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Year: 2011
Biology of the sauropod dinosaurs: the evolution of gigantism
Sander, P M; Christian, A; Clauss, M; Fechner, R; Gee, C T; Griebeler, E M; Gunga,
H C; Hummel, J; Mallison, H; Perry, S F; Preuschoft, H; Rauhut, O W M; Remes, K;
Tütken, T; Wings, O; Witzel, U
Sander, P M; Christian, A; Clauss, M; Fechner, R; Gee, C T; Griebeler, E M; Gunga, H C; Hummel, J; Mallison, H;
Perry, S F; Preuschoft, H; Rauhut, O W M; Remes, K; Tütken, T; Wings, O; Witzel, U (2011). Biology of the
sauropod dinosaurs: the evolution of gigantism. Biological Reviews of the Cambridge Philosophical Society,
86(1):117-155.
Postprint available at:
http://www.zora.uzh.ch
Posted at the Zurich Open Repository and Archive, University of Zurich.
http://www.zora.uzh.ch
Originally published at:
Sander, P M; Christian, A; Clauss, M; Fechner, R; Gee, C T; Griebeler, E M; Gunga, H C; Hummel, J; Mallison, H;
Perry, S F; Preuschoft, H; Rauhut, O W M; Remes, K; Tütken, T; Wings, O; Witzel, U (2011). Biology of the
sauropod dinosaurs: the evolution of gigantism. Biological Reviews of the Cambridge Philosophical Society,
86(1):117-155.
Biology of the sauropod dinosaurs: the evolution of gigantism
Abstract
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.
Biol. Rev. (2011), 86, pp. 117–155.
doi: 10.1111/j.1469-185X.2010.00137.x
117
Biology of the sauropod dinosaurs:
the evolution of gigantism
P. Martin Sander1 , Andreas Christian2 , Marcus Clauss3 , Regina Fechner4 , Carole
T. Gee1 , Eva-Maria Griebeler5 , Hanns-Christian Gunga6 , Jürgen Hummel7 , Heinrich
Mallison8 , Steven F. Perry9 , Holger Preuschoft10 , Oliver W. M. Rauhut4 , Kristian
Remes1,4 , Thomas Tütken11 , Oliver Wings8 and Ulrich Witzel12
1 Steinmann
Institute, Division of Palaeontology, University of Bonn, Nussallee 8, 53115 Bonn, Germany
für Biologie und Sachunterricht und ihre Didaktik, University of Flensburg, Auf dem Campus 1, 24943 Flensburg, Germany
3
Clinic for Zoo Animals, Exotic Pets and Wildlife, University of Zurich, Winterthurerstr. 260, 8057 Zurich, Switzerland
4 Bayerische Staatssammlung für Paläontologie und Geologie, University of Munich, Richard-Wagner-Strasse 10, 80333 Munich, Germany
5 Institut für Zoologie, Abteilung Ökologie, University of Mainz, Johann-Joachim-Becher Weg 13, 55128 Mainz, Germany
6 Zentrum für Weltraummedizin Berlin, Institut für Physiologie, Charite-University of Berlin, Arnimallee 22, 14195 Berlin, Germany
7
Institut für Tierwissenschaften, University of Bonn, Endenicher Allee 15, 53115 Bonn, Germany
8 Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung an der Humboldt-Universität zu Berlin, Invalidenstrasse
43, 10115 Berlin, Germany
9 Institut für Zoologie, Morphologie und Systematik, University of Bonn, Poppelsdorfer Schloss, 53115 Bonn, Germany
10
Institut für Anatomie, Abteilung für Funktionelle Morphologie, University of Bochum, Universitätsstrasse 150, 44801 Bochum, Germany
11 Steinmann Institute, Division of Mineralogy, University of Bonn, Poppelsdorfer Schloss, 53115 Bonn, Germany
12 Institut für Konstruktionstechnik, Fakultät für Maschinenbau, University of Bochum, Universitätsstrasse 150, 44801 Bochum, Germany
2 Institut
(Received 9 September 2009; revised 13 March 2010; accepted 16 March 2010)
ABSTRACT
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.
* Address for correspondence: E-mail: martin.sander@uni-bonn.de
Re-use of this article is permitted in accordance with the Terms and Conditions set out at http://wileyonlinelibrary.com/onlineopen#
OnlineOpen Terms
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
P. Martin Sander and others
118
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.
Key words: Dinosauria, Sauropoda, gigantism, Mesozoic, long neck, phylogenetic heritage, evolutionary innovation.
CONTENTS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) General introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Importance of body size . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(3) Methods of estimating body mass in dinosaurs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(4) Unique body size of sauropods and theropods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(5) Cope’s Rule in Sauropodomorpha and selective advantages of large body size . . . . . . . . . . . . . . . . . . . . . . . .
(6) Diversity of the Sauropoda . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(7) Sauropodomorph phylogeny and evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
II. Bauplan and biology of sauropod dinosaurs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Bauplan and skeletal anatomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Musculature reconstruction and locomotor evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(3) Locomotion: gait and speed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(4) Integument . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(5) Respiratory system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(6) Dentition and digestive system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(7) Circulatory system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(8) Nervous system and sense organs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(9) Organ size and its scaling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(10) Physiology and thermoregulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(a) Lines of evidence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(b) Bone histologic evidence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(c) Scaling effects: gigantothermy and ontogenetic change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(d) Synthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(11) Life history, growth, and reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
III. Body size evolution in sauropodomorpha . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Body size in basal dinosauriforms and basal sauropodomorphs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Body size in early and basal sauropods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(3) Body size in Neosauropoda . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(4) Independent gigantism in several lineages . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(5) Island dwarfing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(6) Body size evolution and Cope’s Rule . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
IV. Hypotheses explaining giant body size . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Limits to body size . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Resource availability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
V. More resources available through different boundary conditions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Physical boundary conditions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(a) Increased oxygen content of atmosphere . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(b) Increased plant productivity through increased CO2 content of the atmosphere . . . . . . . . . . . . . . . . . . .
(c) Higher ambient temperatures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Biological boundary conditions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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Biology of the sauropod dinosaurs
VI.
VII.
VIII.
IX.
X.
XI.
XII.
XIII.
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(a) More nutritious food . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(b) Exceptionally productive habitats: mangroves and tidal flats . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
More resources available through evolutionary innovation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Long neck . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(a) First hypothesis: extension of reach . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(b) Second hypothesis: large feeding envelope versus acceleration of whole body . . . . . . . . . . . . . . . . . . . . . .
(2) Feeding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(3) Greater digestive efficiency . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(4) Avian-style respiratory system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Fewer resources used . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Reduction in body density . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(a) Superior skeletal materials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(b) Light-weight construction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Reduced cost of locomotion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(3) Reduced cost of respiration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(4) Lower basal metabolic rate and gigantothermy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(5) Reduced cost of reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Faster population recovery and faster individual growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Ovipary and gigantism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Survivorship, high growth rate, and high BMR . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Historical contingency . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Decreased oxygen content of atmosphere . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Poor food quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
I. INTRODUCTION
(1) General introduction
Body size is one of the most fundamental attributes of any
organism (Hunt & Roy, 2005; Bonner, 2006). While some
body size maxima (and minima) can be observed and studied
directly in living organisms (e.g. the largest trees and the
largest marine vertebrates), others have occurred in the geologic past. These must be studied from the fossil record, e.g.
the largest insects (giant dragonflies of the Carboniferous), the
largest terrestrial predators (theropod dinosaurs), and the
largest terrestrial animals ever, the sauropod dinosaurs
(Fig. 1). Their uniquely gigantic body size commands special interest from an evolutionary perspective. Sauropod
dinosaurs represent a hugely successful radiation of herbivores that originated in the Late Triassic, dominated terrestrial ecosystems in the Jurassic, and flourished until the very
end of the Cretaceous (Curry Rogers & Wilson, 2005; Tidwell
& Carpenter, 2005). The aim of this paper is to review the
evolution of gigantism in sauropod dinosaurs and to discuss
and explore hypotheses explaining their unique body size.
Body size may either be expressed as linear dimensions,
such as total length or height, or as body mass. Body mass is
more relevant to most biological processes and thus is most
commonly used throughout this review. Since sauropod
skeletons are often incompletely preserved and the femur is
the largest bone in the sauropod skeleton, its length is a good
140
140
140
140
141
141
141
142
142
143
143
143
143
144
144
144
144
145
145
145
145
145
145
146
148
148
148
proxy for body size (Carrano, 2006), be it defined as linear
dimensions or as body mass.
Large body size evolved very early on and remained a
hallmark throughout sauropod evolution (Dodson, 1990).
The discrepancy in body size between other dinosaurs and
sauropods, as well as between the largest land mammals
and sauropods (Figs 1, 2), has recently been highlighted by
the availability of more accurate mass estimates (see Table 1)
calculated from volume estimates based on photogrammetric
measurements of actual skeletons (Gunga et al., 2007, 2008;
Stoinski, Suthau & Gunga, in press) or based on scientific
reconstructions (e.g. Paul, 1987, 1997a; Henderson, 1999,
2006; Seebacher, 2001). These estimates place common
sauropods consistently in the 15–40 t category (Table 1).
In addition, there are a number of very large sauropods,
e.g. the basal macronarian Sauroposeidon (Wedel, Cifelli &
Sanders, 2000a, b) and the titanosaur Argentinosaurus, for which
published estimates (reviewed in Mazzetta, Christiansen &
Farina, 2004) are a staggering 70–90 t! Small sauropod
species with an adult body mass of less than 4–5 t are almost
unknown (Table 1) with the exception of several dwarf forms
from palaeo-islands (Weishampel, Grigorescu & Norman,
1991; Jianu & Weishampel, 1999; Dalla Vecchia, 2005;
Sander et al., 2006; Benton et al., 2010; Stein et al., in press).
The largest representatives of all other dinosaur lineages,
despite being very big in general perception, rarely exceeded
the 10 t threshold and thus actually are in the size
range of very large terrestrial mammals such as the fossil
indricotheres (Fortelius & Kappelman, 1993) and extant and
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
120
Fig. 1. The largest representatives of different terrestrial
vertebrate clades, both extant and extinct. (A) Non-dinosaurian
terrestrial vertebrates and birds: (a) the tortoise Geochelone
gigantea, (b) the Komodo dragon Varanus komodoensis, (c) the
Pleistocene Australian monitor † Varanus (Megalania) prisca,
(d) the Eocene boid snake † Titanoboa cerrejonensis, (e) Homo
sapiens, (f) the African elephant Loxodonta africana, (g) the longnecked Oligocene rhinoceros † Paraceratherium (Indricotherium)
transouralicum, (h) Struthio camelus, (i) an unnamed Miocene †
Phorusracidae. (B) non-avian dinosaurs: (a) the hadrodaur †
Shantungosaurus giganteus, (b) the ceratopsian † Triceratops horridus,
(c) the theropod † Tyrannosaurus rex, (d) the theropod † Spinosaurus
aegyptiacus, (e) the sauropod † Brachiosaurus brancai, (f) the
sauropod † Argentinosaurus huinculensis. Scale = 5 m.
fossil elephants (Fig. 2). Among animals, only whales grow to
a body mass larger than sauropods, but a direct comparison
between these two groups is not very meaningful because of
the fundamentally different constraints of the aquatic versus
the terrestrial environment.
(2) Importance of body size
Body size is fundamentally linked to the bauplan, life history,
and ecology of any organism (Clutton-Brock & Harvey, 1983;
Peters, 1983; Schmidt-Nielsen, 1984; Alexander, 1998; Hunt
& Roy, 2005; Makarieva, Gorshkov & Li, 2005; Bonner,
2006), each bauplan having its lower and upper limit at
which it can function. In addition, body size evolution and
implications of body size for other species characteristics have
received an increasing amount of attention in recent years
because it has been realized that evolutionary innovation is
closely tied to body size changes in evolutionary lineages.
Miniaturization may lead to new designs, and body size
decrease and increase is coupled with heterochrony leading
to changes in morphology (Long & McNamara, 1995, 1997a,
b; McNamara, 1997; McNamara & McKinney, 2005).
(3) Methods of estimating body mass in dinosaurs
Any discussion of gigantism in sauropod dinosaurs requires
reliable estimates of their body mass. Highly disparate
estimates can be found in the literature (Peczkis, 1994; see
P. Martin Sander and others
also Table 1), mainly due to different methods employed.
Mass estimates are generally either based on some
measure of volume that is then converted into body
mass or on a biomechanical approach, e.g. using long
bone circumference (Anderson, Hall-Martin & Russell,
1985; corrected by Alexander, 1989; see also Packard,
Boardman & Birchard, 2009; Cawley & Janacek, 2010).
Each method has different sources of error, and the main
advantages and disadvantages of some of these methods have
been intensively discussed in the literature (Colbert, 1962;
Lambert, 1980; Schmidt-Nielsen, 1984, 1997; Anderson
et al., 1985; Haubold, 1990; Gunga et al., 1999; Paul,
1997b, Henderson, 1999; Seebacher, 2001; Motani, 2001;
Christiansen & Fariña, 2004; Mazzetta et al., 2004; Foster,
2007; Packard et al., 2009).
One method for estimating body mass based on
reconstructed body volume involves three-dimensional
photogrammetry of actual skeletons using a laser scanner
(Gunga et al., 1999; 2007, 2008; Bates et al., 2009; Stoinski
et al., in press). Advantages of this approach include that
geometrical calculations can be made easily based on the
respective body parts, and that different hypothetical body
shapes, resulting in different body masses, can be tested
(Gunga et al., 2007, 2008; Bates et al., 2009; Stoinski et al., in
press). Segment masses can also easily be obtained. Finally,
with photogrammetrical methods, measurement errors are
also partitioned and do not affect the entire estimate. In
mass estimated based on long bone circumference, on the
other hand, whenever a local measurement error occurs
(e.g. due to deformation during fossilization), the direct
result is that the total mass of the animal is calculated
incorrectly. A similar method is based on creating 3D skeletal
mounts from digitized bones, and using these instead of laserscanned mounts (Mallison, 2007, in press b). This allows easy
correction of errors in mounts and thus revisions.
Recent work by Wedel (2005) suggests that volume-based
estimates are generally too high because they are based on
a specific density in a living sauropod of 0.9–1 kg L−1 , as
in modern crocodilians. However, it is becoming generally
accepted that because of their extensively pneumatized axial
skeleton (Perry, 2001; Henderson, 2004; Wedel, 2003a, b,
2005, 2009; Schwarz & Fritsch, 2006) living sauropods
probably had a specific density of about 0.8 kg L−1 (Wedel,
2005), which is more like that of birds (0.73 kg L−1 ,
Hazlehurst & Rayner, 1992). Wedel (2005) accordingly
suggested that volume-based mass estimates published before
the modern consensus on pneumatized skeletons should be
reduced by about 10%.
A caveat to the tissue density of 0.8 kg L−1 given by
Wedel (2005), and a novel method for estimating body mass,
is offered by a recent allometric study on the dimensions
of semicircular canals (SCC) in the skull (Clarke, 2005).
Plotting SCC diameter of the Berlin specimen of Brachiosaurus
(recently assigned to a new genus, Giraffatitan, based on
numerous differences from the type species, B. altithorax;
Taylor, 2009) on a regression of SCC dimensions against
body mass in extant amniotes, Clarke (2005) found that
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
Biology of the sauropod dinosaurs
121
Table 1. Compilation of body mass estimates for selected sauropods from the literature. The table lists those species for which
reliable estimates are available because of abundant and complete fossil material and the largest valid sauropod species (in bold)
which are known from less complete material. It also intends to show the variation of estimates obtained by different methods
Taxon
Reference
Mass (kg)
Amargasaurus cazaui
Amphicoelias fragillimus
Anchisaurus sinensis
Antarctosaurus giganteus
Antarctosaurus wichmannianus
Antarctosaurus wichmannianus
Apatosaurus louisae
Apatosaurus louisae
Seebacher (2001)
Paul (1998)
Seebacher (2001)
Mazzetta et al. (2004)
Mazzetta et al. (2004)
Mazzetta et al. (2004)
Colbert (1962)
Anderson et al. (1985)
6853
90000–150000
84
69000
33410
24617
32420
30000–37500
Apatosaurus louisae
Apatosaurus louisae
Apatosaurus louisae
Apatosaurus louisae
Apatosaurus louisae
Alexander (1989)
Christiansen (1997)
Paul (1998)
Seebacher (2001)
Foster (2007)
34000–35000
19500
17500
22407
34035
Apatosaurus louisae (juvenile)
Foster (2007)
Apatosaurus louisae
Packard et al. (2009)
18000
Apatosaurus sp.
Erickson et al. (2001)
25952
Argentinosaurus huinculensis
Barosaurus lentus
Mazzetta et al. (2004)
Foster (2007)
72936
11957
Barosaurus sp.
Brachiosaurus altithorax
Brachiosaurus altithorax
Brachiosaurus altithorax
Seebacher (2001)
Paul (1998)
Seebacher (2001)
Foster (2007)
20040
35000
28265
43896
Brachiosaurus brancai
Brachiosaurus brancai
Brachiosaurus brancai
Janensch (1938)
Colbert (1962)
Anderson et al. (1985)
40000
78260
31600
Brachiosaurus brancai
Anderson et al. (1985)
29335
Brachiosaurus brancai
Brachiosaurus brancai
Brachiosaurus brancai
Brachiosaurus brancai
Brachiosaurus brancai
Alexander (1985)
Paul (1988)
Alexander (1989)
Christiansen (1997)
Gunga et al. (1999)
46600
45000–50000
47000
37400
74420
Brachiosaurus brancai
Brachiosaurus brancai
Mazzetta et al. (2004)
Gunga et al. (2008)
39500
38000
Brachiosaurus brancai
Packard et al. (2009)
16000
Camarasaurus grandis
Foster (2007)
18413
Camarasaurus grandis
Foster (2007)
9321
Camarasaurus lewisi
Camarasaurus supremus
Camarasaurus supremus
Cetiosaurus oxoniensis
Dicraeosaurus hansemanni
Seebacher (2001)
Christiansen (1997)
Mazzetta et al. (2004)
Mazzetta et al. (2004)
Christiansen (1997)
4254
11652
8800
9300
15900
5400
Method of mass estimate
polynomial volume
method not given
polynomial volume
regression analysis
regression analysis
regression analysis
scale model
long bone
circumference
scale model
scale model
method not given
polynomial volume
long bone
circumference
long bone
circumference
nonlinear regression
analysis
long bone
circumference
regression analysis
long bone
circumference
polynomial volume
method not given
polynomial volume
long bone
circumference
method not given
scale model
long bone
circumference
long bone
circumference
scale model
method not given
scale model
scale model
stereophotogrammetry
and laser scanning
of mounted skeleton
scale model
laser scanning of
mounted skeleton
nonlinear regression
analysis
long bone
circumference
long bone
circumference
polynomial volume
scale model
scale model
scale model
scale model
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
P. Martin Sander and others
122
Table 1. (cont.)
Taxon
Reference
Mass (kg)
Dicraeosaurus hansemanni
Gunga et al. (1999)
12800
Dicraeosaurus hansemanni
Diplodocus carnegii
Diplodocus carnegii
Mazzetta et al. (2004)
Christiansen (1997)
Foster (2007)
5700
15200
12657
Diplodocus carnegii
Foster (2007)
12000
Diplodocus sp.
Diplodocus sp.
Colbert (1962)
Anderson et al. (1985)
10560
5000–15000
Diplodocus sp.
Henderson (1999)
13421
Diplodocus sp.
Packard et al. (2009)
4000
Euhelopus zdanskyi
Europasaurus holgeri
Paul (1997b)
Stein, unpublished data
3800
690
Haplocanthosaurus delfsi
Foster (2007)
21000
Haplocanthosaurus priscus
Foster (2007)
10500
Haplocanthosaurus sp.
Haplocanthosaurus sp.
Janenschia sp.
Paul (1997b)
Seebacher (2001)
Lehman & Woodward (2008)
12800
14529
14029
Lufengosaurus huenei
Magyarosaurus dacus
Seebacher (2001)
Stein, unpublished data
Mamenchisaurus hochuanensis
Mamenchisaurus hochuanensis
Mamenchisaurus hochuanensis
Massospondylus sp.
Omeisaurus tianfunensis
Omeisaurus tianfunensis
Omeisaurus tianfunensis
Opisthocoelicaudia skarzynskii
Christiansen (1997)
Seebacher (2001)
Mazzetta et al. (2004)
Seebacher (2001)
Christiansen (1997)
Seebacher (2001)
Mazzetta et al. (2004)
Anderson et al. (1985)
14300
18170
15100
137
9800
11796
9800
22000
Opisthocoelicaudia skarzynskii
Opisthocoelicaudia skarzynskii
Opisthocoelicaudia skarzynskii
Paul (1997b)
Seebacher (2001)
Packard et al. (2009)
8400
10522
13000
Paralititan stromeri
Patagosaurus sp.
Plateosaurus engelhardti
Plateosaurus engelhardti
Burness et al. (2001)
Seebacher (2001)
Seebacher (2001)
Gunga et al. (2007)
59000
9435
1073
630–912
Riojasaurus sp.
Sauroposeidon proteles
Seismosaurus halli
Seismosaurus halli
Seismosaurus hallorum
Shunosaurus lii
Shunosaurus lii
Shunosaurus lii
Supersaurus vivianae
Thecodontosaurus antiquus
Ultrasauros macintoshi
Seebacher (2001)
Wedel et al. (2000a)
Gillette, (1994)
Seebacher (2001)
Foster (2007)
Christiansen (1997)
Seebacher (2001)
Mazzetta et al. (2004)
Foster (2007)
Seebacher (2001)
Paul (1998)
3039
50000–60000
100000
49276
42500
3400
4793
3600
40200
25
45000–50000
1193
900
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
Method of mass estimate
stereophotogrammetry
and laser scanning
of mounted skeleton
scale model
scale model
long bone
circumference
long bone
circumference
scale model
long bone
circumference
3-D mathematical
slicing
nonlinear regression
analysis
scale model
long bone
circumference
long bone
circumference
long bone
circumference
scale model
polynomial volume
long bone
circumference
polynomial volume
long bone
circumference
scale model
polynomial volume
scale model
polynomial volume
scale model
polynomial volume
scale model
long bone
circumference
scale model
polynomial volume
nonlinear regression
analysis
method not given
polynomial volume
polynomial volume
laser scanning of
mounted skeleton
polynomial volume
method not given
method not given
polynomial volume
method not given
scale model
polynomial volume
scale model
method not given
polynomial volume
method not given
Biology of the sauropod dinosaurs
123
Sauropoda
Theropoda + Ornithischia
Mammalia
Count
100
10
1
10−1
5x10−1
101
5x101
102
5x102
103
5x103
104
5x104
105
Size classes (kg)
Fig. 2. Comparison of body masses of sauropod dinosaurs, theropod and ornithischian dinosaurs and mammals. The mass data
for sauropods are found in Table 1, while those for the other dinosaurs are primarily from Seebacher (2001) with additional data
from Christiansen (1997) and Anderson et al. (1985). The data for mammals were compiled from Janis & Carrano (1992), Fortelius
& Kappelman (1993), and Spoor et al. (2007). With the exception of the two largest forms they represent extant mammals only.
Mammals show a strongly right-skewed distribution, theropods and ornithischians show intermediate masses, and sauropods show
a strongly left-skewed distribution. Not that the y-axis is logarithmic.
the dimensions of the posterior SCC are consistent with a
body mass of about 75 t, while the anterior SCC suggests a
higher mass and the lateral SCC a lower mass. At 30–50 t,
the most recent volume-based estimates for this individual
are considerably lower (Seebacher, 2001; Gunga et al., 2008).
A higher tissue density than 0.8 kg L−1 would result in higher
body mass estimates and thus would be more consistent with
the results of Clarke (2005).
(4) Unique body size of sauropods and theropods
Dinosaurs have long been associated with extraordinary body
size (Dodson, 1990), and estimates of maximal dinosaurian
body size have received more than passing attention.
Partially this is because of the innately human interest
in identifying the largest ever representative of a group
(Owen-Smith, 1988), which sometimes led to exaggerated
claims of body mass for dinosaurs and fossil mammals
(Fortelius & Kappelman, 1993). However, only recently
has it been realized that two groups stand out among the
dinosaurs from an ecological perspective, the Theropoda
and the Sauropoda. While other studies (Janis & Carrano,
1992; Farlow, 1993; Paul, 1994, 1997b, 1998; Alexander,
1998) addressed this issue, that of Burness, Diamond &
Flannery (2001) is most to the point. Regressing land mass
size against body mass of the largest species inhabiting the
land mass (top species) for recent and Pleistocene terrestrial
tetrapods, Burness et al. (2001) observed that there is close
correlation between these two variables when trophic level
(herbivory versus carnivory) and metabolism (bradymetabolic
ectothermy versus tachymetabolic endothermy) are taken
into account (Fig. 3). The study included top species on land
masses ranging from small oceanic islands of a few square
kilometers in size to continents as large as Asia.
When adding the largest herbivorous and carnivorous
dinosaurs then known to their dataset (Fig. 3), the estimated
body masses of these species were an order of magnitude
greater than predicted by the ectotherm regressions for
the land mass they inhabited (Burness et al., 2001).
The largest herbivores in the study all belonged to
Sauropoda (Sauroposeidon, Argentinosaurus, Paralititan) and the
largest carnivores to Theropoda (Tyrannosaurus, Giganotosaurus,
Charcharodontosaurus). Specifically, the theropods were an
astounding 12 times heavier than predicted by the
regression equations for extant ectotherms, and the difference
for sauropods is also remarkable (1.5–3 times heavier
than predicted). If both of these dinosaur groups were
tachymetabolic endotherms, as we will argue below, the gap
between prediction and observation is even larger. In fact,
the magnitude of the gap led Burness et al. (2001) to suggest
that dinosaurs must have been ectothermic. As predicted
from energy loss between trophic levels (Burness et al., 2001;
Owen-Smith & Mills, 2008), the largest herbivores, the
sauropods, are an order of magnitude larger than the largest
carnivores (Fig. 3).
(5) Cope’s Rule in Sauropodomorpha and selective
advantages of large body size
Sauropodomorpha, as an evolutionary lineage, started out
with small animals of 101 kg body mass (BM), such as
Saturnalia (Langer et al., 1999) and Panphagia (Martinez &
Alcober, 2009) from the Carnian (early Late Triassic), from
which the later giants with a BM of 105 kg evolved. This
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
P. Martin Sander and others
124
Table 2. Selective advantages and disadvantages of larger body
size based on a compilation by Hone & Benton (2005)
Benefits of larger body size
-
Increased defence against predation
Increase in predation success
Greater range of acceptable foods
Increased success in mating
Increased success in intraspecific competition
Increased success in interspecific competition
Extended longevity
Increased intelligence (with increased brain size)
At very large size, the potential for thermal inertia
Survival through lean times and resistance to climatic variation
and extremes
Problems caused by larger body size
Fig. 3. Body mass of the largest species inhabiting a land mass
regressed against the size of the land mass in extant and Late
Pleistocene terrestrial amniotes. The species are grouped by
metabolism (bradymetabolic ectothermy versus tachymetabolic
endothermy) and trophic level (herbivores versus carnivores).
The two outliers of endothermic herbivores are island dwarf
elephants. The largest species were ectothermic herbivores on
only three land masses, precluding regression analysis of this
group. Note that maximum body mass for a given land mass
decreases with increasing metabolic rate and trophic level. Fossil
mammal taxa adhere to the regressions while sauropod and
theropod dinosaurs do not, being much larger than predicted.
See text for details. Redrawn from Burness et al. (2001).
profound evolutionary body size increase over four orders of
magnitude begs the question of the applicability of Cope’s
Rule (Polly, 1998; Hone & Benton, 2005; Hone et al., 2005;
Carrano, 2006). In its most general formulation, Cope’s
Rule posits that body size tends to increase in evolutionary
lineages over time, while more stringent versions either call
for a general shift in average body size in a lineage from
smaller to larger or for a general spread in the range of body
sizes as evolutionary time progresses.
Bonner (2006) offered a rather simple (if not simplistic)
explanation for Cope‘s Rule in its most general form, i.e.
that as life diversifies, there is always room for body size to
expand in one direction: to the top. As habitat is partitioned
and ecospace becomes crowded, one way out is evolution
towards larger body size (Bonner, 2006). However, this
works only if body size in the specific evolving lineage has
not yet met the physical limits of its bauplan and if the
ecological carrying capacity allows for long-term survival
of the population. Furthermore, Bonner‘s (2006) hypothesis
only accounts for the increase in size range, but not for a
general shift towards larger average body size—which is
what happened in the sauropod lineage, in which even small
taxa are one order of magnitude larger than their basal
sauropodomorph ancestors.
Cope’s Rule has been discussed controversially in the past,
and its validity has not been universally accepted (Polly, 1998;
-
Increased vulnerability to predation
Increased development time (both pre- and postnatal)
Increased demand for resources
Increased extinction risk because of:
- Longer generation time gives a slower rate of evolution,
reducing the ability to adapt
- Lower abundance (i.e. small genetic pool, also reduces
ability to adapt)
- Lower fecundity through reduced number of offspring
Blankenhorn, 2000; Alroy, 1998, 2000; Knouft & Page, 2003;
Moen, 2006). This discussion is not the focus of this review,
but we obtain from it hypothesized selective advantages that
drive body size evolution towards a larger average (Stanley,
1973; Clutton-Brock & Harvey, 1983; Blankenhorn, 2000;
Hone & Benton, 2005; Table 2).
For herbivores the most important of these selective advantages (Table 2) is generally believed to be that larger body size
decreases predation pressure. Strong evidence for this view
was published most recently by Owen-Smith & Mills (2008).
Two factors, the energy loss from one trophic level to the
next and large size as predation protection, provide an explanation of why in modern terrestrial ecosystems the largest
mammalian herbivores are an order of magnitude larger
than the largest mammalian carnivores (Burness et al., 2001).
This is also the case in most dinosaur faunas in which the
largest herbivore (generally a sauropod) is an order of magnitude larger than the largest predator, a theropod. Theropod
body size thus may have been limited by sauropod body size.
As sauropods reached a certain body size maximum, e.g.
dictated by land mass size, so would theropods.
On the other hand, with predation pressure potentially
being the dominant force driving evolutionary body size
increase in herbivores, limitations to theropod body size
other than prey availability (e.g. biomechanical limits to
their bipedal body plan) may have affected maximum body
size in sauropods. Once sauropods had evolved to a body
size sufficient to protect them from theropod predation,
their evolutionary size increase might have come to a halt
because of the selective disadvantages of large body size
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
Biology of the sauropod dinosaurs
(Table 2). Studies of African savannah ecosystems (OwenSmith & Mills, 2008) suggest that the abundance of the
largest herbivores, i.e. elephants, is limited by food abundance, not by predation pressure. Sauropods in the Late
Jurassic Morrison Formation ecosystem are also hypothesized to have been food-limited. Through their capacity for
outcompeting smaller animals in access to food and their
relative immunity to predation, elephants may also limit
the abundance of smaller herbivores and the trophic energy
available for carnivores (Hummel & Clauss, 2008; OwenSmith & Mills, 2008). If these observations were to apply
to herbivory-based ecosystems in general, understanding
sauropod biology and gigantism would hold the key to understanding Late Triassic to Cretaceous terrestrial ecosystems in
general.
(6) Diversity of the Sauropoda
Sauropod dinosaurs were a highly diverse group with over 90
valid genera known in 2005 (Upchurch & Barrett, 2005). New
species are constantly being found (e.g. Bonitasaura salgadoi
Apesteguía, 2004; Brachytrachelopan mesai Rauhut et al., 2005;
Puertasaurus reuili Novas et al., 2005; Turiasaurus riodevensis
Royo-Torres, Cobos & Alcalá, 2006; Futalognkosaurus dukei
Calvo et al., 2007; Daxiatitan binglingi You et al., 2008;
Spinophorosaurus nigerensis Remes et al., 2009). The current tally
is at 175 genera and approximately 200 species (Mannion
& Upchurch, in press a, b), making the Sauropoda the most
diverse of all major dinosaurian herbivore groups. They
are also the longest-lived dinosaurian herbivore group, with
the first sauropods being found in the Late Triassic (Yates
& Kitching, 2003) and the last in the latest stages of the
Maastrichtian (see Upchurch, Barrett & Dodson, 2004).
Sauropods are known from all continents, including a first
record from Antarctica (Smith & Pol, 2007). The recent
finds reveal a remarkable diversity in body plans and feeding
adaptations (Apesteguía, 2004; Rauhut et al., 2005; Sereno
et al., 2007) which, together with the fragmentation of Pangea
during the Jurassic and Cretaceous, may be responsible for
the diversity increase through time.
Sauropods remain rare in the Lower Jurassic of China
and South Africa, the only regions that have yielded an
extensive terrestrial fossil record for this time interval. Until
recently, it was believed that sauropod dinosaurs had their
greatest diversity and ecological impact in the Late Jurassic
and afterwards started to decline, becoming rare in the
Late Cretaceous (Dodson, 1990; Weishampel & Norman,
1989). However, as dinosaur research entered the global
age, it became apparent that this is a view centered on
North America, and current discoveries suggest that many
terrestrial ecosytems were dominated by sauropods to the
very end of the Cretaceous.
(7) Sauropodomorph phylogeny and evolution
The prerequisite for all enquiries into the evolution of body
size, and gigantism in particular, are robust phylogenetic
hypotheses (see Gould & MacFadden, 2004). These have
125
only become available for sauropods in the last 15 years,
through the work of J.A. Wilson (Wilson, 2002, 2005;
Wilson & Upchurch, 2009; see also Wilson & Sereno, 1998),
P. Upchurch (Upchurch et al., 2004; see also Upchurch,
1995, 1998, 1999), and K. Curry Rogers on titanosaurs
(Curry Rogers, 2005; see also Salgado, Coria & Calvo,
1997). These hypotheses largely agree on the general aspects
of sauropod phylogeny (Fig. 4) with a consensus now having
been reached (Wilson & Upchurch, 2009). Also, Taylor et al.
(in press) define Sauropoda as all taxa closer to Saltasaurus
than to Melanorosaurus, and hopefully this definition will lead
to some systematic stability.
Recent discoveries (Buffetaut et al., 2000, 2002) and
phylogenetic work (Upchurch, Barrett & Galton, 2007a;
Upchurch et al., 2007b; Yates, 2007) reveal a number of
taxa more basal than the traditionally recognized most basal
sauropod Vulcanadon from the Lower Jurassic of Zimbabwe.
However, the earliest evidence for a fully graviportal stance
is only seen in cf. Isanosaurus from the Rhaetian of Thailand
(Buffetaut et al., 2002). Other basal taxa are Kotasaurus and
Barapasaurus from the Lower Jurassic of India, Shunosaurus
from the Middle Jurassic of China, and Spinophorosaurus from
the Middle Jurassic of North Africa (Fig. 4). One particular
clade of basal sauropods, the Mamenchisauridae (Fig. 4),
seem to be an endemic, or near-endemic eastern Asian
radiation (Russell, 1993; Upchurch, Hunn & Norman, 2002;
Rauhut et al., 2005; Wilson, 2005; Wilson & Upchurch, 2009)
and include the sauropods with the relatively longest necks,
such as Omeisaurus and Mamenchisaurus.
Advanced sauropods form a monophyletic clade called
Neosauropoda (Upchurch, 1995, 1998; Wilson & Sereno,
1998; Wilson, 2002, 2005; Upchurch et al., 2004; Harris,
2006), which is divided into two main lineages, the
Diplodocoidea and the Macronaria (Fig. 4). Diplodocoids
include the bizzarre rebbachisaurids (Lavocat, 1954; Calvo &
Salgado, 1995; Sereno et al., 1999, 2007) and dicraeosaurids
(Janensch, 1914; Salgado & Bonaparte, 1991; Rauhut et al.,
2005) as well as the familiar diplodocids (Marsh 1884;
Hatcher, 1901; Gilmore, 1936; Upchurch et al., 2004)
(Fig. 4). Whereas rebbachisaurids are so far only known from
the Cretaceous, both dicraeosaurids and diplodocids appear
in the Late Jurassic. Unequivocal records of diplodocids
are not known from sediments younger than the latest
Jurassic, whereas dicraeosaurids are still found in the
Early and, possibly, the earliest Late Cretaceous (Stromer,
1932; Salgado & Bonaparte, 1991; Rauhut, 1999), and
rebbachisaurids might have survived until the later stages of
the Late Cretaceous (Sereno et al., 2007). Macronarians are
the most successful clade of sauropods (Fig. 4) and include the
Late Jurassic Camarasaurus (e.g. Osborn & Mook, 1921), the
Brachiosauridae (e.g. Brachiosaurus and Cedarosaurus), which
flourished from the Late Jurassic to the Early Cretaceous
(Riggs, 1903; Janensch, 1914; Wedel et al., 2000b, Upchurch
et al., 2004) but may not be a natural grouping, and
the titanosaurs, the most diverse and widespread clade of
Cretaceous sauropods (Curry Rogers, 2005).
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
126
P. Martin Sander and others
Fig. 4. Simplified sauropod phylogeny compiled from Wilson (2002), Upchurch et al. (2007a), Yates (2007), Allain & Aquesbi (2008),
and Remes et al. (2009). Only well-known taxa whose position in the phylogeny is relatively stable are shown. Arrows indicate
stem-based taxa, and dots indicate node-based taxa.
Titanosaurian anatomy is still poorly understood because
most taxa are only known from a single or a few incomplete
skeletons each and have not been studied in sufficient detail.
Titanosaurs differ in several aspects of their locomotor
apparatus from more basal sauropods, including their more
widely spaced legs, documented by anatomical features and
so-called ‘wide-gauge’ trackways (Wilson, 2005). A basal
titanosaur known from abundant material is Phuwiangosaurus
from the Lower Cretaceous of Thailand. Typical derived
titanosaurs are Rapetosaurus from the latest Cretaceous
of Madagascar (Fig. 4) and Alamosaurus from the latest
Cretaceous of the southwestern USA.
II. BAUPLAN AND BIOLOGY OF SAUROPOD
DINOSAURS
We focus on those aspects of the sauropod bauplan and
biology that are potentially informative on the gigantism
issue. When describing the bauplan of a group like the
sauropods, it is important to acknowledge that the consistency
we observe in one organ system (e.g. the skeletal system with
a generally ‘characteristic’ design) need not necessarily imply
that other organ systems were of similar consistency across
the species described. A good example for this, among the
mammals, is provided by the primates which are a clearly
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
Biology of the sauropod dinosaurs
defined group with a comparatively uniform skeletal bauplan,
yet exhibiting an extreme variety of digestive tract designs,
including both foregut- and hindgut fermentation (Chivers
& Hladik, 1980).
(1) Bauplan and skeletal anatomy
The sauropod body plan is unique among terrestrial
tetrapods: a body superficially similar to that of proboscideans
(elephants) among mammals is combined with a very small
head on a very long neck and a tail, considerably exceeding
those of other dinosaurs in relative (and absolute) length (Figs
1, 5). The small and light-weight skull is biomechanically
linked to the long neck because of the leverage exerted by
the head on the neck (Witzel & Preuschoft, 2005; Witzel,
2007; Witzel et al., in press).
All sauropods were quadrupedal, graviportal animals with
massive, columnar limbs supporting the body (Fig. 5). The
fossil record suggests that the optimization of the forelimb
towards a fully erect, parasagittally-swinging column was not
an exaptation that allowed gigantism, but evolved in parallel
(Remes, 2008), and that this parallel evolution was necessary
for sauropods to attain a multi-tonne body mass.
With the exception of the basal macronarians Brachiosaurus
(Fig. 5), and Cedarosaurus, the hindlimbs were considerably
longer in sauropods than the forelimbs, and in all sauropods
bore the greater part of the body weight (Alexander, 1985,
1989). The proximal limb elements (humerus and femur)
were distinctly longer than the lower limb bones. The
metacarpus was arranged in a vertical semicircle (Bonnan,
2003), while the pes was semi-digitigrade. The feet probably
bore a soft heel pad, like in modern elephants, as indicated
by the extensive sauropod footprint record. The toes are
reduced, or at least short. The rough and pitted articular
surfaces of the long bones indicate thick cartilage caps
around the major joints, which was recently confirmed by
Fig. 5. The sauropod body plan and body size. The
reconstruction of Brachiosaurus brancai (recently renamed
Giraffatitan, see Taylor, 2009) is based on the mounted skeleton
in the Natural History Museum Berlin. Sauroposeidon from the
Lower Cretaceous of Oklahoma (USA), one of the recently
described truly gigantic sauropods, is only known from a string
of four neck vertebrae. Based on these, the animal can be
estimated to have been about 30% larger in linear dimension
than the Berlin Brachiosaurus. Modified from Wedel et al. (2000b).
127
the fossilized remains of such a cap (Schwarz, Wings &
Meyer, 2007d). Since the exact thickness and shape of the
articular cartilage is not known and the range of motion of
most limb joints is less easily constrained than in mammals,
biomechanical analyses of sauropod locomotion are less
precise than in mammals.
The trunk was short and deep. Characteristic of sauropods
are the elongated pedicels of the vertebral arches (Upchurch
et al., 2004). This is a biomechanical adaptation to the statics
of a long body stem, which is supported by two pairs of
limbs, which are placed close together. Thus the bending
moments produced by the weight of the body are ‘‘positive’’
(dorsally convex) along the full length of the trunk, and
dorsal tension-resisting structures like muscles and ligaments
are permanently stressed. A long distance between muscles
and centra (= lever arm), which is provided by the long
pedicels, reduces the forces that act along the body axis.
This results in energy savings for the dorsal musculature and
less substance and thus less weight for the vertebral bodies
(Preuschoft, 1976).
Whereas sauropod limbs contained massive bones, their
presacral vertebrae were a marvel of lightly constructed
lamina systems (Osborn 1899; Janensch, 1929a; Wilson,
1999). With most of the weight being carried by the
hindlimbs, the number of sacral vertebrae and thus the bony
connection between the limbs and the vertebral column
increased during sauropod evolution, from three sacrals in
basal sauropodomorphs, to four in basal sauropods, five
in most sauropods, and finally six sacral vertebrae in some
titanosaurs (Wilson & Sereno, 1998; Wilson, 2002; Upchurch
et al., 2004). In contrast to most older illustrations and skeletal
mounts of sauropods, osteology indicates that tail was held
clear off the ground (Figs 1, 5), consistent with the lack of tail
drag marks in sauropod trackways (Lockley, 1991).
The elongation of the neck involves both the elongation
of single vertebrae as well as an increase in the total
number of cervical vertebrae (up to 19 in Mamenchisaurus),
which happened independently in several lineages. With
the exception of brachiosaurid and probably camarasaurid
and titanosaur sauropods, the long neck appears to have
been held horizontally or slightly curved up when inactive.
The long tail was crucial as a counterbalance during neck
movements.
Smaller sauropods such as the Dicraeosauridae appear
to have relatively shorter necks than the larger forms, and
strongly positive interspecific allometry of neck length was
found by Parrish (2006) for sauropodomorphs in general.
Senter (2007), on the other hand, found no correlation
between limb length and neck lenght in a sample of eleven
sauropod taxa, probably because of the smaller sample
size than that of Parrish (2006). Where it is known from
ontogenetic series, juveniles have relatively shorter necks
than adults, e.g. in Camarasaurus and Diplodocidae (Britt &
Naylor, 1994; Ikejiri, Tidwell & Trexler, 2005; Schwarz et al.,
2007b). Such a positive intraspecific allometry of neck length
is also seen in the basal sauropodomorph Massospondylus
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
128
(Reisz et al., 2005), in which the embryos have a relatively
much shorter neck than the adults.
The long necks of sauropods (Fig. 5) are either interpreted
as a means for high browsing (e.g. Bakker, 1987; Paul,
1987, 1998) or for increasing the horizontal feeding range
(e.g. Martin, 1987; Mateus, Maidment & Christiansen,
2009; Seymour, 2009a, Preuschoft et al., in press). Possibly,
different species employed different feeding strategies (e.g.
Dodson, 1990; Dzemski & Christian, 2007). This assumption
is supported by ecological considerations and by the diversity
in jaw and tooth morphology (e.g. Upchurch & Barrett,
2000; Sereno & Wilson, 2005). The neck posture of some
of the largest forms, especially Brachiosaurus and its close
relatives, is the subject of much controversy (Martin, 1987;
Paul, 1998; Stevens & Parrish, 1999, 2005a, b; Seymour
& Lillywhite, 2000; Christian, 2002; Berman & Rothschild,
2005; Dzemski & Christian, 2007; Christian & Dzemski,
2007, in press; Sereno et al., 2007; Sander, Christian &
Gee, 2009; Seymour, 2009a, b; Taylor, Wedel & Naish,
2009; Christian & Dzemski, in press). For Brachiosaurus, the
suggested neck posture differs between horizontal (Stevens
& Parrish, 2005a, b) and nearly vertical (e.g. Janensch, 1950;
Paul, 1988; Christian & Heinrich, 1998; Christian, 2002).
Sauropods probably employed different neck postures during
different activities, like feeding, locomotion and standing at
rest, so that reconstructions of neck postures can differ due to
different approaches used for the reconstruction (Christian
& Dzemski, 2007, in press; Dzemski & Christian, 2007).
Recent work (Christian & Dzemski, 2007, in press;
Dzemski & Christian, 2007; Taylor et al., 2009) indicates
that the mobility of sauropod necks was underestimated by
earlier studies (Stevens & Parrish, 1999, 2005a, b). Feeding
over a large volume (the ‘feeding envelope’) was possible
even if browsing was restricted by neck position to medium
heights. In any case, the long necks of sauropods allowed
them to feed not only at heights out of reached of other
herbivores, but also over a large volume without moving the
massive body.
The extensive sauropod trackway record potentially will
inform us on the issue of the habitual neck position. Sauropod
trackways always show much larger pes prints than manus
prints, and the pes prints are more deeply impressed
(Thulborn, 1990; Lockley & Meyer, 2000; Wright, 2005),
indicating that most of the body weight was carried on
the hindlimbs. This appears inconsistent with a horizontally
held neck which would exert considerable leverage on the
front limbs, necessitating larger feet and resulting in deeper
imprints than observed, while this leverage would be much
reduced if the neck were held more erect, consistent with the
small and shallow manus prints. An in-depth review of the
controversial neck position of sauropods is beyond the scope
of this paper.
(2) Musculature reconstruction and locomotor
evolution
Osteological correlates of muscles and tendons, combined
with comparative work in birds and crocodiles using the
P. Martin Sander and others
extant phylogenetic bracket approach, allow reasonably
reliable reconstructions of musculature and its evolution.
Applied to the limb musculature, such work (Remes, 2006,
2008; Fechner, 2009; Rauhut et al., in press) leads to a
deeper understanding of the musculoskeletal (and therefore
biomechanical) design of the sauropod locomotory apparatus
and its evolution. In the forelimb, a change from an adductordriven to an abductor-driven locomotory system took place
at the base of the Sauropoda (Remes, 2008a; Rauhut et al.,
in press), while the same evolutionary change had already
occurred at the base of the Dinosauria in the hindlimb
(Fechner, 2009).
In contrast to mammals, sauropods retained the primitive
condition of the caudofemoralis musculature as the
main propulsive muscle in locomotion (Gatesy, 1990). In
comparison to other archosaurs, the attachment area of
this muscle is more distally placed, thus trading torque for
increased lever arm length, clearly an adaptation to giant
size. While the reconstruction of other parts of the sauropod
musculature may bear on the issue of their unique gigantism,
such work is still in its early stages.
(3) Locomotion: gait and speed
Biomechanical calculations indicate that the large size of
sauropods limited them to certain gaits, excluding the
possibility of running, i.e. a gait with a suspended phase.
Also, the extremely posterior position of the centre of mass
in some groups (e.g. diplodocids) induces strong lateral
moments during leg retraction that must be countered in
the forelimbs. This must have made pacing and other
gaits impossible in which the contralateral forelimb to
the currently propelling hindlimb is protracted. In a walk,
travelling speeds of 5.4–8.6 km h−1 were calculated on the
basis of strictly pendulous, non-muscle-powered movements
of the limbs (Preuschoft et al., in press). Top speeds of nearly
20 km h−1 appear possible based on preliminary computeraided engineering (CAE) modeling (Mallison, in press b).
Sauropods are similar in their limb design to elephants, with
sturdier sauropods having similar, or even slightly greater,
strength indicators to extant proboscideans (Alexander,
1985). This indicates that they were comparably athletic.
Since elephants can move at speeds of up to 35 km h−1
(Hutchinson et al., 2006), we must assume that similarly sized
sauropods achieved similar speeds, while larger animals with
equal strength indicators were even faster.
The track record indicates that sauropods usually
progressed at slow speeds (Thulborn, 1990; Christiansen,
1997; Lockley & Meyer, 2000), with estimates from trackways
ranging from about 2 to 7 km h−1 (Thulborn, 1990; Mazzetta
& Blanco, 2001). The average speed seems to have been
below 2 km h−1 . Faster locomotion might rarely have been
recorded because a soft, sometimes slippery surface that
might preserve footprints is not the kind of substratum a
graviportal animal would run on.
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
Biology of the sauropod dinosaurs
(4) Integument
Limited evidence exists for the structure of the integument in
sauropods. Carbonized skin remains of diplodocid sauropods
indicates that their skin was covered by a mosaic pattern of
non-imbricating scales (Czerkas, 1994; Ayer, 2000), and
the same was obviously also true for other sauropods
(Mantell, 1850; Upchurch, 1995; Rich et al., 1999). Along
the dorsal midline, at least some of these animals sported
a row of triangular skin flaps, probably serving display
purposes (Czerkas, 1994). In titanosaurs, the skin additionally
contained osteoderms (Upchurch et al., 2004; Le Loeuff,
2005). Such a skin structure with a mosaic of scales is also
seen in embryonic titanosaurid sauropods from Argentina
(Chiappe et al., 1998; Coria & Chiappe, 2007), which lack any
indication of insulating structures to cover the naked skin.
(5) Respiratory system
Sauropods are characterized by a dorsally placed, paired
or unpaired bony narial opening which traditionally has
been equated with fleshy nostrils in the same dorsal position.
However, Witmer (2001) argues convincingly for far rostrally
placed fleshy nostrils and a complex narial aparatus that
may have improved heat exchange between air and blood
stream. Based on palaeoneurological studies (Knoll, Galton
& López-Antoñanzas, 2006), there is no evidence for the
proboscis-like structure hypothesized by Bakker (1986), a
conclusion reached earlier by Barrett (1994), Upchurch
(1994), and Upchurch & Barrett (2000) based on jaw
mechanics and tooth wear.
Much of the axial skeleton, sometimes even including the
ribs, was strongly pneumatized (Henderson, 2004; Wedel,
2005, 2007, 2009; Schwarz, Frey & Meyer, 2007a), with
pneumatization moving gradually backwards along the
skeleton during sauropod evolution. In the most derived
sauropods, it even invaded the tail vertebrae and the ischia.
A consensus has recently emerged that this pneumatization
indicates the presence of an avian-style flow-through lung
and large airsacs in the body cavity of sauropods (Perry &
Reuter, 1999; Wedel, 2005, 2009; O’Connor, 2009; Perry,
Breuer & Pajor, in press). The same appears to have been
the situation in theropods (O’Connor & Claessens, 2005;
O’Connor, 2009) and thus must have evolved in the most
basal saurischians, although the evidence for an avian-style
respiratory system in basal sauropodomorphs is inconclusive
(Wedel, 2007, 2009). Although a secondary hard palate is
lacking in sauropods, some sort of fleshy folds must have
been present that prevented food from entering the nostrils
(Leahy, 2000), as in birds.
The bird-type lung would also have been advantageous in
overcoming the problem of tracheal dead space caused by the
very long trachea of sauropods (Perry, 1983, 1989; Daniels
& Pratt, 1992; Calder, 1996; Hengst et al., 1996; Paladino,
Spotila & Dodson, 1997; Paul, 1998; Wedel, 2003b; Perry
et al., in press). In fact, in some birds such as swans—a
group already with a long neck—the trachea makes an
extra loop against the breast bone before it enters the body
129
cavity (McLelland, 1989), indicating that dead space does
not limiting tracheal length in the bird respiratory system.
(6) Dentition and digestive system
All sauropods appear to have been exclusively herbivorous
(Weishampel & Jianu, 2000; Upchurch & Barrett, 2000;
Barrett & Upchurch, 2005; Stevens & Parrish, 2005b).
However, recent finds (Bonitasaura salgadoi, Apesteguía, 2004;
Nigersaurus taqueti, Sereno & Wilson, 2005; Sereno et al.,
2007) reveal an unexpected diversity of dentitions (Barrett
& Upchurch, 2005), beyond the long-known distinction
of pencil-shaped teeth restricted to the front of the snout
in diplodocoids and titanosaurs versus the more massive
dentitions of spoon-shaped teeth with wear facets in basal
sauropods and basal macronarians (Sander, 1997; Upchurch
& Barrett, 2005). This variety of dental designs can
safely be assumed to reflect some degree of ecological
niche diversification (Bakker, 1986; Calvo, 1994; Stevens
& Parrish, 1999; Christiansen, 2000; Upchurch & Barrett,
2000, 2005). Furthermore, slight carbon isotope differences
found in different sauropod taxa support a certain degree of
niche partitioning or at least differences in dietary breadth
and/or habitat (Tütken, in press). As large herbivores,
sauropods must have relied on symbiotic gut microbes
(contra Ghosh et al., 2003), and their digestive tract must
have contained capacious fermentation chambers, probably
in the hindgut as in birds and herbivorous squamate
reptiles (Farlow, 1987; Hummel et al., 2008; Hummel &
Clauss, in press). The evidence for fermentative digestion
in sauropods consists of (a) phylogenetic bracketing that
indicates that symbiotic fermentation bacteria were the same
as in modern herbivorous birds and mammals, (b) all large
recent herbivores employ fermentative digestion, and (c)
the fact that sauropods would have needed to consume
impossibly large amounts of plant matter without it (Hummel
& Clauss, in press).
The food was gathered by shearing bites, nipping, or
branch-stripping (Fiorillo, 1998; Barrett & Upchurch, 2005;
Chatterjee & Zheng, 2005; Stevens & Parrish, 2005b).
Because fermentation rate depends on particle size and
the mastication capability of sauropods must have been
rather limited, a gastric mill has long been hypothesized
to serve in reducing plant particle size before fermentation.
Occasional finds of polished pebbles with sauropod skeletons
(e.g. Janensch, 1929b; Bird, 1985; Christiansen, 1996) were
taken as evidence for such a gastric mill, but comparative
and experimental work (Wings & Sander, 2007; Wings, 2007,
2009) on ostriches and other herbivorous birds indicates that
these pebbles are not the remains of an avian-style gastric
mill, leaving it uncertain whether and how sauropods reduced
particle size.
Coprolites could potentially provide information on
particle size, and data from faeces are extensively used in
animal nutrition studies (Udén & Van Soest, 1982; Fritz et al.,
2009). Although putative sauropod coprolites containing
grass phytoliths and many other plant remains have been
described from the latest Cretaceous of India (Ghosh et al.,
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130
2003; Prasad et al., 2005; Mohabey, 2005), their sauropod
affinity is difficult to establish (Mohabey, 2005; Sander et al.,
in press a). As putative sauropod gastric contents (Brown,
1935; Stokes, 1964; Bird, 1985) are no longer tenable (Ash,
1993; Sander et al., in press a), there is currently no direct
evidence on sauropod food and food processing.
Sauropods as herbivores were thus most similar to
extant herbivorous reptiles, but differ from herbivorous
birds in the apparent lack of a gastric mill, and from
ornithischian dinosaurs (which were exclusively herbivorous)
and herbivorous mammals in their lack of extensive
mastication. However, the data of Clauss et al. (2009) on
the relationship between particle size and retention time in
extant animals and those of Franz et al. (2009) for scaling of
gut contents show that sauropods could have compensated
for the lack of particle reduction by an increased retention
time (as already suggested by Farlow, 1987). Franz et al.
(2009) also concluded that the digestive system did not place
constraints on sauropod body size.
(7) Circulatory system
The circulatory system has few osteological correlates.
However, aspects of the circulatory system of sauropod
dinosaurs have received considerable attention, especially in
conjunction with the position of the neck and blood pressure
problems associated with it (Kermack, 1951; Badeer &
Hicks, 1996; Seymour, 1976, 2009b; Seymour & Lillywhite,
2000; Gunga et al., 2008; Ganse et al., in press; review in
Alexander, 2006). Phylogenetic bracketing (Witmer, 1995)
and physiological arguments suggest that all dinosaurs had
a four-chambered heart with a complete separation of
pulmonary and body blood (Seymour, 1976; Paladino et al.,
1997; Gunga et al., 1999; Seymour & Lillywhite, 2000) and,
thus, were able to generate the blood pressure necessary
to supply the brain in a raised head with blood. However,
some researchers have argued that no sauropod would have
been able to hold the neck upright habitually because of
the very high blood pressure required which would damage
the arterial tissue and also the brain if the sauropod ever
were to lower its head (Choy & Altmann, 1992). These
arguments do not take into account hypothetical soft tissue
structures (Badeer & Hicks, 1996; Ganse et al., in press) such
as a rete mirabile (Colbert, 1993) or hypertrophied cardiac
and arterial structures, which could have served to ensure
an adequate supply of blood to the brain at a minimum
energetic cost, as is seen in giraffes (Mitchell & Skinner,
2009). Some suggestions of hypothetical soft tissue structures
appear exaggerated and are untestable, however, such as the
presence of seven additional hearts along the neck (Choy
& Altmann, 1992)—a structure unknown from all extant
vertebrates. In sauropods that held the neck high, the heart
must have been extraordinarily large to supply the head with
blood (Seymour, 1976, 2009b).
P. Martin Sander and others
(8) Nervous system and sense organs
Some aspects of the central nervous system are accessible
to palaeontological investigation because it has distinct
osteological correlates, such as an ossified brain case and
the neural canal of the vertebrae. Most recently, growth
marks in dentine have also been used to infer characteristics
of the nervous system (Appenzeller et al., 2005).
Endocasts indicate that the brain of sauropods was small
(Janensch, 1935–36; Jerison, 1969, 1973; Hopson, 1977,
1979; Knoll et al., 2006) and not very highly developed
(e.g. Chatterjee & Zheng, 2005). However, although the
brain of sauropods was often said to be extraordinarily
small, it actually falls within the allometric regression for
a reptile of this size (Hopson, 1979). Boundaries between
individual parts of the brain are often only poorly defined
in available endocasts (e.g. Osborn, 1912; Osborn & Mook,
1921; Janensch, 1935–36; Hopson, 1979), indicating that
the braincase was only partially filled by the brain, which
was cushioned by connective and fat tissues, as in modern
reptiles (Hopson, 1979). Most sauropods have a pronounced,
tapering dorsal process over the cerebral hemispheres,
which was interpreted as a parietal organ by some authors
(Janensch, 1935–36), but an interpretation as an unossified
zone or enlarged cerebral blood vessel seems to be more
likely (Hopson, 1979). The pituitary gland seems to have a
positive allometric relationship with body size and is thus
very large in sauropods (Edinger, 1942).
Recently, Clarke (2005) studied in detail the vestibular
labyrinth of Brachiosaurus brancai from Tendaguru, already
described by Janensch (1935–36). The dimensional analysis
of the labyrinth showed that body mass and the average
semicircular dimensions of Brachiosaurus brancai generally fit
with the allometric relationship found in previous studies
of extant species. Most remarkable was that the anterior
semicircular canals were found to be significantly larger than
the allometric relationship would predict. Therefore Clarke
(2005) hypothesized a greater sensitivity of the organ, which
can be interpreted in a further step as slower pitch movements
of the head in this direction, and most likely a flexion of the
neck, rather than a head pitching about the atlas joint. These
suggestions are supported by the most recent studies on the
neck and head posture of Brachiosaurus brancai by Christian
& Dzemski (2007; see also Dzemski & Christian, 2007).
Semicircular canal arrangement also indicates the habitual
pose of the head, from sligthly tilted upwards in prosauropods
to horizontal in Camarasaurus, and increasingly downturned
in diplodocoids, as recently described in the extreme form
Nigersaurus (Sereno et al., 2007).
Sauropods seem to have had large eyes (for their skull
size) since sclerotic rings indicate that almost the entire orbit
was filled by the eyeball, in contrast to larger theropods with
similar skull sizes, in which the eyeball only occupied the
dorsal part of the orbit. Sauropod nares are large, and the
fleshy nose was obvioulsy a highly sophisticated structure
(Witmer, 2001). Furthermore, the olfactory bulbs were well
developed in sauropods (Janensch, 1935–36), indicating that
olfaction was important to these animals.
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
Biology of the sauropod dinosaurs
An enlargement of the neural canal in the sacral region of
sauropods has popularly been interpreted as a ‘second brain’.
However, this enlargement, which can be considerably
larger than the braincase of sauropods (Janensch, 1939), was
probably filled with other tissues, such as a glycogene body
as in modern birds (Giffin, 1991), and by nerves extending
from the spinal cord to the legs.
Appenzeller et al. (2005) studied frequency domains and
power spectra in growth marks in dentine of Brachiosaurus
brancai teeth to assess the influence of the sympathetic (low
frequency) and parasympathetic (high frequency) autonomic
nervous system drive on the formation of this biological
structure. The growth marks can be regarded as expressions
of rhythmic falls and rises in blood supply to developing
enamel and dentine. Blood supply, in turn, is controlled
by the autonomous nervous system. In Brachiosaurus brancai
low frequency bands indicate an active sympathetic nervous
system which is consistent with the high hydrostatic pressures
which the cardiovascular system would have had to overcome
to ensure an adequate blood supply, especially to the brain.
(9) Organ size and its scaling
Based on body mass estimates, allometric scaling equations
(Calder, 1996; Schmidt-Nielsen, 1984) allow estimates of
the size of various anatomical (skeletal mass, organ size,
blood volume etc.) and physiological features (SchmidtNielsen, 1984). Applied to dinosaurs (Gunga et al., 1995,
1999, 2002, 2007, 2008; Franz et al., 2009; Ganse et al., in
press), these estimates are important in the modeling of many
life functions of sauropods, such as growth, metabolism,
respiration, locomotion, and reproduction. Not surprisingly,
staggering values for body mass also result in staggering
size estimates for organs, e.g. a 200 kg heart for a 38 t
Brachiosaurus (Gunga et al., 2008; Ganse et al., in press).
These estimates might also help to test other hypotheses
as well, such as questions about tissue density and the size
of organs. The latter can be derived from the body mass
and calculated using scaling equations. Examples are the
integument, respiratory system, heart, and gastrointestinal
tract. It can then be tested whether these organs are actually
anatomically able to fit into the thoracic and abdominal
cavity of a sauropod. This has been attempted recently
for Brachiosaurus brancai and especially Plateosaurus engelhardti
(Gunga et al., 2007, 2008; Franz et al., 2009, Ganse et al., in
press).
(10) Physiology and thermoregulation
Among the most debated aspects of sauropod biology
(and of dinosaurs in general) is their metabolic rate (e.g.
Seymour, 1976; Spotila et al., 1991; Sander & Clauss,
2008), and this topic requires a somewhat more extensive
treatment, beginning with the clarification of terminology.
Ectothermic refers to an animal acquiring the heat necessary
for the organism to function from the environment, while
an endothermic animal generates this heat metabolically.
Poikilothermic refers to an animal in which body temperature
131
tracks ambient temperature, while homoiothermic refers to a
constant body temperature that is elevated above ambient
temperature. Bradymetabolic indicates the low basal metabolic
rate (BMR) of most extant reptiles (∼30 kJ/kg body mass0.75) ,
while tachymetabolic refers to the elevated BMR seen in modern
placental mammals (289 kJ/kg body mass0.75 ). As a general
rule, a tachymetabolic animal has a BMR an order of
magnitude greater than a bradymetabolic animal of the
same body mass (Case, 1978; Schmidt-Nielsen, 1984, 1997;
Walter & Seebacher, 2009).
(a) Lines of evidence
Evidence from bone histology, posture, ecology, oxygen
isotope composition of skeletal apatite, and modeling has
been used in elucidating dinosaur, including sauropod,
thermometabolism, with contrary views having been
advanced (for reviews, see Padian & Horner, 2004; Chinsamy
& Hillenius, 2004). Arguments proposed for tachymetabolic
endothermy include: the mammal-like posture of sauropods
with their fully erect stance and gait (Ostrom, 1970) and the
cardiac requirements resulting from this bauplan (Seymour,
1976), predator-prey ratios of dinosaur faunas (Bakker,
1975), fibrolamellar and Haversian bone tissue which is only
seen in large mammals and birds today (de Ricqlès, 1980),
much higher growth rates than in ectotherms as indicated
by fibrolamellar bone and growth mark counts (Case,
1978; see below), low intra-bone oxygen isotope variability
similar to endothermic mammals (Barrick & Showers, 1994;
Barrick, Stoskopf & Showers, 1997), and latitude-dependent
differences in enamel oxygen isotope compositions between
sympatric ectotherms (crocodiles and turtles) and saurischian
dinosaurs (Fricke & Rogers, 2000; Amiot et al., 2006).
Bradymetabolic ectothermy appeared perhaps most
strongly supported by modeling of heat exchange with the
environment, indicating that a tachymetabolic sauropod
would overheat (Dunham et al., 1989; Spotila et al., 1991;
Alexander, 1989, 1998: O’Connor & Dodson, 1999). In
fact, African elephants are said to be at the body size
limit for tachymetabolic endotherms because of heat loss
problems, being prone to heat stroke. Their large ears are
major heat dissipation devices, raising the question of how
an endothermic sauropod would have circumvented this
problem. As already noted by Colbert (1993), because of their
long necks and tails, sauropods had a much more favorable
(i.e. higher) surface to volume ratio than a sauropod-sized
elephant.
Overheating problems again are cited by a new study
(Gillooly, Allen & Charnov, 2006) that combines a recent
gigantothermy model with an avian-like gas exchange model
that takes bradymetabolism into account. According to this
model, a sauropod heavier than 10 tonnes would encounter
body temperatures that are incompatible with life unless
some cooling mechanism existed. However, the modeling
results of Gillooly et al. (2006) may be compromised by
their use of unrealistically high growth rates of >5000 kg
year−1 for sauropods (Sander et al., in press b). In addition,
the tracheal surface and air sac system probably present in
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132
sauropods could have served as an efficient internal cooling
system (Wedel, 2003b, Sander & Clauss, 2008; Perry et al.,
2009, in press) to prevent overheating during exercise and in
high ambient temperatures.
Another argument for ectothermy was the scaling of
foraging time (Midgley, Midgley & Bond, 2002), based on
the observation that elephants feed 80% of their time. This
comparison would suggest that an endothermic sauropod
would not have been able to gather enough food due to time
constraints. However, this argument is not valid (Sander &
Clauss, 2008) because the time constraints encountered by
elephants are due to their need to chew their food—which
sauropods did not do—and their poor digestive efficiency
(Clauss et al., 2003b).
Weaver (1983) argued that head size in sauropods was too
small to take in enough food for an endothermic metabolism.
This hypothesis was rejected by Paul (1998) and Christiansen
(1999) based on a comparative analysis of muzzle width in
sauropods and mammals. Farlow (1987) added another twist
to the debate by suggesting that the heat generated by
fermentation of food in the sauropod gut ‘‘may have been
a significant source of thermoregulatory heat’’. However,
Clarke & Rothery (2008) analysed body temperature across
a large variety of mammalian species and concluded that
no general pattern of either increasing or decreasing body
temperature with body mass among herbivores was evident.
In addition, Clauss et al. (2008a) reviewed evidence from
measurements of BMR of animals of different digestive types,
finding that BMR is not reduced in herbivores to compensate
for fermentation heat, and suggesting that fermentative heat
was not important in sauropod thermoregulation.
P. Martin Sander and others
Lehman & Woodward, 2008; Woodward & Lehman, 2009).
These all report fibrolamellar bone tissue in the long bones
of virtually all sauropods (Klein & Sander, 2008; Sander
et al., in press b). Laminar fibrolamellar bone unequivocally
indicates bone apposition rates only seen in endothermic
vertebrates today. This is in agreement with data from
growth mark records that indicate body mass gains of a
few tons per year. Such growth rates are not seen in any
living ectotherm (Case, 1978) and cannot be reconciled with
the BMR of modern bradymetabolic terrestrial vertebrates
but point to tachymetabolic endothermy in sauropods, at
least during the phase of active growth (Sander et al., in
press b).
Bone histologic evidence for endothermy also consists of
the loss of developmental plasticity in the sauropodomorph
lineage, i.e. there is a tight correlation between body size
and ontogenetic age in sauropods and terminal body size
is not variable within species (Sander & Klein, 2005;
Klein & Sander, 2008; Sander et al., in press b). In the
basal sauropodomorph Plateosaurus, on the other hand,
developmental plasticity was still present, but in combination
with fibrolamellar bone. This may represent an early
stage in the evolution of endothermy in sauropodomorphs
(Sander & Klein, 2005). Bone histology also shows that
evolutionary body size increase in sauropodomorphs from
basal sauropodomorphs to large sauropods was brought
about by a strong increase in growth rate for which the
evolution of tachymetabolic endothermy may have been a
prerequisite (Sander et al., 2004; Sander & Klein, 2005).
(c) Scaling effects: gigantothermy and ontogenetic change
(b) Bone histologic evidence
Bone histologic evidence for ectothermy in sauropods was
seen in lamellar-zonal bone with lines of arrested growth
(LAGs) in sauropod bone tissue (Reid, 1981). However, this
work has been superseded by in-depth studies of sauropod
long bone histology. These document the overwhelming
abundance of fibrolamellar bone indicative of very high
growth rates. The argument by Reid (1981) and others
(Chinsamy & Hillenius, 2004; Chinsamy-Turan, 2005) has
also been weakened by the recognition that LAGs are
common in bones of mammals (Klevezal, 1996; Horner,
de Ricqlès & Padian., 2000; Sander & Andrássy, 2006).
Although fibrolamellar bone has repeatedly been described in
recent wild alligators with moderate growth rates (ChinsamyTuran, 2005; Tumarkin-Deratzian, 2007), this has not been
documented in sufficient detail, such as high-magnification
photomicrographs and polarized light images, to substantiate
these claims.
Our current understanding is that perhaps the strongest
evidence for metabolic rate in sauropods comes from the
numerous and detailed bone histologic studies conducted by
different groups (Rimblot-Baly, de Ricqlès & Zylbergberg,
1995; Curry, 1999; Sander, 1999, 2000; Erickson, Rogers
& Yerby, 2001; Sander & Tückmantel, 2003; Sander et al.,
2004, 2006, in press b Erickson, 2005; Klein & Sander, 2008;
Scaling effects are of primary importance in the discussion
of sauropod BMR because surface area increases with the
second power but volume increases with the third power.
While in modern small to medium-sized species, the two
strategies of endothermy and ectothermy are very distinctive,
they may converge at very large body size due to scaling
effects (Paladino , O’Connor & Spotila, 1990; Paladino et al.,
1997). This strategy, observed in the extant leatherback
turtle, was termed gigantothermy by Paladino et al. (1990;
see also Spotila et al., 1991). As body size increases, BMR
in reptiles, birds, and mammals increases with a slope of
less than unity, with an exponent of either 0.67 (White &
Seymour, 2003, 2005) or of 0.75 (Brody, 1945; Savage et al.,
2004) being found in the literature. The higher exponent,
however, may not be real but may result from the increasing
importance of heat production from fermenting gut contents
in large herbivores (White & Seymour, 2005; Clauss et al.,
2008a).
Thus it has been recognized for some time that a fully
grown sauropod dinosaur would not have been affected by
the daily temperature cycle even if it was bradymetabolic (e.g
Colbert, Cowles & Bogert, 1946; Alexander, 1989, 1998).
Independently of BMR, adult sauropods must have been
homoiotherms because of their very low surface to volume
ratio, which meant that their body temperature would at best
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Biology of the sauropod dinosaurs
have fluctuated with the seasons, but not on a daily basis as
in modern poikilotherms (Colbert, 1993; Seebacher, 2003).
The scaling effects discussed above apply to the changes in
body size experienced by the individual during its ontogeny as
well. However, these changes have received little attention so
far. This is surprising because no other terrestrial vertebrate
passes through five orders of magnitude during its ontogeny,
from a juvenile of a BM of a few kg to a fully grown
adult of >10 000 kg. The histologic growth record suggests
that, at least from about 20% maximum linear size (Sander,
2000; Klein & Sander, 2008), juvenile sauropods grew at
rates comparable to those of large mammals because they
laid down the same type of laminar fibrolamellar bone.
However, at a body size of 102 kg, juvenile sauropods would
not have enjoyed the benefits of gigantothermy and must
have had the BMR of modern mammals. On the contrary,
the heat flow models (e.g. Dunham et al., 1989) indicate
that up to a body mass of 103 kg, juvenile sauropods faced
the problem of excessive loss of metabolic heat if they did
not possess some type of integumentary insulation such as
feathers or hair. There is only one record of embryonic skin
(Chiappe et al., 1998) and none for juveniles. This embryonic
skin appears naked, presenting a paradox.
(d) Synthesis
How can the evidence for tachymetabolism provided by
bone histology be reconciled with the overheating problem
indicated by heat exchange modeling of adult sauropods? As
reviewed above, internal cooling surfaces must have existed
that allowed sauropod dinosaurs to shed their excess body
heat, and these presumably were located in the extensive air
sac system and trachea of sauropods. The unique ontogenetic
body size range of sauropods presumably was accompanied
by an equally unique ontogenetic variation in BMR (Farlow,
1990; Sander & Clauss, 2008). Growing sauropod dinosaurs
must have been tachymetabolic endotherms, but BMR may
have decreased rapidly as maximum size was approached,
when the heat loss problem became most severe, and a high
BMR was no longer needed to sustain growth.
(11) Life history, growth, and reproduction
The life of a sauropod began in an egg with a hard,
calcareous shell. This is indicated by eggs with embryos
of an indeterminate titanosaur from the Late Cretaceous
locality of Auca Mahuevo, Argentina (Chiappe et al., 1998,
2005; Salgado, Coria & Chiappe, 2005). Other Late
Cretaceous localities around the world have yielded eggs
and clutches of the same oogenus as the finds from
Argentina (Megaloolithus) and presumably were laid by
titanosaurian sauropod dinosaurs as well (Sander et al., 2008;
Griebeler & Werner, in press; Wilson et al., 2010). Pre-Late
Cretaceous sauropod eggs are unknown. Hard-shelled eggs
of the basal sauropodomorph Massospondylus from the Early
Jurassic of South Africa (Reisz et al., 2005) suggest that all
sauropodomorphs laid hard-shelled eggs. High shell porosity
and field data from southern Europe and India indicate that
133
most Megaloolithus clutches were buried in the substratum
or under plant matter (Sander et al., 2008). The exception
is the eggs from Auca Mahuevo, Argentina, which show
low porosity (Sander et al., 2008; Jackson et al., 2008) and
probably were not buried.
Clutch size in the buried eggs was small (<10 eggs).
None of the Late Cretaceous Megalooltihus eggs exceed 25 cm
in diameter and 5 l in volume, which is extremely small
compared to an adult sauropod. Small clutch size and size
of the eggs suggests that several clutches were produced
by the titanosaurid female per season, because otherwise
parental investment would have been unrealistically small
(Sander et al., 2008; Griebeler & Werner, in press). Because
of small egg size, sauropod hatchlings were also extremely
small compared to the parent animals. This alone suggests
that there was little parental care, and there is ample other
evidence against parental care (Sander et al., 2008; Myers
& Fiorillo, 2009), with the possible exception of the Auca
Mahuevo titanosaurs (Sander et al., 2008). Thus, titanosaurid
(and by extension, all other) sauropods produced numerous
small eggs with very precocial young that were left to fend
for themselves (Myers & Fiorillo, 2009) and suffered high
mortality before reaching sexual maturity in the second or
third decade of their life (Sander et al., 2008). Sauropods
differ fundamentally in this respect from terrestrial mammals
which do not combine large body size with numerous
small offspring, but show a negative correlation between the
number of offspring and body size (Janis & Carrano, 1992).
Not only were hatchling sauropods very small compared
to the adults, but they must have been very abundant
in sauropod populations (Sander et al., 2008; Griebeler &
Werner, in press). Juvenile sauropods are rare finds and thus
appear underrepresented in the fossil record (Carpenter
& McIntosh, 1994; Foster, 2005), and only very few
skeletons of small juveniles (less than 2 m in total length) are
known (Schwarz et al., 2007b). However, for most sauropod
species known from several individuals, the material also
represents growth series beginning at individuals less than
half maximum size (see data in e.g. Sander, 2000; Klein &
Sander, 2008; Sander et al., in press b). Limited data from
trackways and bonebeds suggest that sauropod herds were
composed of a much higher proportion of juvenile animals
than is observed in aggregations of mammalian herbivores
(Paul, 1998; Myers & Fiorillo, 2009). Correspondingly,
trophic energy represented by large herbivore species should
have been available to a predator guild to a much higher
degree in the sauropod ecosystem as compared to large
mammal-dominated ecosystems with reproductive output
of large herbivores confined to a few well-protected young
(Hummel & Clauss, 2008).
Bone histology indicates that juvenile growth was very
rapid because long bones of juveniles consist of highly
vascularized fibrolamellar bone (Sander, 2000; Klein &
Sander, 2008; Sander et al., in press b) of the type seen
in juvenile large mammals. The qualitative growth record
also suggests that sexual maturity was reached well before
maximum size (Sander, 2000; Klein & Sander, 2008; Sander
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134
et al., in press b), a pattern that is consistent with other
dinosaurs (Erickson et al., 2007; Lee & Werning, 2008).
Growth was determinate, as indicated by avascular bone
with closely spaced growth marks in the outermost cortex
(external fundamental system; Sander, 2000; Klein & Sander,
2008; Sander et al., in press b).
Unlike in other dinosaurs (Erickson, 2005), growth rates
have been difficult to quantify in sauropods because histologic
growth marks are rare and appear late in ontogeny, if at all
(Sander, 2000; Klein & Sander, 2008; Sander et al., in press
b). Compared to other dinosaurs, bone histology suggests that
sauropods had the highest growth rates as evidenced by the
lack of growth marks and the limited comparative data from
growth curves (Erickson et al., 2001). The few growth mark
records that are available suggest that full size was reached
in less than four decades (Curry, 1999; Sander, 1999, 2000;
Sander & Tückmantel, 2003; Wings et al., 2007; Lehman &
Woodward, 2008; Sander et al., in press b). Maximum growth
rates in the exponential phase of growth may have ranged
from 500 kg to 2000 kg per year (Wings et al., 2007; Lehman
& Woodward, 2008), and earlier estimates of over 5000 kg
per year (Erickson et al., 2001) are exaggerated (Lehman &
Woodward, 2008; Sander et al., in press b).
Similarly, age at sexual maturity is difficult to ascertain,
but it seems to have occurred in the second or third decade
of life (Sander, 2000; Sander & Tückmantel, 2003). Both
of these estimates are maximal ages because growth rate
must have been slower in the individuals with growth
marks than in the majority of sauropod samples, which
lack growth marks. Based on survivorship curves for large
extant herbivores, Dunham et al. (1989) also argue for an age
at first reproduction of less than 20 years in sauropods.
Adult sauropods presumably were almost immune from
predation because of their body mass being an order of
magnitude greater than that of the largest predators. Their
sheer volume made it difficult for an attacker to place an
effective bite rather than scratch the skin (Preuschoft et al., in
press). With sauropod hatchlings being so small, there must
have been strong selection pressure for high juvenile growth
rates because they would have shortened the time during
which the young sauropods were endangered by predators.
Selection for high growth rates would have been particularly
strong without parental care. In more general terms, a high
growth rate fueled by a high BMR is a prerequisite for giant
body size because tetrapods with a low BMR grow too slowly
to benefit from the selective advantages of large body size.
A high BMR thus emerges as a prerequisite for gigantism.
III. BODY SIZE EVOLUTION IN
SAUROPODOMORPHA
(1) Body size in basal dinosauriforms and basal
sauropodomorphs
In order to understand the evolution of gigantism in
sauropods, it is necessary to consider the body sizes of
P. Martin Sander and others
both the immediate (basal sauropodomorphs) and more
remote outgroups (basal saurischians, basal dinosauriforms)
to Sauropoda.
The oldest and most basal dinosauriforms are found in
the Middle Triassic of Argentina (Novas, 1996) and include
animals such as Marasuchus (Sereno & Arcucci, 1994) and
Pseudolagosuchus (Arcucci, 1987). These dinosaurian ancestors
were surprisingly small animals probably weighing less than
1 kg. There seems to be a size increase at the base of
Saurischia, although most basal saurischians (e.g. Eoraptor,
Sereno et al., 1993; Guaibasaurus, Bonaparte, Ferigolo &
Riberio, 1999) are still of moderate size, with an estimated
body mass well below 100 kg, and maybe even less than 10 kg
(see Peczkis, 1994, for a body mass estimate for Eoraptor;
Guaibasaurus was of similar size). The same is true for the
basalmost sauropodomorphs known, Saturnalia (Langer et al.,
1999), Panphagia (Martinez & Alcober, 2009), and Pantydraco
(Yates, 2003; Galton, Yates & Kermack, 2007), although the
latter is only known from juvenile individuals.
A notable size increase is seen within basal
sauropodomorphs, but the phylogenetic uncertainty in this
part of the dinosaur tree makes an interpretation of the
evolution of body size difficult. However, many typical
‘prosauropods’, such as Plateosaurus from the Late Triassic of Central Europe and Riojasaurus from contemporaneous
rocks of Argentina, reached masses well over 2 t (e.g. Sander,
1992; Peczkis, 1994), and fragmentary remains from various Late Triassic and Early Jurassic formations indicate
that some of these animals might well have exceeded 4 t
(Rauhut personal observation). Evolutionary size increase in
‘prosauropods’ was obviously not linear: based on the phylogenetic hypotheses of Yates (2004, 2007), one of the smallest
known ‘prosauropods’, Anchisaurus, with an estimated mass
of less than 50 kg (Peczkis, 1994), is more closely related to
sauropods than several taxa that exceeded 1 t.
Fechner (2009, see also Rauhut et al., in press) points out
that increasing size was also an important, if not the most
important, determinant in the evolution of dinosauriforms
and that many osteological, myological, and functional
characteristics of sauropod dinosaurs can only be understood
by taking the evolution of basal dinosauriforms into account.
(2) Body size in early and basal sauropods
Very large sauropod humeri (Buffetaut et al., 2002) from
the Triassic of Thailand document the very rapid evolution
(within a few million years after their origin) of very large
body size in sauropods (Buffetaut et al., 2002; Sander et al.,
2004). This rapid body size increase resulted from an
evolutionary increase in growth rate compared to relatively
small basal sauropodomorphs such as Plateosaurus (Sander
et al., 2004). This increase in growth rate appears to be
linked to the evolution of tachymetabolic endothermy in the
sauropdomorph lineage (Sander et al., 2004; Sander & Klein,
2005; Sander et al., in press b; see also section II.10b).
Sauropods are apparently unique among dinosaurs
because the other major dinosaur lineages (with the possible
exception of Theropoda) show a gradual body size increase
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Biology of the sauropod dinosaurs
135
over tens of millions of years (Sander et al., 2004; see
also Hone et al., 2005; Carrano, 2006). The Early Jurassic
sauropods from India (Barapasaurus and Kotasaurus) also
represent large forms, as do the Middle and Late Jurassic
sauropods from China, e.g. Mamenchisaurus (Wings et al.,
2007), and other areas, such as the Patagonian Patagosaurus
(Bonaparte, 1986). That theropods may also have evolved
rapidly to very large size, is suggested by footprints left
by Allosaurus-sized theropods in the Late Triassic (Thulborn,
2003; Lucas et al., 2006) and the remains of an Allosaurus-sized
coelophysoid from the Late Triassic of Bavaria, Germany
(Rauhut, personal observation).
(3) Body size in Neosauropoda
The Neosauropoda, all taxa more derived than the sauropods
discussed in the previous section, are characterized by large
to giant body size with a few notable exceptions, i.e. the
repeated occurrence of island dwarfing (Sander et al., 2006;
Stein et al. in press; Benton et al., 2010) and the apparent trend
in some titanosaurs towards evolutionary body size reduction
with no apparent island effects (Hone et al., 2005; Carrano,
2005, 2006). However, some of the largest sauropods also
evolved among the Titanosauria (Bonaparte & Coria, 1993;
Novas et al., 2005; Calvo et al., 2007). Within diplodocoids,
the dicraeosaurids are also characterized by relatively small
body sizes (Rauhut et al., 2005). However, no truly small
sauropods are known. Even the ‘dwarf’ sauropods were
animals with an adult body mass well in excess of 500 kg
(Peczkis, 1994; Sander et al., 2006; Stein et al., in press), a
size which is reached by less than 10% of modern mammal
species (Hotton, 1980).
(4) Independent gigantism in several lineages
Although sauropods were large animals in general, it is
important to point out that extreme sizes (close to or
in excess of 40 t) were reached independently by several
different lineages of sauropods at different times throughout
the later Mesozoic (Fig. 6). Specific cases are the Late
Jurassic (Kimmeridgian) basal eusauropod Turiasaurus (RoyoTorres et al., 2006), possibly the basal diplodocoid Amphicoelias
(Carpenter, 2006), the Late Jurassic (Tithonian) Diplodocus
(Seismosaurus) hallorum (Gillette, 1991, 1994; Herne & Lucas,
2006) and ‘Supersaurus’ (Upchurch et al., 2004) among the
Diplodocoidea, the Early Cretaceous (Aptian) brachiosaurid
Sauroposeidon (Wedel et al., 2000a, b), and several titanosaurs.
The latter include Paralititan from the early Late Cretaceous
(Cenomanian) of Egypt (Smith et al., 2001), as well as
Argentinosaurus (Bonaparte & Coria, 1993; Mazzetta et al.,
2004), Puertasaurus (Novas et al., 2005), Antarctosaurus giganteus
(Van Valen, 1969; Mazzetta et al., 2004), and Futalognkosaurus
(Calvo et al., 2007) from the Late Cretaceous of Argentina.
Extreme size among these very large titanosaurs probably
evolved independently as well, but this is difficult to evaluate
because of the uncertain relationships of these taxa within
Titanosauria. Other examples of independent evolution
of gigantism in sauropods may include the poorly known
Fig. 6. Independent evolution of gigantic species (>40 t
body mass) in several lineages of Sauropoda as shown by
optimization of body size on a sauropod phylogeny (part of
the supertree of Dinosauria published by Lloyd et al., 2008).
Note that Turiasaurus, Paralititan, Puertasaurus, Futalognkosaurus,
and Huanghetitan are not listed because they were not covered by
this phylogeny. Body masses were taken from various sources
(see Table 1). Lack of a colored box in front of the genus name
indicates a lack of mass data.
Huanghetitan ruyangensis from the middle Cretaceous of China,
which has ribs over 3 m in length (Lü et al., 2007).
Giant sauropods thus occurred from the Late Jurassic to
the Late Cretaceous, over a time span of at least 85 million
years, and this extreme gigantism developed independently
in most major groups of neosauropods (Fig. 6). The large
number of very recently described giant forms suggests that
truly giant forms may have been even more common than
suggested by the current fossil record. The stratigraphic
range of these extreme giants and the fact that some of
the largest sauropods are found in the latest Cretaceous
(e.g. Puertasaurus) are especially noteworthy in light of the
size-area relationship outlined by Burness et al. (2001), since
their gigantism thus does not seem to be influenced by the
progressice fragmentation of the supercontinent of Pangea
during this time.
Differences in skull morphology, neck anatomy and
reconstructed neck position in the different lineages that
evolved giant sauropods indicate different feeding types
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
136
(Upchurch & Barrett, 2000; Barrett & Upchurch, 2005).
This suggests adaptations other than a specific feeding mode
lead to very large body size.
(5) Island dwarfing
As best exemplified by Quaternary proboscideans (Roth,
1990, 1992; Guthrie, 2004; Vos, Van den Hoek Ostende
& Van den Bergh, 2007), dwarfed taxa of large to giant
herbivores may evolve in island situations. The diminutive
latest Cretaceous titanosaur Magyarosaurus from Romania has
long been considered to have been an island dwarf (Nopcsa,
1914; Weishampel et al., 1991; Jianu & Weishampel, 1999;
Benton et al. 2010), but only the study of bone histology
provides unequivocal evidence for island dwarfing. This was
the case in the Late Jurassic basal macronarian Europasaurus
(Sander et al., 2006), but Magyarosaurus has now passed
the test as well (Benton et al., 2010; Stein et al., in press).
Other instances of putative island dwarfing are sauropods
from the Albian-Cenomanian Adriatic-Dinaric carbonate
platform (Dalla Vecchia, 2005). The latest Cretaceous
titanosaurs Rapetosaurus from Madagascar and Ampelosaurus
from southern France and northern Spain may also represent
island forms (as already noted for Ampelosaurus by Jianu &
Weishampel, 1999), because southern France together with
the Iberian peninsula also formed a large island (Dercourt
et al., 2000) and Madagascar had already split from mainland
Africa at this time (Smith, Smith & Funnell, 1994). Another
example of a larger island dwarf may be represented by
the Late Jurassic Cetiosauriscus from Switzerland (Schwarz,
Meyer & Wings, 2007c).
The estimated body mass of Europasaurus was around
800 kg (Stein et al., in press), and that of Magyarosaurus was in
the same range (700–1000 kg, Peczkis, 1994). These island
dwarfs are informative for the evolution of body size changes
in sauropods because they show that the decrease in body
size evolved through a decrease in growth rate (Sander et al.,
2006; Stein et al., in press), the reverse of what is seen in the
evolutionary increase in growth rate leading to the first large
sauropods (Sander et al., 2004).
(6) Body size evolution and Cope’s Rule
Two independent studies (Hone et al., 2005; Carrano,
2006; see also Carrano, 2005) have recently attempted
to quantify body size evolution in dinosaurs, and in
sauropods in particular, to assess whether Cope’s Rule
was in operation in these groups. Using phylogenetically
independent comparisons, Hone et al. (2005) showed that
there was a strong but gradual body size increase in
Dinosauria as a whole, while Sauropoda showed a rapid
size increase in the Triassic but apparently decreased in size
during the Cretaceous. Carrano (2006) evaluated body size
change in all of Dinosauria and in major subclades such
as Sauropodomorpha using squared change parsimony.
He concluded that dinosaurs in general, as well as most
subclades, showed a continuous increase in body size
during their evolutionary history. Exceptions were the
P. Martin Sander and others
Sauropodomorpha, where in Macronaria there appeared
to be a reduction in body size represented by several smallbodied titanosaurs, and the Theropoda (Carrano, 2006).
Both these studies, however, are superseded by the new finds
of giant titanosaurs and the island dwarfs reviewed above,
and Carrano (2006) also did not include some large-bodied
titanosaurs such as Alamosaurus.
Our current understanding would suggest that Macronaria
in general and Titanosauria in particular extended the
ancestral body size range to relatively very small and
very large forms, and the giant South American Cretaceous sauropods (Argentinosaurus, Antarctosaurus, Puertasaurus,
Futalognkosaurus) appear particularly ‘oversized’ for the landmasses they were inhabiting. While Carrano (2006) was not
able to offer an explanation for the more numerous relatively
small titanosaurs, a closer look at palaeogeographic change
from the Middle Jurassic to the end of the Cretaceous combined with the area-body size relationship established by
Burness et al. (2001) does: we observe that both the breakup
of Pangea and the sea level rise since the Triassic resulted
in a fragmentation of land masses and an increased number
of islands. With sauropod body size, as the largest inhabitants of the land masses, being closely tied to land mass
size (Burness et al., 2001), the evolution of smaller forms was
the result. The island dwarfs Europasaurus and Magyarosaurus,
being the smallest macronarian sauropods, are only the most
extreme known results of this process. Other dinosaur lineages continued to increase in average size until the end of
the Cretaceous (Hone et al., 2005; Carrano, 2006), despite
the ever-increasing fragmentation of land masses, because
they had not reached the upper limits of body size for the
landmass they were inhabiting.
IV. HYPOTHESES EXPLAINING GIANT BODY
SIZE
(1) Limits to body size
Given that Cope’s Rule in its most general formulation is
valid (Bonner, 2006), the question with regard to sauropod
dinosaurs must be what limited their body size (Alexander,
1989), not what drove body size increase. The existence
of limits to body size in the extant fauna is underscored
by the body size-land area relationship of Burness et al.
(2001). Sauropods (and theropods) somehow circumvented
the constraints imposed on mammals and other dinosaurian
groups (Carrano, 2006), raising the question of the nature of
these constraints. For heuristic purposes, we will repeatedly
ask how these constraints act on mammalian megaherbivores
(defined as herbivores exceeding 1000 kg body mass;
Owen-Smith, 1988) and on large ground birds and draw
a comparison between mammalian megaherbivores and
sauropod dinosaurs. The question of sauropod gigantism
thus is linked throughout to the question of why other
groups, most notably mammals, have not reached similar
dimensions, even though they are well within the theoretical
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
Biology of the sauropod dinosaurs
limits for terrestrial animals (Hokkanen, 1986). Although
the subject will be touched upon repeatedly, exploring the
theoretical limits of the tetrapod bauplan in the terrestrial
realm is not the topic of our paper.
The constraints limiting body size fall into two broad
categories: intrinsic constraints, founded in the animal’s
design and physiological makeup, and extrinsic constraints,
founded in biotic and physical factors of the environment an
animal inhabits, i.e. the boundary conditions of the system.
As the example of gigantism in Carboniferous dragonflies
illustrates (Beerling, 2007; Lighton, 2007), intrinsic and
extrinsic constraints are mutually effective on an organism.
Thus, because of design limitations of the tracheal respiratory
system of dragonflies, in today’s atmosphere of 21% O2 they
are limited to a maximum body length of 12 cm and a
wingspan of 16 cm. During the Carboniferous, the same
biological design allowed wing spans of over 70 cm due
to an oxygen level of 30% (Berner et al., 2003; Berner,
VanDenBrooks & Ward, 2007). When oxygen level fell in
the Permian and Triassic (Berner, 2006; Berner et al., 2007),
dragonflies decreased in maximum body size (Beerling, 2007;
Lighton, 2007).
Gravity also limits body size, and the current gravity
constant of 0.981 ms−2 has been proposed to limit body
size to 20 t (Economos, 1981) based on a mass estimate for
the largest land mammal ever, Paraceratherium (also known
as Indricotherium). However, sauropods were much heavier
than the largest land mammals, and Günther et al. (2002)
suggested the upper limit for terrestrial organisms due to
gravitational forces to be at least 75 t. Similarly, Hokkanen
(1986) calculated that bone strength and muscle forces only
become limiting to terrestrial animal size at masses in excess
of 100 t.
137
(2001), places an upper limit on body size, since all of the
Earth’s landmasses are of limited size and can be viewed as
islands.
Land area is, of course, only a crude proxy for a
population’s resources which depends on the portion of
the landmass that is actually inhabitable, on the productivity
of an area, but also on intra- and interspecific competition
for resources. According to the classical theory of island
biogeography (MacArthur & Wilson, 1967), larger islands
have more individuals per taxon (the authors assume a
linear increase with increasing area size), which increases
intraspecific competition for resources, and they also have
more species, which increases interspecific competition.
However, in addition to land area (as a proxy for available
resources) and BMR, there is a crucial third factor in the
maximum body size-land area relationship which was not
discussed by Burness et al. (2001). This factor is recovery
rate after a severe population crash. It greatly influences the
likelihood of chance extinction of the top species (Janis &
Carrano, 1992; Farlow, 1993). Not surprisingly, high per capita
resource availability and high population growth rates are
factors known in conservation biology to increase the chance
of population survival (Gilpin & Soulé, 1986; Primack, 1993).
From an evolutionary perspective, high population recovery
rates can also be viewed as an adaptation to overcome
temporary resource limitations, because a species that has
a high recovery rate can ensure its long-term survival, even
under low population densities and thus on temporarily
limited resources.
In the remainder of this paper, we will approach
the gigantism issue from the resource perspective. This
perspective takes all constraints into account and aids
in formulating hypotheses about how sauropod dinosaurs
overcame them (Fig. 7).
(2) Resource availability
A different approach to understanding the limits of body size
is resource availability. Resource availability has long been
considered important in island habitats (Palkovacs, 2003)
but, as suggested by the maximum body mass-land area
relationship of Burness et al. (2001) (Fig. 3), it is of general
importance for explaining the upper limits of body size. This
constraint has its explanation in the relationship between
resources available to the top species, its population density,
and its risk of chance extinction (Janis & Carrano, 1992;
Farlow, 1993; Paul, 1994, 1997b, 1998).
As each individual of the top species requires a certain
amount of the available resources, expressed as its home
range (Burness et al., 2001), and resources are related to
land area, the size of a landmass determines the number
of home ranges and thus individuals of the top species that
can inhabit it. The amount of resources required by an
individual depends on its body size and its BMR. The larger
and more metabolically active the individuals, the fewer
are supported by the landmass. With increasing body size,
the number of individuals with a given BMR will decrease,
reaching a threshold below which chance extinction becomes
increasingly likely. This is what, according to Burness et al.
V. MORE RESOURCES AVAILABLE THROUGH
DIFFERENT BOUNDARY CONDITIONS
(1) Physical boundary conditions
Although gravity is of overriding importance in determining
the bauplan of an organism, we have to assume that
there were no secular variations in Earth’s gravity in the
Phanerozoic geologic past (Economos, 1981). Among other
possibly different boundary conditions, atmospheric oxygen
levels (Hengst et al., 1996; Berner et al., 2007; Ward, 2006),
levels of carbon dioxide (Maurer, 2002) as well as higher
ambient temperatures have been implicated in sauropod
dinosaur gigantism (Fig. 7).
(a) Increased oxygen content of atmosphere
All else being equal, would an increased level of atmospheric
oxygen allow the evolution of gigantic terrestrial tetrapods?
This possibility is suggested by the example discussed above
of the uniquely gigantic dragonflies of the Carboniferous
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
P. Martin Sander and others
138
Reproduction mode:
- faster population recovery through ovipary
0%
100%
25%
75%
?
50%
50%
?
25%
75%
?
100%
0%
100%
75%
50%
Fewer resources used:
- reduction in body densitiy
- reduced cost of locomotion
- reduced cost of respiration
- lower basal metabolic rate
- reduced cost of reproduction
25%
0%
More resources available:
- higher O2 content of atmosphere
- higher plant productivity
- higher ambient temperatures
- more nutritious food
- exceptionally productive habitat
- long neck resulting in:
- extension of reach
- larger feeding envelope
- feeding: more and more selectively
- greater digestive efficiency
- more oxygen uptake through
avian-style lungs
Fig. 7. Three factors, i.e., more resources available, fewer resources used, and the reproduction mode, potentially resolved the land
area versus body size enigma of Burness et al. (2001) and thus contributed to the gigantism of sauropods and theropods. Specific
hypotheses (discussed in the text) underlying each contributing factor are listed below each factor. Because very likely more than one
factor was important, the relative contribution of each is best visualized in a ternary diagram. The symbols with the question marks
indicate potential solutions to the gigantism enigma, and the relative importance of each factor can be read off the percentage scale
leading up to its respective corner. Note that we do not offer a final solution but that this graph is meant to visualize the possibilities
of interplay between the three factors.
(Lighton, 2007). Hengst et al. (1996) explored this hypothesis
for sauropod dinosaurs, based on the premise of an oxygen
level of 30% or above in the Jurassic atmosphere (Landis et al.,
1996). Physically modelling respiration in the Late Jurassic
sauropod Apatosaurus, they concluded that the respiratory
system of this animal could not have delivered enough oxygen
to the tissues at today’s oxygen levels. This applied even under
the assumption that Apatosaurus had the basal metabolic rate
of a reptilian ectotherm. However, the hypothesis of Hengst
et al. (1996) is superseded by the likely presence of a birdlike lung in sauropods and the current understanding that
oxygen levels were significantly lower in the Jurassic and
Cretaceous than today (Gans et al., 1999; Dudley, 1998;
Berner, 2006; Berner et al., 2007; see also Fig. 8) or at about
the same level (Bergman, Lenton & Watson, 2004; Belcher
& McElwain, 2008).
(b) Increased plant productivity through increased CO2 content of the
atmosphere
Another hypothesis that has been advanced is that an up to
tenfold higher CO2 content of the Mesozoic atmosphere than
today (e.g. Royer et al., 2004; Berner, 2006; see also Fig. 8)
increased plant productivity, thus allowing larger body size
on the same plant resources (Paladino et al., 1997; Burness
et al., 2001; Maurer, 2002). However, experiments have
shown that while an increased CO2 level does increase plant
productivity, the decrease in protein content and increase
in levels of nonstructural carbohydrates and phenolics in
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
Biology of the sauropod dinosaurs
139
260
25
240
Current oxygen level
220
20
180
160
Content (%)
15
140
120
10
100
80
Femur length (cm)
200
Oxygen
60
5
40
CO2
Current CO2 level
0
Triassic
250
20
0
230
Jurassic
210
190
Cretaceous
170
150
130
110
90
70
50
Age (Mya)
Fig. 8. Variation of atmospheric composition(O2 , CO2 ) and body size through time. Each data point is located at the beginning of
a stage, starting with the Carnian and ending with the Cretaceous-Tertiary boundary. The variation of body size through time is an
extension of the Carrano (2006) data set with femur length as a proxy for body size. Missing data points for body mass are either
due to lumping of data from two stages (i.e. the Kimmeridgian and Tithonian) or missing data (i.e. for the Berriasian, Barremian,
and Aptian). Body size increases gradually from the Late Triassic to the Late Jurassic, forming a plateau in the Cretaceous. The two
sharp drops in body mass in the Early and Late Cretaceous are probably due to a poor terrestrial fossil record at these times. Note
the lack of correlation between atmospheric composition and sauropod body mass. CO2 content of the atmosphere also determines
global temperature, and this graph thus suggests that sauropod body size is not correlated with global temperature variations through
time, either. The data for O2 and CO2 levels are from Ward (2006).
sum result in a decreased food quality (at least for insects)
(e.g. Roth & Lindroth, 1995; Ehleringer, Cerling & Dearing,
2002), thereby offsetting the hypothesized effect at least
partially. Midgley et al. (2002) also question the increased
plant productivity as a result of increased atmospheric CO2
because global primary productivity probably is saturated at
much lower CO2 levels than those of the Mesozoic, arguing
that water and nutrient availability were the limiting factors.
In addition, while on average, CO2 level may have been
much higher than today, it was by no means constant (Berner,
2004; Berner et al., 2007). There is no obvious correlation
of CO2 level with body size evolution in sauropods (Fig. 8),
such as a sudden increase of CO2 concentration in the
Late Triassic (to produce the first large sauropods), a high
in the Kimmeridgian and Tithonian (to result in gigantism
in several lineages of sauropods at this time), and in the
Late Cretaceous (the age of the giant titanosaurs). Thus, we
suggest that increased atmospheric CO2 levels were not a
prerequiste to the evolution of gigantism in sauropods.
(c) Higher ambient temperatures
Higher average ambient temperatures are also worth
considering because they would tend to blur the concepts
of endo- versus ectothermy: with high ambient temperatures,
homoiothermy can be achieved in large, compact animals
with a low metabolic rate (Spotila et al., 1991), whereas
tachymetabolic species face overheating in the absence of
effective physiological or behavioural cooling mechanisms.
Thus, large size could provide the advantages of a high,
constant body temperature at low cellular metabolic cost
(gigantothermy: Dunham et al., 1989; Spotila et al., 1991;
Paladino et al., 1997).
A correlation between ambient temperature and maximum body size has been established for modern ectotherms
(Makarieva et al., 2005), and gigantism in snakes appears to
be related to a global thermal maximum (Head et al., 2009).
Although not treated extensively in the recent scientific
literature (but see Paladino et al., 1997), the hypothesis that
increased average ambient temperature during the Mesozoic
greenhouse allowed the exceptional body size of sauropods
needs to be considered from the point of view of the energy
budget of a living sauropod. Higher ambient temperatures
could have benefitted an endothermic animal in that less of
the fodder taken in would need to be alotted to generating body heat (Seebacher, 2003). A poikilothermic dinosaur
would have profited from increased ambient temperatures
because of the ability to forage longer and more intensively, thus taking up more energy. However, the hypothesis
of higher ambient temperatures permitting gigantism is
not compatible with laboratory experiments on ectotherms
(Atkinson & Sibly, 1997) and observations on endothermic
mammals (Bergmann’s Rule) and birds (reviewed by Ashton,
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
P. Martin Sander and others
140
2001), because endothermic animals tend to be larger in
colder environments and not vice versa.
As atmospheric temperature is generally believed to be
determined by CO2 content (Wallmann, 2007), one again
should look for a correlation between sauropod body size
and atmospheric CO2 levels to test the hypothesis that
extreme temperatures led to extreme body sizes of sauropods.
However, this correlation is not apparent (Fig. 8).
(2) Biological boundary conditions
(a) More nutritious food
Another extrinsic biotic hypothesis is that sauropod gigantism
was made possible by some or all of the plant groups of the
pre-angiosperm flora, such as cycads, ginkgoes, conifers,
and ferns, being more nutritious than the plant groups
preferentially ingested by modern herbivores, namely grasses
and dicot leaf browse. Laboratory experiments designed to
evaluate metabolizable energy content of the pre-angiosperm
flora (Hummel et al., 2008) show that several of these plant
groups offer herbivores energy yields comparable to modern
angiosperm browse (contra Weaver, 1983) while others had
much lower yields. In particular, all three tested species of
Equisetum offered high levels of energy, even reaching the level
of grasses or herbs. Araucaria foliage also reached high levels,
but only after prolonged fermentation (Hummel et al., 2008).
Non-podocarpaceous conifers, Ginkgo, and some ferns such as
Angiopteris would also have yielded as much energy as the most
nutritious food plants available to modern herbivores today
(Hummel et al., 2008). However, protein content of Araucaria
was insufficient for this plant to have served as the sole food
source of a growing sauropod (Hummel et al., 2008). Thus,
the sauropods’ dietary choices, which were restricted to the
pre-angiosperm flora before the mid-Cretaceous, apparently
did not pose an obstacle in their evolution of gigantic body
size nor did they foster it.
The two groups of food plants that offer the greatest
amount of energy, Equisetum and Araucaria, most likely grew
in large, monospecific stands, such as dense thickets around
waterways (Equisetum) or in forests (Araucaria), much as they do
today. They would have offered great amounts of biomass in
a concentrated area to the continuously browsing sauropods.
This also would have applied to other forest-forming plant
groups such as the various families of conifers. Other plant
taxa, for example, ferns, cycads, and bennettitites, were
probably patchier or sparser in their distribution and thus
less dependable as a food source (Gee, in press).
While some Mesozoic plants were both highly nutritious
and abundant, there is no evidence from fermentation
experiments to explain sauropod gigantism through more
nutritious food. In addition, even if Mesozoic forage was
more nutritious than modern forage and would have made
gigantism possible, one would have to explain why this led
to the unique gigantism of sauropods. In fact, herbivorous
dinosaurs in general do not show any obvious evolutionary
response to the rise of angiosperms (Coe et al., 1987; Wing &
Tiffney, 1987; Weishampel & Jianu, 2000; Barrett & Willis,
2001; Lloyd et al., 2008; Butler et al., 2009).
(b) Exceptionally productive habitats: mangroves and tidal flats
Other hypotheses based on increased resource availability
from plants are those that involve exceptionally productive
habitats. One such hypothesis is that of Smith et al. (in
Nothdurft & Smith, 2001; see also Smith et al., 2001),
in which they recognize mangroves as allowing sauropod
gigantism. This hypothesis was based on the discovery of
the giant sauropod Paralititan from the Cenomanian of
Egypt but was seen to be of general applicability. Based
on associated plant remains (of the fern Weichselia), the
authors concluded that Paralititan had preferentially inhabited
mangrove environments. Mangroves, today being the second
most productive environments on Earth after the tropical
rainforests, would thus have provided the resource base for
the evolution of exceptional body size. This hypothesis was
based on the largely unsubstantiated premises that Weichselia
is a mangrove plant, that such fern mangrove communities
were very widespread and as productive in the past as
modern angiosperm mangrove communities are today, and
that Paralititan really inhabited these environments (Smith
et al. in Nothdurft & Smith, 2001). While this hypothesis may
be applicable to the case of Paralititan, it obviously falls short
of explaining sauropod gigantism in general, with their need
to occupy huge land masses (Burness et al., 2001).
Links between gigantism and particular food resources
may be suggested by the rich worldwide and temporally
extensive record of sauropod footprints from tidal flat
sediments (Lockley & Meyer, 2000). Particularly in Upper
Jurassic and Lower Cretaceous peritidal carbonate rocks,
so-called megatracksites are preserved that cover thousands
of square kilometers and show that sauropods lived in or
migrated into the tidal flats several hundred kilometres
from the nearest coast. Modern sedimentary environments
of this kind are generally devoid of vertebrate life, and
it remains unclear what the food base for the sauropods
would have been. One possiblity are the Cheirolepidiaceae,
an extinct conifer family, some members of which were
succulent halophytes (Gomez et al., 2002). However, based
on the carbon isotope composition of sauropod bones and
teeth, intensive feeding on marine food resources, such as
algae or other marine plants, can be excluded (Tütken, in
press). Nothing is known about the isotopic signature of
Cheirolepidiaceae, though.
VI. MORE RESOURCES AVAILABLE THROUGH
EVOLUTIONARY INNOVATION
(1) Long neck
We now want to explore evolutionary innovations that may
have made more resources available to the individual, leading
to gigantism in sauropods (Figs 6, 8). The most important of
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
Biology of the sauropod dinosaurs
these is the hallmark of sauropod anatomy, the long neck.
Potential selective advantages conferred by the long neck
can be framed as two hypotheses. The first hypothesis is
that the long neck allowed adult sauropods to exploit food
resources beyond the reach of other large herbivores or
smaller individuals of the same sauropod species, e.g. plant
matter high above the ground. The second hypothesis is that
a long neck and the resultant large feeding envelope would
have conveyed a considerable energy savings in feeding as
opposed to moving the whole body while feeding.
(a) First hypothesis: extension of reach
A very long neck obviously allows access to food at great
heights, i.e. in the crowns of trees, if such a neck can be
raised sufficiently high. Alternatively, sauropods that were
unable to raise their neck could have accessed the additional
resources by rearing up on their hindlimbs (Dodson, 1990;
Paul, 1998; Mallison, in press a). In addition, during periods
of food shortage, the ability to reach resources that could
not be exploited by other animals would have carried a high
selective advantage (Sander et al., 2009). A similar selective
advantage could have existed in low-browsing sauropods
as well, e.g. if low-growing swamp plants such as stands
of horsetails were not accessible or only difficult to reach
without a long neck (Sander et al., 2009). The hypothesis of
the long neck greatly increasing the food resources available
to a very large terrestrial herbivore thus seems to be well
supported (Preuschoft et al., in press).
(b) Second hypothesis: large feeding envelope versus acceleration
of whole body
The energetic advantage of feeding with a long neck over
covering the same feeding volume by walking depends on
several factors, especially the distribution of food, the size
of the animal, and the mechanical construction of the neck
(Preuschoft et al., in press). With respect to the costs associated
with travel during foraging, it is mainly the acceleration of the
huge body that is energy-expensive, not so much the travel
itself. Shipley et al. (1996, p. 242) modeled the influence of
locomotion on foraging behaviour in modern herbivores
and state that an ‘‘animal may choose to exploit many bites
at one ‘feeding station’ before moving on’’ over foraging
continuously because of the considerable cost incurred
from acceleration and deceleration. This means that an
adaptation that enables more bites per feeding station would
be advantageous for any animal—regardless of its body size.
Obviously, a long neck is such an adaptation (Preuschoft et al.,
in press). The interesting question resulting from this insight
is why such long necks are not more common in herbivorous
animals. If chewing, i.e. a dental battery, is in the adaptive
repertoire of a lineage, then long necks will not be an
option due to the disproportional increase in size and mass
of the ingestive apparatus with increasing body size. This
positive head allometry is apparent both in mammals, e.g.
in horses (MacFadden, 1994), and in ornithischian dinosaurs
(Long & McNamara, 1997a, b). Herbivorous birds, e.g.
141
geese, lack a dental battery and have long necks, as do basal
sauropodomorph dinosaurs from which sauropods must have
arisen.
Applied to sauropods, moving the neck during feeding was
not very energy-expensive. The neck could have been kept at
the different inclinations by strong ligaments (e.g. Alexander,
1985, 1989; Dzemski & Christian, 2007; Schwarz et al.,
2007a) and muscles with slow fibres, so that little energy
was required to keep the neck in a certain posture. During
feeding, slow sideways movements of the neck probably were
predominant and would have served to cover systematically
the feeding envelope. Quicker and forceful changes of the
position of the head could have been accomplished by flexion
in the cranial neck section, so that only a small fraction of
the body mass was involved in activities with high energy
expenses. These assumptions fit the mechanical analyses
of Christian & Dzemski (2007, in press) and Dzemski &
Christian (2007). However, feeding on large trees requires
great flexibility in the neck, so that the head can be moved
in a maze of branches. Sauropods with very long cervical
ribs (e.g. Mamenchisaurus) were thus probably not capable of
accessing a larger three-dimensional volume by rearing up,
simply because their necks would be too immobile (Mallison,
in press a). By contrast, Diplodocidae had very mobile necks
that potentially allowed treetop navigation.
If we assume that feeding on low vegetation (e.g. Equisetum)
was important for sauropods, rather than on food distributed
at different heights, then we would expect a positive
allometry of neck length in order to compensate for the
increasing distance between the origin of the neck and
the ground in larger animals. Neck allometry is indeed
positive interspecifically in sauropodomorphs (Parrish, 2006)
and intraspecifically (Britt & Naylor, 1994; Ikejiri et al.,
2005; Schwarz et al., 2007b). We conclude that this second
hypothesis is supported as well. The selective advantage of
the long neck of sauropods was the ability to exploit food
sources that could not be reached by other herbivores or by
smaller individuals of the same species and a considerably
energy savings in feeding as opposed to moving the whole
body while feeding.
(2) Feeding
There are three ways for sauropods to have obtained more
resources through feeding: by consuming more fodder, by
feeding more selectively on the most nutritious plant parts
such as seeds and young shoots, or by consuming plants
with a higher energy content than today’s vegetation (a
boundary conditon hypothesis, discussed in Section V.2a).
Consumption of greater quantities of food would appear
to be an unlikely option because the head of sauropods is
not disproportionally larger than expected for herbivores of
their size (Paul, 1998; Christiansen, 1999). The previously
hypothesized avian-style gastric mill in sauropods (e.g.
Christiansen, 1996) would also have limited the rate of food
intake (Sander & Clauss, 2008), but Wings & Sander (2007)
showed that sauropods probably did not have a gastric
mill. As time required for mastication was no constraint
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
142
for sauropods, plant anatomy—how much material can
be harvested in one bite—might have become a crucial
determinant of intake, and might thus have determined
sauropod foraging decisions (Hummel & Clauss, in press).
However, it should be noted that the lack of a modern
analogue—an endothermic herbivore without adaptations
to mastication or to grinding in a gizzard, both of which
are intake-limiting factors—leaves us speculating whether
sauropods—and other herbivorous dinosaurs with similar
characteristics—could have achieved higher food intake
rates than extrapolated from mammalian herbivores.
Also unlikely is the hypothesis that sauropods were highly
selective feeders on the most nutritious plant parts, i.e. seeds
and young shoots. Known as the Jarman-Bell Principle,
herbivores become less selective with increasing body mass,
and all modern megaherbivores are bulk feeders (OwenSmith, 1988; Cameron & du Toit, 2007). On the one hand,
this is an effect of the increasing disparity in plant and oral
anatomy with increasing body size. As herbivores become
larger, they lose the ability to select only the most nutritious
parts of plants which tend to be small (buds, seeds etc.).
Also, due to their larger (more clumsy) mouth parts, they
have to ingest larger chunks of food. On the other hand,
because lower quality food is much more abundant than
higher quality food, large herbivores cannot afford to search
for the more dispersed high-quality food items due to their
very high absolute food intake requirement (Demment &
Van Soest, 1985). Note however, that this does not mean
that large herbivores cannot subsist on high-quality food if it
is abundant. Renecker & Hudson (1992) provide an excellent
review, using the moose (Alces alces) as an example of a large
herbivore that, if high-quality food is abundant, can subsist
on it.
(3) Greater digestive efficiency
The hypothesis of particularly efficient digestion is difficult to
test in extinct animals. Nevertheless, one might be tempted
to pursue such speculations based on the enormous body
mass of sauropod dinosaurs, given the widespread notion
that digestive efficiency increases with increasing body mass
in herbivores (Demment & van Soest, 1985). This concept
relies on the belief that ingesta retention time—the time
that the ingested food stays in the gut and hence can be
digested—increases with body mass (Illius & Gordon, 1992).
This view has also been adopted for dinosaurs (Farlow,
1987; Midgley et al., 2002). In a literature review of available
data for mammalian herbivores, however, the generality
of this relationship has been rejected (Clauss et al., 2007,
2008b) because, among large mammalian herbivores, ingesta
retention time does not consistently increase with body mass.
The concept of increasing digestive efficiency with
increasing body mass has other limitations, too: with
increasing body mass, the fineness that forage can be
masticated into decreases in mammals—in other words,
larger herbivores ingest larger particles (Fritz et al. 2009),
which are more difficult to digest. Also, the absorptive
surface of the gut increases with body mass as M0.75
P. Martin Sander and others
whereas gut capacity increases as M1.0 (Clauss & Hummel,
2005; Clauss et al., 2007), leading to less absorptive area
per unit of ingesta. Among ruminants, energetic losses due
to methane production increase with body mass (Clauss
& Hummel, 2005). Data compilations from the literature
have so far not supported the conclusion that larger animals
achieve higher digestion coefficients (Pérez-Barbería et al.,
2004; Clauss & Hummel, 2005; Clauss et al., 2009). Rather,
among mammalian herbivores, different solutions for the
interplay between intake, ingesta retention time, chewing
efficiency, and digestive efficiency have been reached by
different species and taxonomic groups (Clauss et al., 2009).
In particular, subtle differences in metabolic rate need to
be taken into account when explaining this variation (e.g.
Schwarm et al., 2006).
One important constraint was recognized by Demment
& Van Soest (1985), namely that digestive efficiency cannot
be optimized endlessly, but is limited by the quality of
the forage itself. To put it simply, digestive efficiency can
only approach 100%, but it cannot increase further. Thus,
increased ingesta retention in larger-bodied animals may be
beneficial if offsetting the negative effect of decreased particle
size reduction (as expected in non-chewing sauropods), but
further increases in retention time probably will have a
negative effect (Clauss et al., 2003a). The optimal ingesta
retention time for a herbivore of a given efficiency in
particle size reduction will always be limited by the maximum
digestibility of the forage it feeds on.
Large sauropods probably digested their forage with a
similar efficiency to many extant mammalian herbivores.
Other strategies observed in mammals, such as very
inefficient fibre digestion offset by very high forage intake
rates (in giant pandas, Ailuropoda melanoleuca), appear unlikely
for sauropods—or they would have been particularly
habitat-destructive and would not plot above the regression
line in Burness et al. (2001) (Fig. 3). Such a presumed ‘efficient
digestion’ in sauropods would entail long ingesta retention
times, which may have allowed the exploitation of resources
that were not attractive to smaller animals (Franz et al., 2009).
A case in point is the slow energy release pattern observed for
Araucaria as discussed above (Hummel et al., 2008) (Section
V.2a).
(4) Avian-style respiratory system
Increased oxygen uptake by the lungs of a sauropod dinosaur
compared to a mammal of the same size would potentially
allow gigantism. The tissues would be supplied with more
oxygen, allowing a higher growth rate and a faster cell
metabolism, making the organism work more efficiently on
the same resources. Such a highly effective lung is seen in
modern birds which extract about twice as much oxygen per
unit air volume as mammals do. Two features of the avian
lung make this possible: the air sac system which continuously
provides fresh air to the parenchymal tissue of the lung and
the crosscurrent gas exchange in this tissue (Perry, 1983,
1989, 1992).
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
Biology of the sauropod dinosaurs
Perry (1983, 1989, 1992) originally hypothesized that some
saurischian dinosaurs had avian-style lungs. In recent years
this has been generally accepted for the theropod lineage
(Perry, 2001; O’Connor & Claessens, 2005; O’Connor, 2009)
based on careful anatomical observations of pneumaticity
in the skeleton and on phylogenetic arguments with birds
as surviving theropod dinosaurs (O’Connor & Claessens,
2005; O’Connor, 2009). In the sauropodomorph lineage of
Saurischia, a consensus is also emerging that the great extent
and specific pattern of pneumatization of the precaudal part
of the axial skeleton is evidence for an air sac system (see
above, Perry, 2001; Wedel, 2003a, b, 2005, 2009; O’Connor
& Claessens, 2005; Schwarz & Fritsch, 2006; Schwarz et al.,
2007a; O’Connor, 2009). Thus, a hypothetical avian-style
lung in sauropods is compatible with the evidence (Perry &
Reuter, 1999).
Applying this insight to a mathematical model leads to the
recognition that an avian-style lung in sauropod dinosaurs
indeed would have greatly increased respiratory efficiency
(Perry et al., 2009, in press). In addition, a highly efficient
avian-style lung would mean that the volume of the gas
exchange part (exclusive of the air sacs) would be small, and
gravitational influence on the respiratory system even of a
large sauropod would not be constraining (Perry & Reuter,
1999). This is because of the small vertical extent of an avianstyle lung which obviates the need to raise the blood within
the lung against gravity. This presents a problem in very
large mammals such as elephants and led to the evolution of
special support structures (Perry et al., 2009, in press).
VII. FEWER RESOURCES USED
In order to understand fully the importance of reduced
resource use for sauropod gigantism, the energy budget of
a living sauropod dinosaur would have to be reconstructed,
as attempted by Weaver (1983). However, the different
pathways of energy uptake and energy expenditure are now
known to be much more complex then envisaged by Weaver
(1983). While highly desirable, quantification remains the
subject of future research and qualitative considerations
must suffice here.
The energy budget of an animal is divided into consumption of energy for growth, maintenance, thermoregulation,
support, locomotion, respiration, feeding, and reproduction.
In the following, we evaluate the possible ways that sauropod
dinosaurs could have conserved energy through evolutionary innovations and scaling effects and thus made better use
of the resources available to them than similar-sized mammalian megaherbivores and ornithischian dinosaurs would
have been able to.
(1) Reduction in body density
Body mass (and its distribution) fundamentally influences the
static and kinetic energy requirements of an organism, and
the reduction of body mass relative to linear dimensions,
143
i.e. reduction of specific body density, will convey a major
energetic advantage (and thus selective advantage, Currey
& Alexander, 1985; Wedel, 2005, 2009). This leads to the
hypothesis that reduction in specific body density made
the gigantism of sauropod dinosaurs possible. Bone, being
the densest tissue in the skeleton and also the one that is
most accessible to palaeontologists, is the obvious focus for
testing this hypothesis. One way to reduce skeletal mass is to
evolve particular light-weight constructions and the other is
to evolve materials of superior strength.
(a) Superior skeletal materials
This hypothesis can be framed as follows: sauropod bone
tissue may differ at one or more hierarchical levels in its
physical properties from that of other tetrapod bone, making
it significantly stronger mechanically. This, in turn, would
allow more slender or thinner bones and result in a lower
specific density of the animal.
The hypothesis was tested using the approach of materials
science, where materials are investigated for their structure at
all hierarchical levels, from shape to nanostructure. Pyzalla
et al. (2006a, b) and Dumont et al. (2009, in press) have
recently taken this materials science approach to sauropod
bone, focusing on primary fibrolamellar bone, the dominant
tissue type in the cortex of sauropod long bones (Klein &
Sander, 2008; Sander et al., in press b). They compared
sauropod primary fibrolamellar bone to fibrolamellar and
Haversian bone in large mammals using X-ray diffraction,
proton-induced X-ray emission (PIXE) spectroscopy, and
other methods for eludicating hierarchical structure. These
methods indicate that sauropod bone retains its original
crystallite orientation and that its microstructure at the
different hierarchical levels appears to be the same as that of
modern bone. Current evidence thus rejects the hypothesis
that sauropod dinosaur bone was an unusually high-strength
material.
(b) Light-weight construction
Light-weight constructions are well known in nature and
have frequently evolved, their study being a focus of the
field of biomechanics. With the discovery of the cavernous
nature of the cervical and dorsal vertebral column in all
but the most basal sauropods, it has been argued that
the sauropod vertebral column was such a light-weight
construction. However, only through the more detailed study
of vertebral pneumaticity enabled by computed tomography
(Wedel, 2000a, 2003b, 2005, 2009; Schwarz & Fritsch,
2006; Schwarz et al., 2007a) and histology (Woodward &
Lehman, 2009), has the quantification of weight reduction
in the vertebral column been possible (see section I.3).
The extensive air sac system of sauropods with diverticula
invading most of the presacral vertebral column and the ribs
resulted in a specific body density of 0.8 kg L−1 , with certain
parts such as the neck having a value of 0.6 kg L−1 only
(Henderson, 2004; Wedel, 2005; Schwarz & Fritsch, 2006).
This is also expressed as a body mass reduction by 8–10%
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
144
in volume-based estimates (Wedel, 2005). The hypothesis
that the light-weight construction of the axial skeleton of
sauropods contributed to their gigantism thus is supported.
Interestingly, the largest land mammal, Paraceratherium, had
pleurocoel-like openings in the presacral vertebrae, but it
is not known what these were filled with and whether they
contributed to lightening the skeleton.
(2) Reduced cost of locomotion
Locomotor activity of an animal represents one of the most
important components of its energy budget (Biewener, 2003),
leading to the hypothesis that improved scaling of the cost
of locomotion would have allowed sauropod gigantism by
slowing down the increase in overall energy uptake with
evolutionarily increasing body size. In addition to scaling
effects, design of the locomotory apparatus needs to be taken
into consideration. While the cost of transport will decrease
per unit of body mass (Langman et al., 1995; Alexander,
2006), this relationship has not been studied quantitatively in
sauropods. As graviportal animals with long legs, the general
sauropod locomotory design resembles that of graviportal
mammals, leaving scaling effects as the greatest potential
energy savings. Since much of locomotion in sauropods may
have been linked to feeding (protection from predators not
having been an issue), locomotion and the the long neck
should be considered together (see Section VI.1).
(3) Reduced cost of respiration
In addition to providing the organism with more oxygen
(see Section VI.4), better oxygen uptake through a bird-like
respiratory system would translate into energy conservation
because breathing involves muscular work and thus energy
consumption. However, the contribution to the energy
budget of a living sauropod would have been relatively
small because the muscles involved in breathing would have
been only a small fraction of the muscle mass of the animal.
Furthermore, the presence of large air sacs would result
in a low-frequency breathing pattern. Birds have a greater
tidal resting volume and lower breathing frequency than
mammals of the same body mass. Since the work of breathing
and its energetic cost is directly proportional to breathing
frequency and inversely proportional to the compliance of
the respiratory system, an avian-like lung-air-sac system in
a sauropod would be extremely energy-efficient to operate.
The result in the case of a bradymetabolic homoiothermic
giant sauropod would be an extremely low energetic cost of
breathing per unit time compared with extant mammals and
birds (Perry et al., 2009). In a tachymetabolic homoiotherm,
the energetic cost of breathing per unit oxygen acquired
would be absolutely higher, because of the higher metabolic
rate, but relatively still much lower than in a mammal-like
lung.
(4) Lower basal metabolic rate and gigantothermy
Body heat, whether generated metabolically (as in
endotherms) or being taken up from the environment
P. Martin Sander and others
(as in ectotherms), is central to the energy budget of an
animal. If sauropods had a lower BMR than mammalian
herbivores in extant ecosystems, it would have allowed the
former to evolve a larger body size (see also Burness et al.,
2001; McNab, 2009). A lower metabolic rate would not
have triggered gigantism in itself, but rather permitted
other evolutionary factors to push body size to extremes
(McNab, 2009). However, the hypothesis of a lower BMR is
contradicted by ample evidence (as reviewed in Section II.11)
for sauropods having been tachymetabolic endotherms, at
least during the phase of active growth lasting for most of
their life history. Specifically, as noted by McNab (2009),
a hypothetical sauropod dinosaur with a basal metabolic
rate of a varanid cannot be reconciled with the high
growth rates inferred for sauropods. Although energetic
scaling effects and gigantothermy may have represented
a contributing factor to gigantism, saving resources by
having been bradymetabolic throughout ontogeny as the
explanation for sauropod gigantism thus must be rejected
(contra McNab, 2009). This hypothesis is open to further
testing by a comprehensive model of the energy budget of a
living sauropod, including the potentially drastic reduction
in BMR during ontogeny.
(5) Reduced cost of reproduction
Another important part of the energy budget of an animal
is taken up by reproduction, albeit with a more episodic
energy expenditure. It thus could be hypothesized that
sauropod dinosaurs employed a more energy-efficient mode
of reproduction than other dinosaurs and large mammals.
This would have to be sought in the ovipary of sauropods
and possibly in the relatively minute eggs they produced
(Case, 1978; Weishampel & Horner, 1994; Sander et al.,
2008). Available evidence consists of the eggs and clutches
of the Late Cretaceous fossil egg taxon Megaloolithus which
occurs around the world, particularly in Europe, India, and
Argentina. All except the Argentinian eggs were buried in
the substratum or under plant matter and are found in
small clutches of less than ten eggs (Sander et al., 2008). If
only one clutch was produced by the female each season,
this would amount to a very small parental reproductive
investment, especially since any form of parental care
appears unlikely (Mueller-Töwe et al., 2002; Sander et al.,
2008). Charnov, Warne & Moses (2007) showed that the
average lifetime reproductive effort [LRE, defined as (litters
or clutches per year) x (litter or clutch size) x (average adult
life span) x (offspring mass at independence/adult mass at
first reproduction], where the latter quotient measures the
degree of parental care on average does not differ between
mammals and lizards, and thus LRE is approximately similar
in these major vertebrate groups. Based on the comparison
with modern species, we reject the hypothesis of more
energy-efficient reproduction in sauropods. Nevertheless
reproduction and life history are important in understanding
sauropod gigantism.
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Biology of the sauropod dinosaurs
VIII. FASTER POPULATION RECOVERY
AND FASTER INDIVIDUAL GROWTH
(1) Ovipary and gigantism
Their oviparous, more r-selected mode of reproduction
(Section II.11) may have been a major contributing factor
to sauropod gigantism. This hypothesis was first advanced
by Janis & Carrano (1992) for dinosaurs in general (see also
Farlow, 1993) and later applied specifically to sauropods by
Paul (1994, 1997b). Based on a large dataset of number
of offspring versus body mass for mammals and birds, Janis
& Carrano (1992) noticed that the number of offspring
decreased significantly with body size for mammals while
this was not the case in birds, where it remained constant.
They then hypothesized that because all dinosaurs were
oviparous, the same relationship might have applied, and
that ovipary enabled dinosaurs to achieve a greater body
mass than mammals because the greater reproductive output
of large dinosaurs led to a lower risk of chance extinction
than for similar-sized mammals.
Further support for their hypothesis comes from other
macroecological analyses. Positive correlation of clutch size
and body size is documented for turtle species (Frazer, 1986),
for snakes (Ford & Seigel, 1989) and for reptiles in general
(Blueweiss et al., 1978; King, 2000). No relationship was
found for galliform birds (Kolm et al., 2007), as was stated by
Janis & Carrano (1992). The difference between reptiles and
birds may be explained by their internal thermal conditions
(Shine, 2005). The data for modern reptiles also show that
increasing clutch size with increasing body size alone is
insufficient to explain gigantism (otherwise there would be
widespread gigantism in modern reptiles).
The argument of Janis & Carrano (1992) is linked to
the selective disadvantages of large body size (Blankenhorn,
2000; Hone & Benton, 2005), specifically that large body size
increases the risk of extinction of a species. This is because
long generation times decelerate evolutionary adaptation
processes, and the increased demand for resources of the
individual will lead to lower population densities. The
increased risk of demographic population extinction caused
by low densities is also at the centre of the hypothesis of
Burness et al. (2001) that maximum body size is limited by
land mass size. The hypothesis of Janis & Carrano (1992)
lends itself to a modelling test using evidence for sauropod
reproduction and population turnover that has become
available since their study (e.g. Erickson, 2005; Sander et al.,
2008) and combining it with the body-size-area relationship
of Burness et al. (2001). However, in a qualitative fashion
we already identify the production of many small offspring
allowing fast population recovery as an important factor
contributing to sauropod gigantism.
(2) Survivorship, high growth rate, and high BMR
Adult sauropods presumably were almost immune from
predation because their body mass was an order of magnitude
greater than that of the largest predators. Their sheer volume
145
made it difficult for an attacker to place an effective bite
rather than scratch the skin (Preuschoft et al., in press).
With sauropod hatchlings being so small, there must have
been strong selection pressure for high juvenile growth rates
because they would have shortened the time during which the
young sauropods were endangered by predators. Selection
for high growth rates would have been particularly strong
without parental care. In more general terms, a high growth
rate fueled by a high BMR are prerequisites to giant body
size because tetrapods with a low BMR grow too slowly
to benefit from the selective advantages of large body size.
A high, i.e. mammalian or bird BMR thus emerges as a
prerequisite for gigantism, while a reptilian BMR limits body
size to around 1 t under current environmental conditions
(Makarieva et al., 2005; Head et al., 2009).
IX. HISTORICAL CONTINGENCY
In addition to hypotheses addressing sauropod gigantism
from a bauplan limitation or a resource perspective, there
have been repeated attempts in the literature to explain this
phenomenon as the result of a historical evolutionary process.
However, these hypotheses suffer the general problem of
historical hypotheses in that they may explain how a certain
species or group outcompeted another one but not why
sauropods were ‘uniquely free of the size constraints evident
in other groups’ (Carrano, 2006, p. 24).
(1) Decreased oxygen content of atmosphere
Ward (2006) and Berner et al. (2007) suggested that
the evolutionary success of the Saurischia in the Late
Triassic, replacing rhynchosaurs as the major herbivores
and therapsids and crurotarsan archosaurs as the major
carnivores (Benton, 1990), was made possible by the avianstyle respiratory system of the early saurischians. The Late
Triassic was the time of the lowest atmospheric oxygen
levels of the entire Phanerozoic, and the ability of taking
up twice as much oxygen than other tetrapods would have
been of great selective adavantage. This hypothesis is in
accordance with several observations, e.g. both sauropods
and theropods increased in body size very rapidly compared
to ornithischian dinosaurs, and saurischian dinosaurs
dominated the Jurassic faunas. However, as noted above,
there is no positive evidence that basal sauropodomorph
dinosaurs (prosauropods) had an air sac system and hence
bird-like lungs (Wedel, 2007), although their presence might,
of course, be reconstructed on phylogenetic grounds.
(2) Poor food quality
Midgley et al. (2002) proposed that the low food quality
of the pre-angiosperm vegetation would have driven the
evolutionary increase of sauropod body size. Their hypothesis
is based on the observation that in living mammals large body
size correlates with low food quality. Implicitly they argue
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
146
that the evolution of animals larger than the largest mammals
was driven by the need for prolonged retention times of the
low-quality fodder in ever larger guts which led to ever longer
retention times. However, this hypothesis has flaws. First, the
laboratory experiments of Hummel et al. (2008) have shown
that many pre-angiosperm plants are no less nutritious
than angiosperms. Second, sauropod dinosaurs continued
to thrive in a world populated by angiosperms, i.e. during
the Late Cretaceous. In addition, there is no evolutionary
response to the mid-Cretaceous floral turnover in terms of
a size decrease in sauropods (Barrett & Upchurch, 2005).
Finally, the premise of Midgley et al. (2002) that retention
time increases with body size may not be well supported
(Clauss et al., 2007; see also Section VI.3). We thus reject the
hypothesis of Midgley et al. (2002).
X. DISCUSSION
We are now able to identify those hypotheses that may
explain gigantism and those that probably do not, based on
a current (2010) understanding. This leads to the recognition
that the gigantism of sauropod dinosaurs was made possibly
by a unique combination of two retained plesiomorphies and
three key evolutionary innovations (Fig. 9).
Probably the most conspicuous features of the sauropod
bauplan, the very long neck, was the first key innovation in
the evolution of gigantism. Its importance is supported by
observations that the group with relatively and absolutely
shortest necks, the Dicraeosauridae and Rebbachisauridae
were significantly smaller than all other sauropod groups
(Upchurch et al., 2004; Sereno et al., 2007), i.e. that
neck length scales with positive interspecific allometry
(Parrish, 2006). The long neck allowed exploitation of food
inaccessible to smaller herbivores and a much larger feeding
envelope than in a short-necked animal and thus significantly
decreased the energetic cost of feeding (Stevens & Parrish,
1999; Preuschoft et al., in press; Seymour, 2009a). It also must
have been advantageous in that it greatly increased body
surface area and thus the heat loss capacity of an exercising
sauropod. The evolution of a long neck was biomechanically
possible in sauropodomorphs because the head was small,
not serving in mastication of the food, but only for gathering
it. Non-mastication is the first of the plesiomorphic conditions
retained in sauropods.
Mammals, on the other hand, were prevented from
evolving long necks in large forms by their extensive
mastication which necessitates a relatively large head to
accommodate the dentition, a very strong masticatory
musculature and very strong (=heavy) bony elements to
sustain the resulting stresses, particularly as body size
increases. As in mammals, extensive mastication of plant food
in the major ornithischian dinosaur lineages Ornithopoda
and Ceratopsia may have placed a constraint on their
body size. Other, less obvious constraints originating from
mastication were discovered through the fermentation
experiments of Hummel et al. (2008). In these experiments,
P. Martin Sander and others
Equisetum had the highest energy content of any of the
non-angiosperm plants. While disadvantageous to mammals
because of their abrasiveness on chewing teeth, sauropods
could extensively have relied on this resource because of their
lack of mastication. This view is supported by recent work on
the scaling and interplay of gut contents, food retention time,
food intake rate, and degree of particle reduction that shows
that sauropods could have compensated for large ingesta
particle size with long retention times (Clauss et al., 2009;
Franz et al., 2009).
The other major factor allowing the evolution of the long
sauropod neck was their hypothesized avian-style respiratory
system, which positively affected neck length in two ways:
by allowing extremely light construction (Wedel, 2003b,
2005) and by solving the problem of tracheal dead space
(Wedel, 2003b, Perry et al., 2009, in press). The lightweight construction of the neck resulted from the extensive
pneumatization of the neck vertebrae originating from the
invasion of the axial skeleton by diverticula of cervical air
sacs. Only with the storage capacity provided by the air sacs,
could the problem of tracheal dead space facing long-necked
mammals such as giraffes (Perry, 1983, 1992; Daniels &
Pratt, 1992; Calder, 1996; Hengst et al., 1996; Paladino et al.,
1997; Paul, 1998) be overcome.
Beyond facilitating the evolution of the long neck, the
hypothesized bird-like respiratory apparatus offers additional
advantages, emerging as the second key evolutionary
innovation. These advantages include (a) pneumatization
originating from air sacs greatly lightened the dorsal axial
skeleton of the trunk without compromising its strength
(Wedel, 2005). (b) The continuous-flow, cross-current lung
would have increased oxygen uptake twofold per unit air
breathed compared to the ventilated pool model of the
mammalian lung (Fedde, 1990). This would have decreased
the energetic cost of breathing while at the same time
supplying the tissues with adequate oxgen. (c) The large
internal surface of the trachea and air sacs in contact
with the viscera and the neck would have provided ample
possibility for excess heat loss which then was removed
by exhalation from the body. An effective internal cooling
mechanism presumably was crucial for sauropods during
the phase of active growth when they had a high basal
metabolic rate (Fig. 9C). We note that a respiratory system
analogous to that of birds was recently hypothesized to
have permitted gigantism in flying reptiles, the pterosaurs
(Claessens, O’Connor & Unwin, 2009)
Ovipary is the second plesiomorphy retained in sauropods
that permitted gigantism because it led to higher population
recovery rates in these dinosaurs than in megaherbivore
mammals (Janis & Carrano, 1992). As noted by Farlow,
Dodson & Chinsamy (1995), the hypothesis of Janis &
Carrano (1992) would predict gigantism in Tertiary birds
in the form of multi-tonne ground birds. Since such animals
did not evolve, other constraints may have been effective,
such as the obligatory bipedalism of birds or competition
from mammals.
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
Biology of the sauropod dinosaurs
147
Fig. 9. Flow chart of the evolutionary cascade leading to sauropod gigantism. The green boxes contain the biological properties
of sauropods, and the black arrows indicate primary evolutionary causation. Theropod predation pressure is depicted as a
representative selection factor for body size increase. In addition to primary evolutionary causation, sauropod gigantism was also
driven by evolutionary feedback loops (blue arrows). The blue boxes indicate the selective advantage in the feedback loop. The boxes
on the black arrows show the selective advantages conferred on sauropods by the biological properties. BMR, basal metabolic rate.
From arguments rooted in evolutionary ecology, the high
metabolic rate of sauropods is identified as the third key
evolutionary innovation permitting gigantism because it
fueled the high growth rate required by young sauropods to
survive to sexual maturity (Dunham et al., 1989). The high
growth rate also increased population recovery rate because
the numerous sauropod offspring must have grown quickly to
reach sexual maturity. The low growth rate of ectothermic
reptiles thus provides one explanation why lineages such
as turtles and crocodiles were prevented from evolving
to dinosaurian body size despite their positive scaling of
offspring number with body size (Griebeler & Werner, in
press).
Scaling effects (Alexander, 1989, 1998, 2006) will also have
played an important role in sauropod gigantism, in particular
with regard to locomotory efficiency and thermometabolism
as detailed above, but may have been insufficient to release
other constraints on body size by themselves. In addition,
scaling effects would be insufficient to explain sauropod
gigantism, since they would apply to other taxonomic groups
as well.
This review rejects a number hypotheses about sauropod
gigantism: there is no evidence for a higher atmospheric
oxygen level during the Mesozoic than today. A higher
level is not necessary for the sauropod body plan to
function (contra Hengst et al., 1996), assuming that sauropods
possessed a bird-like respiratory apparatus. Higher ambient
temperatures are also unlikely to have contributed to
sauropod gigantism because there is no evidence that they do
in modern endothermic tetrapods. Higher plant productivity
caused by increased levels of atmospheric CO2 was at least
partially offset by the decreased nutritious value of the plant
matter. Finally, on the biotic side, there is no indication that
sauropod bone tissue had mechanical properties superior
to the fibrolamellar and secondary bone tissue of large
mammals and that sauropods invested less energy into
reproduction than other animals.
A major problem with virtually all hypotheses invoking
different boundary conditions to explain gigantism is that
their variation through Mesozoic time does not correlate
with body size evolution in Sauropoda, nor with their
diversification (Upchurch & Barrett, 2005). In particular,
sauropod body size evolution neither tracks atmospheric
oxygen levels, nor atmospheric CO2 levels, nor global
temperature curves (Fig. 8). The only physical parameter that
seems to be reflected in sauropod body size evolution is land
mass size. This may be the explanation for the observation
by Upchurch & Barrett (2005) that there appears to be a
correlation between sauropod diversity and sea level. These
authors, did not, however, test for a correlation between land
mass size and sauropod diversity.
The goal of future work must be a model of the energy
budget of a living sauropod and its comparison with that
of large mammals. These data can then be combined with
Biological Reviews 86 (2011) 117–155 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
P. Martin Sander and others
148
information on land mass size (Burness et al., 2001) and
carrying capacity to detect a possible coupling of land area
and body mass in sauropod dinosaurs. We are not yet able
to quantify the relative contributions of the three factors
more resources available, fewer resources used, and reproduction mode
(Fig. 7) to the solution to the land area versus body size enigma
because in addition to data about the enery budget of a living
sauropod, this will require understanding the energy flow in
a sauropod ecosystem.
XI. CONCLUSIONS
(1) Sauropod dinosaurs as the largest terrestrial animals
ever represent a challenge to evolutionary biologists
trying to understand body size evolution.
(2) The study of the upper limit of body size must
address extrinsic as well as intrinsic factors, and it
must be determined whether this limit is set by
the bauplan of the organisms or by physical and
ecological constraints imposed by the environment.
Among several possible approaches, we chose the
resource perspective because it has been shown that
resource availability and maximal body size correlate
closely (Burness et al., 2001).
(3) In the interplay of the biology of sauropod dinosaurs
with their environment, a unique combination of
plesiomorphic features (i.e., inherited from their
ancestors) and evolutionary novelties emerge as the key
for a more efficient use of resources by sauropods than
by other terrestrial herbivore lineages. Plesiomorphic
features of sauropods were many small offspring, the
lack of mastication and the lack of a gastric mill.
The evolutionary innovations were an avian-style
respiratory system and a high basal metabolic rate.
(4) We posit that the long neck of sauropods was central to
the energy-efficient food uptake of sauropods because
it permitted food uptake over a large volume with a
stationary body.
(5) In the Late Triassic and Early Jurassic (210–175 million years ago), the combination of biological
properties listed above led to an evolutionary cascade
in the sauropodomorph lineage characterized by
selection for ever larger body size, mainly driven by
predation pressure from theropod dinosaurs.
(6) From the Middle Jurassic onward, sauropod dinosaurs
dominated global terrestrial ecosystems only to
succumb to the catastrophic environmental change
at the end of the Cretaceous 65 million years ago.
XII. ACKNOWLEDGMENTS
P. M. S. would like to thank all members of the Research
Unit 533 for the very stimulating discussion over the last
six years. The writing of this manuscript was a joint
effort, and authors contributed their expertise as follows:
phylogeny, evolution and diversity: O. Rauhut, K. Remes,
P.M. Sander; biomechanics and functional morphology:
A. Christian, R. Fechner, H. Mallison, H. Preuschoft,
O. Rauhut, K. Remes, U. Witzel; physiology and mass
estimates: A. Christian, H.-C. Gunga, S.F. Perry, P.M.
Sander, T. Tütken; nutrition and digestive system: M.
Clauss, C.T. Gee, J. Hummel, O. Wings, T. Tütken;
respiratory biology: S.F. Perry; reproductive biology: E.M. Griebeler, P.M. Sander. K.R. drafted Figs 1 and 3–5.
P.M.S. drafted Figs 2 and 7–9. O.W.M.R. drafted Fig. 6.
We thank Sebastian Marpman (University of Bonn) for
compiling and editing the references and compiling the
data in Table 1. The manuscript was much improved by
two anonymous reviews as well as the efforts of the copy
editor. Generous funding was provided by the Deutsche
Forschungsgemeinschaft (DFG) through its Research Unit
533. This is contribution no. 85 of the DFG Research Unit
533 ‘‘Biology of the Sauropod Dinosaurs: The Evolution of
Gigantism’’.
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