Third Funding Period
The FOR 533 gigantism hypothesis
by P. Martin Sander
The focus of the secong funding period of our Research Unit was on sauropod gigantism, trying to understand how sauropod dinosaurs were able to evolve to a body size one magnitude larger than all other terrestrial animals before and since. The outcome is a coherent hypothesis, hereafter termed the FOR 533 gigantism hypothesis, which was first published as an essay by Sander & Clauss (2008) for the journal Science. The fact that only two of us are the authors is due to the limit on number of authors set by the journal, and we emphasize that the generation of the hypothesis was a joint effort for which all members of the Unit deserve credit. The biological foundations for our hypothesis are found in Klein et al. (2011), and the FOR 533 gigantism hypothesis is described in detail in Sander et al. (2011).
Probably the most conspicuous feature of the sauropod bauplan, the very long neck, must have been a major factor in the evolution of gigantism (Christian & Dzemski 2007, 2011). The long neck allowed for the exploitation of food that was inaccessible to smaller herbivor(Gee 2011) and for a much larger feeding envelope than in a short-necked animal, thus significantly decreasing the energetic cost of feeding (Preuschoft et al. 2011, Seymour 2009). The long neck thus represented an advantage that allowed sauropods to take up more energy from their environment than other herbivores, perrmitting a larger body size. The long neck also must have been advantageous in that it greatly increased the body surface area and thus the heat loss capacity of an exercising sauropod (Perry et al. in press). This is one of several causative evolutionary feedback loops (blue arrows and boxes in Figure 2C) that reinforced selective advantages of features already present. However, any long neck is vulnerable to predator attack. Adult sauropods, by presumably being outside of the prey spectrum of even the largest theropods, would have reduced this vulnerability by their sheer body size. This represents another feed-back loop.
The evolution of a long neck was biomechanically possible in sauropodomorphs because the head was small and did not serve in mastication of the food (Upchurch & Barrett 2000, Preuschoft & Witzel 2005, Witzel 2007, Witzel et al. 2011), but only for gathering it. This is the plesiomorphic condition in tetrapods, and its retention in sauropods was crucial to the evolution of an extremely long neck in combination with gigantic body size. In mammals, on the other hand, extensive mastication 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. It is well known that skull size in mammals shows strong interspecific positive allometry. Because of the heavy head, the mass of muscles and ligaments needed for carrying and moving the neck is much higher in mammals than it was in sauropods, greatly constraining mammalian neck length. As in mammals, extensive mastication of plant food evolved early in at least two ornithischian dinosaur lineages (Ornithopoda and Ceratopsia, see Sander et al. 2011 b) and may have placed a constraint on body size in ornithischian dinosaurs (Sander & Clauss 2008).
Other, less obvious constraints originating from mastication were understood only recently. In the fermentation experiments by Hummel et al. (2008), Equisetum had the highest energy content of any of the non-angiosperm plants. While Equisetum is disadvantageous to mammals because of its abrasiveness on chewing teeth, sauropods could have extensively relied on this resource because of their lack of mastication (Gee 2011). In comparison with sauropods it became apparent that mastication places a constraint on body size limiting food uptake rate (Sander & Clauss 2008), which is a critical factor in very large herbivores. Similarly, a gastric mill would have limited uptake rate, which is consistent with its absence in sauropods (Wings & Sander 2007). We suggest that the particle reduction produced by mastication becomes less necessary in very large animals because of the negative scaling of metabolic rate compared to the isometric scaling of gut volume (Franz et al. 2009), leading to a relatively large gut volume in which large particles could be retained for a long time (Clauss et al. 2009, Hummel & Clauss 2011). Again, high food uptake rates represent an energetic advantage, potentially allowing for larger body size. Favorable gut volume scaling thus is another feed-back loop.
The other major factor that allowed for the evolution of the long neck of sauropods was their hypothesized avian-style respiratory system (Perry et al. 2009, 2011), which positively affected neck length in two ways: through its extremely light construction (Wedel 2003a, 2005, Rauhut et al. 2005) and by providing a solution to the problem of tracheal dead space (Wedel 2003, Perry et al. 2009, 2011). The light-weight construction of the neck resulted from the extensive pneumatization of the neck originating from the invasion of the axial skeleton by diverticula of cervical air sacs. The problem of tracheal dead space facing long-necked mammals such as giraffes (Perry 1983, 1989; Hengst et al. 1996, Paladino et al. 1997) could have been only overcome with the storage capacity provided by the air sacs.
The hypothetical bird-like respiratory apparatus thus emerges as a key evolutionary innovation , offering several advantages beyond making the long neck possible: 1) The pneumatization originating from air sacs greatly lightened the dorsal axial skeleton of the trunk without compromising its strength (Wedel 2005). 2) The continuous-flow, cross-current lung would have increased oxygen uptake twofold per unit air breathed compared to the ventilated pool model of a mammalian lung . This in turn would have decreased the energetic cost of breathing while at the same time supplying the tissues with adequate oxygen (Perry et al. 2009). 3) The large internal surface of the nonvascularized air sacs in contact with the viscera and the neck would have provided ample opportunity for excess heat loss which then would have left the body by exhalation from the body (Perry et al. 2009). An effective internal cooling mechanism was presumably crucial for sauropods during the phase of active growth when they had a high basal metabolic rate (Sander & Clauss 2008, Ganse et al. 2011). The high metabolic rate, in turn, would have been necessary to fuel the high growth rate which was necessary for young sauropods to survive to sexual maturity (Dunham et al. 1989, Sander & Clauss 2008).
Higher population recovery rates in sauropod dinosaurs than in megaherbivore mammals permitted by ovipary of sauropods (Janis & Carrano 1992) in combination with their high growth rates remains a strong hypothesis for explaining sauropod gigantism (Sander & Clauss 2008, Griebeler & Werner 2011). This is supported by the much larger dataset compiled by Griebeler & Werner (2011) and ongoing work by Werner & Griebeler .
In addition to the number of offspring, ontogenetic growth rate also influences population recovery rate because the numerous offspring must grow quickly to reach sexual maturity (Griebeler & Werner 2011). Otherwise, population recovery rate will not be improved. Their low growth rate thus provides an explanation why ectothermic reptiles such as turtles and crocodiles cannot evolve to dinosaurian body size despite their positive scaling of offspring number with body size. High growth rates requiring a high BMR thus not only permit gigantism under stable ecological conditions but also high population recovery rates after a population crash and thus a larger body size because of a reduced risk of extinction. From arguments rooted in evolutionary ecology, particulary the MTE (Brown et al. 2004), the high metabolic rate of sauropods that is prerequiste to high growth rates emerges as a key innovation making gigantism possible (Sander & Clauss 2008, Sander et al. 2011a). Here we see the final feed-back loop in our hypothesis, i.e., that the negative scaling of BMR (Clauss et al. 2007) means that at a very large body mass, a high BMR will be maintained with a low mass-specific metabolic rate, meaning a relatively low energy demand.
Figure 1. The FOR 533 gigantism hypothesis visualized as an evolutionary flow chart, split into three steps of increasing complexity. A) The green boxes contain the biological properties of sauropods, and the black arrows indicate evolutionary causation.Theropod predation pressure is seen as the major selection factor for body size increase but others may have been present as well. B) Sauropod gigantism appears to also have become possible because evolutionary feed-back loops (blue arrows). The blue boxes indicate the selective advantage. C) This diagram represents the complete FOR 533 gigantism hypothesis, with diagrams A) and B) combined. The white boxes on the black arrows show the selective advantages.
The primary aim of the 3rd funding period of the Research Unit 533 is to test its gigantism hypothesis by testing its component hypotheses in the individual projects. Passing these tests will elevate the hypothesis to a theory. Beginning in the third funding period and in preparation for a future coordinated DFG or EU project, we intend to further develop our hypothesis into a theory on gigantism and the upper limits of body size in terrestrial vertebrates in general. This is an especially timely endeavor because of the possible paradigm shift in evolutionary ecology towards the metabolic theory of ecology (MTE). Our research thus will bring paleontology closer to the mainstream of evolutionary biology in Germany and elsewhere. The primary aim of the 3rd funding period of the Research Unit 533 is to test its gigantism hypothesis by testing its component hypotheses in the individual projects. Passing these tests will elevate the hypothesis to a theory. Beginning in the third funding period and in preparation for a future coordinated DFG or EU project, we intend to further develop our hypothesis into a theory on gigantism and the upper limits of body size in terrestrial vertebrates in general. This is an especially timely endeavor because of the possible paradigm shift in evolutionary ecology towards the metabolic theory of ecology (MTE). Our research thus will bring paleontology closer to the mainstream of evolutionary biology in Germany and elsewhere.
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