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Dinosaurs, Dragons, and Dwarfs: the Evolution of Maximal Body Size

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Dinosaurs, Dragons, and Dwarfs: the Evolution of Maximal Body Size 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 Contributed by Jared Diamond, October 15, 2001 Among local faunas, the maximum body size and taxonomic 2. For a given land area, the top herbivore will be larger than affiliation of the top terrestrial vertebrate vary greatly. Does this the top carnivore by a factor predictable from the greater variation reflect how food requirements differ between trophic amounts of food available to herbivores than to carnivores. levels (herbivores vs. carnivores) and with taxonomic affiliation 3. Within a trophic level and for a given area of landmass, top (mammals and birds vs. reptiles)? We gathered data on the body species that are ectotherms will be larger than ones that are size and food requirements of the top terrestrial herbivores and endotherms, by a factor predictable from ectotherms’ lower carnivores, over the past 65,000 years, from oceanic islands and food requirements. continents. The body mass of the top species was found to increase with increasing land area, with a slope similar to that of the On reflection, one can think of other factors likely to perturb relation between body mass and home range area, suggesting that these predictions, such as environmental productivity, over- maximum body size is determined by the number of home ranges water dispersal, evolutionary times required for body size that can fit into a given land area. For a given land area, the body changes, and changing landmass area with geological time. size of the top species decreased in the sequence: ectothermic Indeed, our database does suggest effects of these other factors. herbivore > endothermic herbivore > ectothermic carnivore > We propose our three predictions not because we expect them endothermic carnivore. When we converted body mass to food always to be correct, but because we expect them to describe requirements, the food consumption of a top herbivore was about broad patterns that must be understood in order to be able to 8 times that of a top carnivore, in accord with the factor expected detect and interpret deviations from those patterns. from the trophic pyramid. Although top ectotherms were heavier Data than top endotherms at a given trophic level, lower metabolic rates per gram of body mass in ectotherms resulted in endotherms and For continents and oceanic islands with a good fossil record for ectotherms having the same food consumption. These patterns the last 65,000 years, Table 1 lists the identity and mean adult explain the size of the largest-ever extinct mammal, but the size of body mass of the top herbivore and top carnivore, most of them the largest dinosaurs exceeds that predicted from land areas and known only as Late Pleistocene or Holocene fossils. We chose a remains unexplained. 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 he size and taxonomic affiliation of the largest locally present top species. species (‘‘top species’’) of terrestrial vertebrate vary greatly T We used mean adult mass of each species rather than mass of among faunas, raising many unsolved questions. Why are the top the largest known individual. In studies providing only a range species on continents bigger than those on even the largest of masses, we averaged the range. To generate a species mean, islands, bigger in turn than those on small islands? Why are we averaged male and female body masses. When calculating the the top mammals marsupials on Australia but placentals on the mean mass of extant reptiles, we included only mass estimates for other continents? Why is the world’s largest extant lizard (the individuals of breeding age and͞or size. When no body mass Komodo dragon) native to a modest-sized Indonesian island, of values were available (e.g., for many extinct species), we esti- all unlikely places? Why is the top herbivore larger than the top mated body mass from linear dimensions through comparisons carnivore at most sites? Why were the largest dinosaurs bigger with related extant species of known body mass, using regression than any modern terrestrial species? equations (refs. 3 and 4; P. Christiansen, personal communica- A useful starting point is the observation of Marquet and tion), or else assuming body mass to increase as the cube of linear Taper (1), based on three data sets (Great Basin mountaintops, dimensions. Sea of Cortez islands, and the continents), that the size of a In some cases, a top species occurred on multiple islands landmass’s top mammal increases with the landmass’s area. To within an archipelago but was unlikely to disperse often among explain this pattern, they noted that populations numbering less islands, hence each island must have had a nearly self-sustaining than some minimum number of individuals are at high risk of population. We report such a species only once, using the area extinction, but larger individuals require more food and hence of the largest island on which it was the top herbivore or larger home ranges, thus only large landmasses can support at carnivore. Because some avian carnivores (e.g., sea eagles least the necessary minimum number of individuals of larger- Haliaeetus sp.) readily cross water gaps, we excluded them if they bodied species. If this reasoning were correct, one might expect occurred on islands less than an arbitrarily defined 50 km from body size of the top species also to depend on other correlates a larger landmass. of food requirements and population densities, such as trophic We included terrestrial and freshwater crocodiles known or level and metabolic rate. Hence we assembled a data set suspected to prey on terrestrial vertebrates. We excluded salt- consisting of the top terrestrial herbivores and carnivores on 25 oceanic islands and the 5 continents to test 3 quantitative predictions. †Present address: Department of Biology, Queens University, Kingston, ON, Canada, K7l 3N6. 1. Within a trophic level, body mass of the top species will ‡To whom reprint requests should be addressed. E-mail: [email protected]. increase with land area, with a slope predictable from the The publication costs of this article were defrayed in part by page charge payment. This slope of the relation between body mass and home range article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. area. §1734 solely to indicate this fact. 14518–14523 ͉ PNAS ͉ December 4, 2001 ͉ vol. 98 ͉ no. 25 www.pnas.org͞cgi͞doi͞10.1073͞pnas.251548698 Downloaded by guest on September 27, 2021 Table 1. Top herbivores and top carnivores for various land masses in the Late Pleistocene or Holocene Island Area, km2 Herbivore Mass, kg Ref. Carnivore Mass, kg Ref. Ratio‡‡ Plaza Sur 0.12 Conolophus subcristatus† (Galapagos 2.7 6 Asio flammeus** (Short-eared owl) land iguana) Pinta 59 Geochelone nigra abingdoni 88 § Buteo galapagoensis** (Galapagos (Galapagos tortoise) hawk) Rodriguez 108 Pezophaps solitaria (Solitaire) 23 7 Mascarenotus murivorus (Owl) 0.35 ʈ 17.7 Aldabra 129 Geochelone gigantea (Aldabran 41 8 Tyto alba (Barn owl) 0.41 ¶ 5.0 tortoise) Barbuda 172 Oryzomyine rodent (Undescribed rice 0.79 ¶ Tyto neddi (Barn owl) 1.0 ¶ 0.7 rat) Santa Rosa 209 Mammuthus exilis (Dwarf mammoth) 1150 ¶ Haliaeetus leucocephalus** (Bald eagle) New Providence 228 Geocapromys ingrahami (Bahaman 0.71 9 Titanohierax gloveralleni (Buteonine 7.3 ¶ 0.2 hutia) hawk) Tongatapu 259 Megapodius molistructor (Brush 3.5 ʈ Accipiter cf. rufitorques (Hawk) 0.28 ¶ 5.7 turkey) Ibiza 577 Anser n. sp. (Goose) 2.0 ¶ Haliaeetus albicilla (White-tailed eagle) 4.8 10 0.6 Mauritius 1,874 Raphus cucullatus (Dodo) 19 7 Circus alphonsi (Harrier) 0.63 ¶ 10.3 Mallorca 3,667 Myotragus balearicus (Cave goat) 40 11 Aquila chrysaetos (Golden eagle) 4.2 10 5.2 Crete 8,259 Elephas creutzburgi (Dwarf elephant) 3200 ¶ Lutrogale cretensis (Cretan otter) 11 ʈ 77.6 Puerto Rico 9,104 Elasmodontomys obliquus (Rodent) 50 ʈ Caracara sp. (Caracara) 1.0 12 16.7 Cyprus 9,251 Phanourios minutus (Dwarf 200 13 Genetta cf. plesictoides (Genet) 2 14 34.1 hippopotomus) Hawaii 10,434 ‘‘Large Hawaii goose’’ 7.5 ʈ Haliaeetus albicilla†† (White-tailed 4.8 10 1.4 eagle) Viti Levu 10,531 Megavitiornis altirostris (Pigeon) 15 ʈ Volia athollandersoni (Crocodile) 10 ʈ 8.7 Jamaica 10,991 Heptaxodontidae: unnamed sp.A 100 ʈ Accipitridae: gen͞sp. ind. (Hawk͞eagle) 1.0 ʈ 28.4 (Rodent) Flores 14,154 Feral species only 15 Varanus komodoensis (Komodo 70 16 dragon) New Caledonia 16,648 Sylviornis neocaledoniae (Brush 40 17 Mekosuchus inexpectatus (Crocodile) 15 ʈ 11.8 turkey) Sardinia 24,090 Megaloceros cazioti (Deer) 70 ¶ Cynotherium sardous (Fox) 15 ʈ 3.3 Hispaniola 76,192 Megalocnus zile‡ (Ground sloth) 150 ʈ Titanohierax sp. (Buteonine hawk) 7.6 ¶ 9.6 EVOLUTION Cuba 110,860 Megalocnus rodens‡ (Ground sloth) 150 ʈ Ornimegalonyx oteroi (Strigid owl) 8.3 ¶ 9.0 Sulawesi* 189,216 Bubalus depressicornis (Lowland 225 14 Crocodylus siamensis (Siamese 57 ¶ 14.5 anoa) crocodile) Macrogalidia musschenbroeki 5.1 14 (Sulawesian palm civet) New Zealand 270,534 Dinornis giganteus (Moa) 117 ʈ Harpagornis moorei (New Zealand 13 18 4.5 eagle) Madagascar* 587,040 Aepyornis maximus (Elephant bird) 440 19 Crocodylus robustus (Crocodile) 170 ¶ 6.51 Cryptoprocta spelea (Fossa) 17 ʈ New Guinea 808,510 Nototherium watutense 300 20 Thylacinus cynocephalus (Tasmanian 25 ʈ 5.23 (Diprotodontid marsupial) wolf) Australia* 7,682,395 Diprotodon opatum (Diprotodont 1150 21 Megalania prisca (Varanid lizard) 380 ¶ 3.5 marsupial) Thylacoleo carnifax (Marsupial lion) 73 ʈ South America 17,815,420 Cuvieronius sp.
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