Biology of the sauropod dinosaurs: the evolution of gigantism.
The herbivorous sauropod dinosaurs of the Jurassic and Cretaceous periods were the largest terrestrial animals ever, surpassing the largest herbivorous mammals by an order of magnitude in body mass. Several evolutionary lineages among Sauropoda produced giants with body masses in excess of 50 metric tonnes by conservative estimates. With body mass increase driven by the selective advantages of large body size, animal lineages will increase in body size until they reach the limit determined by the interplay of bauplan, biology, and resource availability. There is no evidence, however, that resource availability and global physicochemical parameters were different enough in the Mesozoic to have led to sauropod gigantism. We review the biology of sauropod dinosaurs in detail and posit that sauropod gigantism was made possible by a specific combination of plesiomorphic characters (phylogenetic heritage) and evolutionary innovations at different levels which triggered a remarkable evolutionary cascade. Of these key innovations, the most important probably was the very long neck, the most conspicuous feature of the sauropod bauplan. Compared to other herbivores, the long neck allowed more efficient food uptake than in other large herbivores by covering a much larger feeding envelope and making food accessible that was out of the reach of other herbivores. Sauropods thus must have been able to take up more energy from their environment than other herbivores. The long neck, in turn, could only evolve because of the small head and the extensive pneumatization of the sauropod axial skeleton, lightening the neck. The small head was possible because food was ingested without mastication. Both mastication and a gastric mill would have limited food uptake rate. Scaling relationships between gastrointestinal tract size and basal metabolic rate (BMR) suggest that sauropods compensated for the lack of particle reduction with long retention times, even at high uptake rates. The extensive pneumatization of the axial skeleton resulted from the evolution of an avian-style respiratory system, presumably at the base of Saurischia. An avian-style respiratory system would also have lowered the cost of breathing, reduced specific gravity, and may have been important in removing excess body heat. Another crucial innovation inherited from basal dinosaurs was a high BMR. This is required for fueling the high growth rate necessary for a multi-tonne animal to survive to reproductive maturity. The retention of the plesiomorphic oviparous mode of reproduction appears to have been critical as well, allowing much faster population recovery than in megaherbivore mammals. Sauropods produced numerous but small offspring each season while land mammals show a negative correlation of reproductive output to body size. This permitted lower population densities in sauropods than in megaherbivore mammals but larger individuals. Our work on sauropod dinosaurs thus informs us about evolutionary limits to body size in other groups of herbivorous terrestrial tetrapods. Ectothermic reptiles are strongly limited by their low BMR, remaining small. Mammals are limited by their extensive mastication and their vivipary, while ornithsichian dinosaurs were only limited by their extensive mastication, having greater average body sizes than mammals.
Steinmann Institute, University of Bonn, Germany. martin.sander@uni-bonn.de
P Martin
PM
Sander
Andreas
A
Christian
Marcus
M
Clauss
Regina
R
Fechner
Carole T
CT
Gee
Eva-Maria
EM
Griebeler
Hanns-Christian
HC
Gunga
Jürgen
J
Hummel
Heinrich
H
Mallison
Steven F
SF
Perry
Holger
H
Preuschoft
Oliver W M
OW
Rauhut
Kristian
K
Remes
Thomas
T
Tütken
Oliver
O
Wings
Ulrich
U
Witzel
D000818:Animals; D005075:Biological Evolution; D049628:Body Size; D001846:Bone Development; D001842:Bone and Bones / Q000033:anatomy & histology*; D025061:Dinosaurs / Q000033:anatomy & histology* / Q000145:classification / Q000254:growth & development*; D005580:Fossils; D010802:Phylogeny
J Exp Biol. 2005 May;208(Pt 9):1611-9
15855392
J Theor Biol. 1986 Feb 21;118(4):491-9
3713220
Science. 2009 Mar 27;323(5922):1671-2; author reply 1671-2
19325098
Science. 2001 Jun 1;292(5522):1704-6
11387472
Br J Nutr. 1982 Mar;47(2):267-72
6279144
Q Rev Biol. 2000 Dec;75(4):385-407
11125698
Science. 2005 Jul 29;309(5735):761-4
16051793
Oecologia. 2003 Jun;136(1):14-27
12712314
PLoS One. 2009 Sep 16;4(9):e6924
19756139
J Evol Biol. 2007 Mar;20(2):627-38
17305829
J Exp Biol. 1995 Mar;198(Pt 3):629-32
7714452
Trends Ecol Evol. 2005 Dec;20(12):677-84
16701457
PLoS One. 2007 Nov 21;2(11):e1230
18030355
J Vestib Res. 2005;15(2):65-71
15951620
J Exp Zool A Ecol Genet Physiol. 2009 Oct 1;311(8):629-46
19810215
J Exp Zool A Ecol Genet Physiol. 2009 Oct 1;311(8):611-28
19204909
Proc Biol Sci. 2003 Aug 22;270(1525):1753-8
12965005
J Evol Biol. 2009 Mar;22(3):446-59
19210589
Anat Rec A Discov Mol Cell Evol Biol. 2005 Apr;283(2):391-401
15747343
Oecologia. 1978 Jan;37(2):257-272
28309655
Proc Biol Sci. 2008 May 7;275(1638):1015-21
18252667
Nature. 2000 Sep 7;407(6800):72-4
10993074
J Evol Biol. 2005 May;18(3):587-95
15842488
J Exp Zool A Ecol Genet Physiol. 2009 Oct 1;311(8):600-10
19189317
Comp Biochem Physiol A Mol Integr Physiol. 2007 Oct;148(2):249-65
17643330
Nature. 2009 Feb 5;457(7230):715-7
19194448
PLoS One. 2009;4(2):e4532
19225569
Nature. 2001 Jul 26;412(6845):429-33
11473315
PLoS Biol. 2006 Jul;4(8):e248
16817695
Science. 2006 Dec 22;314(5807):1925-7
17185599
Nature. 2004 Jun 17;429(6993):746-9
15201907
Biol Lett. 2009 Jun 23;5(3):317-9
19364714
Oecologia. 1992 Mar;89(3):428-434
28313093
Evolution. 2001 Dec;55(12):2523-33
11831667
Science. 1999 Nov 12;286(5443):1342-7
10558986
Nature. 2005 Jun 2;435(7042):670-2
15931221
J Evol Biol. 2006 Jul;19(4):1210-21
16780522
Comp Biochem Physiol A Mol Integr Physiol. 2009 Nov;154(3):376-82
19651229
An Acad Bras Cienc. 2007 Sep;79(3):529-41
17768539
PLoS Biol. 2010 Mar 02;8(3):e1000322
20209142
Proc Biol Sci. 2000 Sep 22;267(1455):1883-7
11052540
J Morphol. 2007 Aug;268(8):701-14
17514722
Naturwissenschaften. 2004 Oct;91(10):493-7
15729763
Proc Biol Sci. 2004 May 22;271(1543):1081-90
15293863
Science. 1998 May 1;280(5364):731-4
9563948
PLoS One. 2009;4(2):e4497
19223979
Proc Biol Sci. 2009 May 7;276(1662):1731-6
19324837
Proc Biol Sci. 2007 Mar 7;274(1610):635-40
17254987
Science. 2003 Jul 11;301(5630):169; author reply 169
12855792
J Exp Biol. 2009 Aug;212(Pt 15):2328-36
19617425
J Morphol. 1980 Dec;166(3):337-86
7441763
Curr Biol. 2007 Nov 20;17(22):R969-71
18029253
J Anim Physiol Anim Nutr (Berl). 2006 Aug;90(7-8):300-8
16867075
Nature. 2002 Jan 31;415(6871):489, 491
11823844
Science. 1999 Apr 30;284(5415):798-800
10221910
Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1347-52
16432187
Integr Comp Biol. 2002 Jul;42(3):424-30
21708737
J Exp Biol. 1998 Apr;201(Pt 8):1043-50
9510518
Proc Biol Sci. 2008 Nov 7;275(1650):2483-90
18647715
Q Rev Biol. 1978 Sep;53(3):243-82
362471
Naturwissenschaften. 2007 Aug;94(8):623-30
17356876
Adv Anat Embryol Cell Biol. 1983;79:1-81
6869074
Proc Biol Sci. 2009 May 22;276(1663):1815-21
19324778
Lancet. 1992 Aug 29;340(8818):534-6
1354287
Science. 2008 Oct 10;322(5899):200-1
18845734
Proc Natl Acad Sci U S A. 2007 Jun 26;104(26):10808-12
17576932
Proc Biol Sci. 2006 Aug 7;273(1596):1849-55
16822743
Proc Natl Acad Sci U S A. 2010 May 18;107(20):9258-63
20435913
Trends Ecol Evol. 1997 Jun;12(6):235-9
21238056
J Anim Physiol Anim Nutr (Berl). 2003 Apr;87(3-4):160-73
14511142
Science. 1994 Jul 8;265(5169):222-4
17750663
Science. 1998 Oct 2;282(5386):50-2
9786796
Science. 2007 Apr 27;316(5824):557-8
17463279
Auton Neurosci. 2005 Feb 7;117(2):115-9
15664564
Evolution. 1973 Mar;27(1):1-26
28563664
Comp Biochem Physiol A Mol Integr Physiol. 2009 Dec;154(4):523-9
19720152
Proc Natl Acad Sci U S A. 2009 Jul 21;106(29):12184-8
19581600
Comp Biochem Physiol A Mol Integr Physiol. 2008 Jul;150(3):274-81
18450489
Am Nat. 2007 Dec;170(6):E129-42
18171160
Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):4046-9
12637681
Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):14518-23
11724953
J Exp Biol. 2006 Oct;209(Pt 19):3812-27
16985198
Nature. 2005 Jul 14;436(7048):253-6
16015329
Science. 2005 Nov 18;310(5751):1177-80
16293759
Nature. 2006 Jun 8;441(7094):739-41
16760975
Science. 1964 Feb 7;143(3606):576-7
17815652
Proc Biol Sci. 2005 Nov 7;272(1578):2325-8
16191647
Am Nat. 2007 Jan;169(1):130-5
17206591
Proc Biol Sci. 2002 Mar 22;269(1491):613-21
11916478
Biol Lett. 2007 Oct 22;3(5):558-61
17638674
Am Nat. 2003 Mar;161(3):413-21
12699221
Science. 2008 Aug 29;321(5893):1197-200
18755974
Proc Natl Acad Sci U S A. 2008 Jan 15;105(2):582-7
18195356
Trends Ecol Evol. 2005 Jan;20(1):4-6
16701331
Science. 2005 Dec 16;310(5755):1800-2
16357257
Biol Rev Camb Philos Soc. 2001 Aug;76(3):411-47
11569792
Evolution. 1976 Mar;30(1):186-187
28565045
PLoS One. 2009;4(2):e4397
19209223
Proc Biol Sci. 2004 May 7;271 Suppl 4:S180-3
15252977
J Anim Ecol. 2008 Jan;77(1):173-83
18177336