. prisca may be exaggerated by more than an order of magnitude. But, even if we were to accept these estimates, it is clear that for taxa of indeterminate growth in particular, maximum dimensions are likely to represent gross deviations from the mean and do not provide reasonable grounds for predicting ecology.

Regardless of oneâ&#x20AC;&#x2122;s position with respect to the identity and expression of constraints on the species richness and body mass of mammalian carnivores, ecology and impact cannot be assessed on the basis of maximum body mass or species richness alone: many factors determine the significance of predators within an ecosystem, including total consumption of meat, mean body mass, geographic range, range of prey species, abundance and metabolism.

In the Australian Pleistocene, species richness of marsupial carnivores was relatively low. However, the four hypercarnivorous taxa (Thylacoleo, Thylacinus, Sarcophilus, Dasyurus) were undoubtedly terrestrial, prey ranged up to juvenile diprotodontid size, distributions were continent-wide across many habitats and all were relatively common (Archer and Dawson 1982; Dawson 1982; Paddle 2000).

Australiaâ&#x20AC;&#x2122;s large Pleistocene reptiles met few, if any, of these criteria. With respect to geographic range, in particular, reptiles are generally much more restricted with respect to both latitude and altitude than mammals, the very largest are concentrated heavily within tropical and subtropical habitats, and it is unlikely that reptiles ever had truly continentwide distributions within Australia.

Regarding late Oligocene to Pliocene Australia, the case for reptilian domination is weaker still. Size estimates are lacking for many species but, again, regarding reptilian taxa, where available these are typically maxima only. Many, perhaps most, of the known reptiles were small. In the absence of postcranial material, all arguments pertaining to whether pre-

Ecology of Australian fossil carnivores

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Pleistocene Australian crocodylians were terrestrial remain highly speculative and, while taphonomic data is inconclusive, it does suggest high levels of local endemism and counts against the proposition that any of these Tertiary crocodylians were competent overland dispersers. Similarly, the habits of Australia’s three Tertiary madtsoiid snakes are poorly understood, while the largest was around one-eighth the size of Wonambi naracoortensis (Scanlon and Lee 2000). On the other hand, known species richness of large marsupial carnivores in the middle–late Tertiary of Australia has greatly increased over recent decades.

The complexities and mixed signals evidenced by the mammalian carnivore fossil record in Australia lead to broader biogeographical conundrums. Although assertions of unexpectedly low species richness, mean body mass, or consumption, are often either greatly overstated or wrong, in some instances there is substance, e.g. low species richness during the Pleistocene. Traditionally, low productivity has been flagged as the primary influence on diversity. However, it has already been demonstrated that these do not necessarily form a simple and positive relationship and mono-factorial models do not fully account for these variables in any community. Because it is singular in so many respects, Australia may provide an important testing ground.

A simple, universal, paradigm linking species richness, mean body mass and productivity cannot be applied to Australia. For example, Australia’s largest marsupial carnivores are found in Pleistocene faunas; yet, overall, this was a period of low productivity. Low species richness and low productivity in Pleistocene Australia are consistent with a simple relationship, but then it is also consistent with constraint by many other factors. These include the relatively small size of the continent, extreme geographic and temporal isolation, phylogenetic constraint, a lack of internal geographic barriers and competition with large terrestrial birds. The relative significance of each of these requires more detailed investigation before the role of productivity or any other factor can be identified as primary.

Acknowledgments For their help in providing constructive criticism, comment and discussion, I am very much indebted to M. Archer, G. Burness, C. Dickman, M. Crowther, T. Flannery, A. Gillespie, C. Janis, R. Molnar, M. Morwood, A. Musser, T. Myers, S. Salisbury, J. Scanlon, R. Shine, C. Stevenson, M. Thompson, P. Willis and an anonymous reviewer. Funding has been provided to S. Wroe through grants from the following institutions: University of Sydney (U2000 Postdoctoral Research Fellowship), French Ministry of Foreign Affairs, Linnean Society of New South Wales, Australian Geographic Society, Institute of Wildlife Research, and the University of New South Wales. Support has also been given by the Australian Research Council (to M. Archer); the National Estate Grants Scheme (Queensland) (grants to M. Archer and A. Bartholomai); the Department of Environment, Sports and Territories; the Queensland National Parks and Wildlife Service; the Commonwealth World Heritage Unit (Canberra); ICI Australia Pty Ltd; the Queensland Museum; the Australian Museum; Century Zinc Pty Ltd; Mt Isa Mines Pty Ltd; Surrey Beatty and Sons Pty Ltd; the Riversleigh Society Inc.; the Royal Zoological Society of New South Wales and many private supporters.

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Manuscript received 15 August 2001; accepted 4 February 2002

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