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Proc Natl Acad Sci U S A. 2001 December 4; 98(25): 14518–14523. Published online 2001 November 27. doi: 10.1073/pnas.251548698. | PMCID: PMC64714 |
Copyright © 2001, The National Academy of Sciences Evolution Dinosaurs, dragons, and dwarfs: The evolution of maximal
body size Gary P. Burness,*† Jared Diamond,*‡ and Timothy Flannery§ *Department of Physiology, University of California School of Medicine, Los Angeles, CA 90095-1751; and §South Australian Museum, North Terrace, Adelaide 5000, SA, Australia Accepted October 15, 2001. Among local faunas, the maximum body size and taxonomic affiliation
of the top terrestrial vertebrate vary greatly. Does this variation
reflect how food requirements differ between trophic levels (herbivores
vs. carnivores) and with taxonomic affiliation (mammals and birds vs.
reptiles)? We gathered data on the body size and food
requirements of the top terrestrial herbivores and carnivores, over the
past 65,000 years, from oceanic islands and continents. The body mass
of the top species was found to increase with increasing land area,
with a slope similar to that of the relation between body mass and home
range area, suggesting that maximum body size is determined by the
number of home ranges that can fit into a given land area. For a given
land area, the body size of the top species decreased in the sequence:
ectothermic herbivore > endothermic herbivore > ectothermic
carnivore > endothermic carnivore. When we converted body mass to
food requirements, the food consumption of a top herbivore was about 8
times that of a top carnivore, in accord with the factor expected from
the trophic pyramid. Although top ectotherms were heavier than top
endotherms at a given trophic level, lower metabolic rates per gram of
body mass in ectotherms resulted in endotherms and ectotherms having
the same food consumption. These patterns explain the size of the
largest-ever extinct mammal, but the size of the largest dinosaurs
exceeds that predicted from land areas and remains unexplained. The size and taxonomic
affiliation of the largest locally present species (“top
species”) of terrestrial vertebrate vary greatly among faunas,
raising many unsolved questions. Why are the top species on continents
bigger than those on even the largest islands, bigger in turn
than those on small islands? Why are the top mammals
marsupials on Australia but placentals on the other continents? Why is
the world's largest extant lizard (the Komodo dragon) native to a
modest-sized Indonesian island, of all unlikely places? Why is the top
herbivore larger than the top carnivore at most sites? Why were the
largest dinosaurs bigger than any modern terrestrial species? A useful starting point is the observation of Marquet and Taper ( 1),
based on three data sets (Great Basin mountaintops, Sea of Cortez
islands, and the continents), that the size of a landmass's top mammal
increases with the landmass's area. To explain this pattern, they
noted that populations numbering less than some minimum number of
individuals are at high risk of extinction, but larger individuals
require more food and hence larger home ranges, thus only large
landmasses can support at least the necessary minimum number of
individuals of larger-bodied species. If this reasoning were correct,
one might expect body size of the top species also to depend on other
correlates of food requirements and population densities, such as
trophic level and metabolic rate. Hence we assembled a data set
consisting of the top terrestrial herbivores and carnivores on 25
oceanic islands and the 5 continents to test 3 quantitative
predictions. | | 1. | Within a trophic level, body mass of the top species will
increase with land area, with a slope predictable from the slope of the
relation between body mass and home range area. | | | 2. | For a given land area, the top herbivore will be larger than
the top carnivore by a factor predictable from the greater amounts of
food available to herbivores than to carnivores. | | | 3. | Within a trophic level and for a given area of landmass, top
species that are ectotherms will be larger than ones that are
endotherms, by a factor predictable from ectotherms' lower food
requirements. |
On reflection, one can think of other factors likely to perturb
these predictions, such as environmental productivity, over-water
dispersal, evolutionary times required for body size changes, and
changing landmass area with geological time. Indeed, our database does
suggest effects of these other factors. We propose our three
predictions not because we expect them always to be correct, but
because we expect them to describe broad patterns that must be
understood in order to be able to detect and interpret deviations from
those patterns. For continents and oceanic islands with a good fossil record for
the last 65,000 years, Table 1 lists the
identity and mean adult body mass of the top herbivore and top
carnivore, most of them known only as Late Pleistocene or Holocene
fossils. We chose a cutoff of 65,000 years ago because that is the
approximate time of emergence of behaviorally modern humans ( 2), who
may have been responsible for the subsequent extinctions of most of
these top species.
| Table 1Top herbivores and top carnivores for various land masses
in the Late Pleistocene
or Holocene |
We used mean adult mass of each species rather than mass of the largest
known individual. In studies providing only a range of masses, we
averaged the range. To generate a species mean, we averaged male and
female body masses. When calculating the mean mass of extant reptiles,
we included only mass estimates for individuals of breeding age
and/or size. When no body mass values were available (e.g., for many
extinct species), we estimated body mass from linear dimensions through
comparisons with related extant species of known body mass, using
regression equations (refs. 3 and 4; P. Christiansen, personal
communication), or else assuming body mass to increase as the
cube of linear dimensions. In some cases, a top species occurred on multiple islands within an
archipelago but was unlikely to disperse often among islands, hence
each island must have had a nearly self-sustaining population. We
report such a species only once, using the area of the largest island
on which it was the top herbivore or carnivore. Because some avian
carnivores (e.g., sea eagles Haliaeetus sp.) readily cross
water gaps, we excluded them if they occurred on islands less than an
arbitrarily defined 50 km from a larger landmass. We included terrestrial and freshwater crocodiles known or suspected to
prey on terrestrial vertebrates. We excluded salt-water and estuarine
crocodilians, able to disperse among islands [e.g., Crocodylus
porosus and Crocodylus aculatus ( 5)]. In gathering
data on carnivores, we excluded omnivorous species (e.g., Brown bear
Ursus arctos). Because this article is concerned with resource consumption, we define
the top herbivore or carnivore at each location as that species with
the greatest food consumption, rather than greatest body mass. Given
the 10-fold higher food consumption per gram of body mass for
endotherms than for
ectotherms, ¶ an endotherm
has the same food consumption as an ectotherm 10 times heavier. We used
the taxon-specific equations of Nagy ¶ (his equations 3, 5,
35, and 67) to calculate food consumption rates (grams of dry
matter per day) from adult body masses. Table 1 gives modern Holocene land areas. Because of Pleistocene
lowered sea levels and resulting emergent continental shelves, most
landmasses had Pleistocene areas somewhat greater than their modern
areas. Only for the island of New Providence was the Pleistocene
increase sufficiently large to influence our results, as we shall
discuss. We excluded islands connected to nearby continents by Late
Pleistocene land bridges, except that we included New Guinea, because
it was a rainforest island connected to arid Australia. New Guinea's
high percentage of endemic species suggests only limited faunal
exchange with Australia. The Main Patterns. The body masses (in kg) of endothermic top herbivores (18 mammals, 9
birds), endothermic top carnivores (11 mammals, 14 birds), and
ectothermic top carnivores (4 crocodilians, 2 lizards) all increased
with increasing land area (in km2) according to
the respective equations: Mass = 0.47
Area0.52 (r2 = 0.61,
P < 0.0001); Mass = 0.05 Area0.47
(r2 = 0.81, P < 0.0001);
and Mass = 0.25 Area0.47
(r2 = 0.78, P = 0.020)
(Fig. A).
The slopes of these three equations are statistically the same
(P > 0.60) but their intercepts are different
(P < 0.005), except that the difference between the
intercepts of the first and third equations falls short of significance
(P = 0.099). Our data set includes only three
ectothermic top herbivores (two tortoises and one lizard), too few to
calculate a regression equation, but on the average 16 times larger
than predicted from the equation for endothermic top herbivores. Thus,
for a given land area, the body size of top species decreased in the
sequence: ectothermic herbivore > endothermic herbivore >
ectothermic carnivore > endothermic carnivore. When we made comparisons between trophic groups (Fig.
A), for a given land area a top herbivore proved to
be 14 times heavier than a top carnivore in the case of endotherms
(ANCOVA, F1,49 = 49.3,
P < 0.0001) and 33-fold heavier in the case of
ectotherms. For example, as is well known, African elephants are much
larger than African lions. When we converted our body mass estimates to food consumed per day
(Fig. B), the food consumption of a top herbivore was
7-fold greater than that of a top carnivore in the case of endotherms
(ANCOVA F1,49 = 42.2,
P < 0.0001) and 24-fold greater in ectotherms
(comparing our three herbivores with the regression line for
ectothermic carnivores). The greater food consumption of herbivores
than of carnivores is as expected, because in trophic pyramids the
energy available to herbivores exceeds that available to carnivores by
a factor variously between 5 and 20 (23). For a given land area, an ectothermic top carnivore was 5 times heavier
than an endothermic top carnivore (ANCOVA,
F1,28 = 12.9, P =
0.0012; see Fig. A), and an ectothermic top
herbivore was 16 times heavier than an endothermic top herbivore.
However, because ectotherms have lower mass-specific metabolic rates
and hence food requirements than endotherms, the food requirements of
ectothermic and endothermic top carnivores for a given land area proved
to be the same (P = 0.17; see Fig. B).
Similarly, for a given land area, the food consumption of our three
ectothermic top herbivores was similar to that of endothermic top
herbivores, falling within the 95% confidence intervals surrounding
the endotherm regression line (Fig. B). Significance of the Slopes and Intercepts. The main patterns of Fig. A and B agree
qualitatively with predictions based on food requirements of individual
animals and on minimum viable population sizes. A quantitative
comparison is possible as follows. Individual larger animals require more food than do smaller animals,
hence they require a larger home range to supply that food. We compared
our regression equations with one that relates mammalian home range
area with body mass ( 24). To allow for comparison with our Fig.
A, data from ref. 24 were replotted (D. Kelt,
personal communication) with body mass as the dependent variable and
home range area as the independent variable, omitting species with body
masses <0.1 kg because at that body mass many biological
characteristics appear to change sign ( 24). The resulting equation was
Mass = 673 Area 0.50
( r2 = 0.61, n = 232,
P < 0.0001; D. Kelt, personal communication). Its
slope (0.50) is almost identical to the slopes (0.47–0.52) of our
equations of body mass of top species vs. land area. Larger home ranges translate into lower population densities, hence
lower population sizes (number of individuals constituting a
population) for a given area. But some minimum population size is
necessary for a population's long-term survival in evolutionary time
(frequent estimates are a few thousand to at least 10,000 individuals;
ref. 25). Hence, larger-bodied animals with larger home ranges require
a larger landmass to achieve that required minimum population size.
Because the trophic pyramid implies 5–20 times more food available to
herbivores than to carnivores, a given area can support a population of
a herbivore species whose individuals consume 5–20 times more than
does a carnivore; we actually found a ratio of 8 for the median food
consumption of top herbivores to top carnivores (Table 1). Because the
high metabolic rates of endotherms result in their having food
requirements equal to those of an ectotherm 10-fold
heavier, ¶ a given area can support a population of an
ectotherm 10-fold heavier than an endotherm at the same trophic level;
we actually found ratios of 5 for carnivores and 16 for herbivores. The low metabolic rates of ectotherms probably explain why ectotherms
are top carnivores on at least five islands whose herbivores are
nevertheless endotherms (Viti Levu, Flores, New Caledonia, Sulawesi,
and Madagascar). The most famous example is the world's largest extant
lizard, the Komodo dragon of Flores (adult body mass averaging 70 kg).
Flores formerly supported as its top herbivore a small elephant-like
stegodont (not listed in Table 1 because of uncertainty whether it
survived after 65,000 years ago). Fig. A shows
Flores' area to be capable of supporting an endothermic top carnivore
of only about 5 kg, no match for a stegodont. Instead, Flores supports
the Komodo dragon, which today attacks feral horses and buffalo, and
thus could have attacked a small stegodont. Despite its large size, the
Komodo dragon has been able to maintain a viable population on Flores
because of its low metabolic rate. Because more energy is available at
lower trophic levels, Flores (and other islands with ectothermic top
carnivores) can support large endothermic herbivores on which those
carnivores prey. The same islands could not have supported endothermic
top carnivores large enough to prey on those herbivores. For example,
on Crete and Cyprus, the top carnivores are small endotherms, an 11-kg
otter and a 2-kg genet, utterly incapable of preying on the top
herbivores of these islands (a 3,200-kg elephant and a 200-kg
hippopotamus, respectively). Effect of Environmental Productivity. Although the world's largest extant lizard is the Komodo dragon,
Australia formerly supported a related larger lizard, the now-extinct
380-kg Megalania prisca. Why did Australia, uniquely among
the continents, evolve a lizard as one of its top carnivores? Part of the answer is that Australia is the smallest continent, thus
from its area alone it would have had difficulty supporting an
endothermic carnivore capable of preying on its top herbivore. The
other part of the answer may be Australia's variable low rainfall and
leached ancient soils, resulting in Australia having much lower net
primary productivity than the other landmasses listed in Table 1. That
is, in food availability and supportable population sizes, Australia is
effectively even smaller than its actual area, so that “normal”
large endotherms could not maintain viable populations, but species
with lower metabolic rates could. In agreement with this
interpretation, although Australia's other top carnivore (the
“marsupial lion”) and its top herbivore (a diprotodont or
“marsupial rhinoceros”) were mammals, they were not placentals
but marsupials, whose metabolic rates and food requirements average
20% lower than those of placentals. ¶ Australia's low
productivity may explain why, even taking into account their low
metabolic rates, the calculated food requirements of those two
marsupials were still 50–60% below expectations for Australia's area
(Fig. B). That is, not only were Australia's top mammals
marsupials rather than placentals, but even those marsupials were
smaller than would have been expected if Australia's productivity had
equaled that of the other continents. Interestingly, between about 115 and 54 million years ago, when it was
still part of the supercontinent Gondwana, Australia supported putative
placental mammals, which had become extinct by around 30 million years
ago ( 26). The second-smallest continent, South America, also had
marsupials (and birds) as its top carnivores, but placentals as its top
herbivores, as long as it was isolated; only after South America became
joined to North America around 2.8 million years ago were marsupial
carnivores replaced by placental top carnivores (the sabretooth
Smilodon, puma, and jaguar) whose ranges were much larger
than the area of South America and extend to North America. In
contrast, on the largest and most productive continents (Eurasia, North
America, and Africa) all marsupials became replaced by placentals over
the last 50 million years ( 27). Similarly, nontribosphenid mammals,
whose representatives the monotremes have even lower metabolic rates
than marsupials, were present on all continents until around 60 million
years ago, but became extinct everywhere except Australia. Thus,
considerations of the different metabolic rates of mammalian groups,
and different areas and productivities of continents, help explain the
differential survival of mammalian groups on the continents. Effect of Dispersal. Continuing dispersal from a mainland across a narrow water gap to a
nearby island could lead to insular presences of mainland species much
too large for the area of the island itself. This explanation may apply
to two otherwise highly deviant data points. First, the modern top
carnivore of the California Channel Islands, the Bald Eagle
Haliaeetus leucocephalus (4.7 kg), is 7-fold larger than
expected from Fig. A for the largest island's area
but regularly flies and forages over water and belongs to the same
population as that on the California mainland, only 30 km distant.
Second, Santa Rosa Island off the California coast supported a species
of dwarfed mammoth ( Mammuthus exilis) only 20% the size of
its mainland relative Mammuthus columbi, but still 50 times
larger than expected from Fig. A even for Santa
Rosa's Pleistocene area. However, Pleistocene Santa Rosa was separated
by less than 8 km from the California coast. The high variance in adult
body mass of M. exilis (ranging from 200 to 2,000 kg) and a
few Santa Rosa records of 6,000-kg mainland-sized individuals suggest
periodic dispersal of mainland individuals to Santa Rosa ( 28), as
expected from the good swimming ability of elephants. Effect of Evolutionary Time Required for Body Size Changes. As illustrated by that example of the Santa Rosa mammoth, when a
mainland species colonizes an island, it may arrive with the
“wrong” size for a top herbivore or carnivore on an island of
that area. It may then undergo an evolutionary decrease or increase in
body size, resulting in the many insular dwarfs and giants discussed in
biology textbooks. But evolutionary change takes time, so that at any
instant there will inevitably be misfits between mass and island area. Our database provides several examples of such misfits. The Wrangel
Island mammoth declined by about 65% in body size within at most 5,000
years after the severing of the Late Pleistocene land bridge to Eurasia
( 29), but after those 5,000 years, it was still 40-fold too large for
Wrangel's area. Crete was invaded over-water from the European
mainland early in the Pleistocene by large elephants that eventually
evolved into a 90-kg dwarf species ( Elephas creticus) of a
size more appropriate to Crete's area (Fig. A).
Crete was then invaded in the Middle Pleistocene by mainland elephants
that underwent a 50% evolutionary size reduction to become the endemic
Elephas creutzburgi, but at the time of its Late Pleistocene
extinction its 3,200-kg mass was still 60-fold too large for Crete's
area ( 30). The pygmy hippopotamus of Cyprus, although dwarfed to 200
kg, was still 4-fold too large for Cyprus's area at the time of its
Early Holocene extinction ( 13). Such episodes of invasion and dwarfing
affected many other insular species of other islands of the
Mediterranean and of Wallacea. Conversely, some small-bodied mainland colonists of islands underwent
evolutionary increase in size to become insular giants, such as the big
flightless dodo of Mauritius (derived from a flying pigeon). The top
herbivore of Hawaii was a 7.5-kg goose much larger than its likely
ancestor but still much smaller than the 60-kg herbivore expected from
Fig. A for Hawaii's area. In contrast to
Mauritius, which is 10 million years old, Hawaii is one of the youngest
islands included in Table 1, having formed no more than 375,000 years
ago ( 31); perhaps a considerably longer time is required for a bird to
evolve from 2 to 60 kg. Yet rapid changes in body size are known from
the fossil record. For instance, the red deer of Jersey Island declined
in mass by 80% in at most 6,000 years ( 32). By comparing sizes of
other insular top species with sizes of ancestors and of top species
expected for that area, it may eventually become possible to draw
firmer conclusions about the time scale of evolutionary changes in body
size. Effect of Geological Time Required for Island Area Changes. The 228-km 2 Caribbean island of New Providence is
expected from its area to support an endothermic top carnivore of only
about 0.7 kg. Instead, its top carnivore was a giant hawk 10 times
larger (7.3 kg) than expected, derived from an ancestor weighing only
about 1 kg. Thus, the explanation for its excessive size cannot be
evolutionary time delays in dwarfing—it evolved to be larger rather
than smaller. Instead, the explanation is that the hawk's island
became much smaller. At low-sea-level times of the Pleistocene, the
shallow Great Bahama Bank emerged as a huge low-lying island of about
109,400 km 2, of which only the highest hills
remained above water as New Providence Island after the terminal
Pleistocene rise in sea level ( 33). For an area of 109,400
km 2, Fig. A predicts an
endothermic top carnivore of 12 kg, close to the actual mass of the New
Providence hawk. That is, the apparent discrepancy is an artifact of
linking the New Providence hawk to an inappropriately small modern
area, instead of to the large Pleistocene area in which it actually
evolved. Similar artifacts are expected for other islands that suffered
great area reductions at the end of the Pleistocene. Earlier Species. Our analysis has been restricted to species that lived within the past
65,000 years. Do similar mass/area relations describe earlier mammals
and dinosaurs (Table 2)?
| Table 2The largest dinosaurs and the largest terrestrial mammals
of alltime |
The largest known mammalian herbivore was the rhinocerotoid
Indricotheriun transouralicun (estimated mass 11,000 kg)
from Asia's Oligocene. At that time, Asia was separated from Europe
and had an estimated area of 50,000,000 km2. With
that estimated mass and area, Indricotheriun falls within
the 95% confidence intervals surrounding our endothermic herbivore
line (see Fig. A). The largest known mammals usually considered to be carnivores were the
880-kg creodont Megistotherium osteothlastes from Africa's
early Miocene ( 34), the 750-kg bear Agriotherium africanum
from Africa's early Pliocene ( 35), and the mesonychid
Andrewsarchus mongoliensis (600–900 kg; G. Paul, personal
communication) from Asia's Oligocene. These species all fall above the
95% confidence interval for endothermic carnivores in Fig.
A. However, the largest living terrestrial species
of the order Carnivora today, whose diets are known with certainty, are
bears (up to 800 kg), seven of whose extant eight species (all except
the polar bear) are actually omnivores. Perhaps those earlier large
presumed carnivores were actually omnivores as well ( 36). The largest terrestrial vertebrates of all time were dinosaurs, of
which Table 2 lists the largest known herbivores and carnivores for
three continents. (Those listed top herbivores and top carnivores were
not necessarily contemporaneous.) Their body masses all fall closer to
the ectotherm lines than to the endotherm lines of Fig.
A, suggesting that dinosaurs were
“cold-blooded.” However, the top carnivorous dinosaurs were still
12 times heavier, and the herbivorous dinosaurs 1.5–3 times heavier,
than predicted from the regression lines from Fig.
A for extant ectotherms; therefore, the
never-since-surpassed size of the largest dinosaurs remains
unexplained. Perhaps the answer has to do with high net primary
productivity during the dinosaur era: atmospheric
CO 2 levels then were up to 10 times the present
levels ( 37) and elevated CO 2 stimulates
productivity of some plants ( 38). Although the previous section suggested reasons why certain data
points deviate from the main patterns of Fig. A and
B, there are other deviations that we cannot yet explain:
the top herbivores of Barbuda, New Providence, and Ibiza are smaller
than expected, and New Guinea's top herbivore and top carnivore are
both of an appropriate mass but, being marsupials, have unexpectedly
low food requirements. We suggest three extensions of our study. | | 1. | Among the world's old rivers and lakes, does size of the
largest fish increase with increasing volume of lake, length and
outflow of river, and productivity? It is suggestive that three of the
world's largest rivers—the Nile, Amazon, and Mississippi—contain
some of the largest known fresh-water fish species. | | | 2. | Among whales, the largest planktivore (Blue Whale
Balaenoptera musculus) and carnivores (Sperm Whale
Physeter catodon and Killer Whale Orcinus orca)
all have worldwide distributions. Will it be possible to discern
mass/area or mass/volume relations (importantly influenced by
productivity) in the oceans, and to relate them to those on land? | | | 3. | Our study applies to different landmasses around the world.
Can similar mass/area relations be discerned for species isolated on
separate islands within an archipelago? |
For providing us with unpublished data, we thank Per Christiansen,
Bob Dewer, Helen James, Ben Kear, Doug Kelt, Ross MacPhee, Cecile
Mourer-Chauviré, Ralph Molnar, Patrick Nunn, Maria Rita Palombo,
Greg Paul, Dave Steadman, Alan Tennyson, John Thorbjarnarson, Gerard
Willemsen, Paul Willis, and Trevor Worthy. We thank Bob Hill for
pointing out the relevance of Cretaceous atmospheric CO2
levels. Funding was provided by the Natural Sciences and Engineering
Research Council (Canada). 1. Marquet P A, Taper M L. Evol Ecol. 1998;12:127–139. 2. Klein R J. The Human Condition. Chicago: University of Chicago Press; 1999. 3. Leslie A J. Dissertation. Philadelphia: Drexel University; 1997. 4. Webb G J W, Messel H. Aust J Zool. 1978;26:1–27. 5. Groombridge B. In: Wildlife Management: Crocodiles and Alligators. Webb G J W, Manolis S C, Whitehead P J, editors. Chipping Norton, U.K.: Surrey Beatty; 1987. pp. 9–21. 6. Snell H L, Christian K A. Herpetologica. 1985;41:437–442. 7. Livezey B C. J Zool. 1993;230:247–292. 8. Coe M J, Bourn D, Swingland I R. Philos Trans R Soc London B. 1979;286:163–176. 9. Clough G C. J Mammal. 1972;53:807–823. 10. Dunning J B., Jr CRC Handbook of Avian Body Masses. Boca Raton, FL: CRC; 1993. 11. Alcover J A, Pérez-Obiol R, Yll E I, Bover P. Biol J Linn Soc. 1999;66:57–74. 12. Morrison J L. In: The Birds of North America. Poole A, Gill F, editors. Philadelphia: Acad. Nat. Sci.; 1996. , No. 249. 13. Simmons A H. Faunal Extinction in an Island Society: Pygmy Hippopotamus Hunters of Cyprus. New York: Kluwer; 1999. 14. Nowak R M. Walker's Mammals of the World. Baltimore: Johns Hopkins Univ. Press; 1999. 15. van den Bergh G D. Scr Geol. 1999;117:1–419. 16. Ciofi C. Sci Am. 1999;280:85–91. 17. Steadman D W. Zool Verh. 1999;327:7–21. 18. Brathwaite D H. Notornis. 1992;39:239–247. 19. Amadon D. Condor. 1947;49:159–164. 20. Flannery T F, Roberts R G. In: Extinctions in Near Time. MacPhee R D E, editor. New York: Kluwer; 1999. pp. 239–253. 21. Murray P. In: Vertebrate Palaeontology of Australasia. Vickers-Rich P, Monaghan J M, Baird R F, Rich T H, editors. Melbourne: Pioneer Design Studio; 1991. pp. 1071–1163. 22. Anyonge W. J Zool. 1993;231:339–350. 23. Ricklefs R E. The Economy of Nature. New York: Freeman; 1996. 24. Kelt D A, Van Vuren D H. Am Nat. 2001;157:637–645. 25. Thomas C D. Conserv Biol. 1990;4:324–327. 26. Rich T H, Vickers-Rich P, Constantine A, Flannery T F, Kool L, van Klaveren N. Science. 1997;278:1438–1442. [PubMed] 27. Szalay F S. Evolutionary History of the Marsupials and an Analysis of Osteological Characters. New York: Cambridge Univ. Press; 1994. 28. Roth V L. In: The Proboscidea: Evolution and Palaeoecology of Elephants and Their Relatives. Shoshani J, Tassy P, editors. Oxford: Oxford Univ. Press; 1996. pp. 249–253. 29. Lister A M. Nature (London). 1993;362:288–289. 30. Caloi L, Kotsakis T, Palombo M R, Petronio C. In: The Proboscidea: Evolution and Palaeoecology of Elephants and Their Relatives. Shoshani J, Tassy P, editors. Oxford: Oxford Univ. Press; 1996. pp. 234–239. 31. Nunn P D. Oceanic Islands. Oxford: Blackwell; 1994. 32. Lister A M. Nature (London). 1989;342:539–542. [PubMed] 33. Morgan G S. In: Biogeography of the West Indies: Past, Present, and Future. Woods C A, editor. Gainesville, FL: Sandhill Crane; 1989. pp. 685–740. 34. Savage R J G. Bull Br Mus (Nat Hist), Geol. 1973;22:485–511. 35. Hendey Q B. Langebaanweg. A Record of Past Life. Cape Town, South Africa: South African Museum; 1982. 36. Farlow J O. Am J Sci. 1993;293:167–199. 37. Ekart D D, Cerling T E, Montanez I P, Tabor N J. Am J Sci. 1999;299:805–827. 38. Saxe H, Ellsworth D S, Heath J. New Phytol. 1998;139:395–436. 39. Wedel M J, Cifelli R L, Sanders R K. Acta Palaeontol Pol. 2000;45:343–388. 40. Christiansen P. J Vert Paleontol. 1999;19:666–680. 41. Fortelius M, Kappelman J. Zool J Linn Soc. 1993;107:85–101.
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