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Some Sauropods Raised Their Necks—Evidence for High Browsing In Biol. Lett. (2010) 6, 823–825 arguments have been put forward against the idea of doi:10.1098/rsbl.2010.0359 high browsing in sauropods. According to Stevens & Published online 2 June 2010 Parrish (1999, 2005), optimal articulation of the Palaeontology neck vertebrae and neck flexibility indicate a low neck position especially in sauropods with extremely long necks. However, Dzemski & Christian (2007); Some sauropods raised Christian & Dzemski (2007) and Taylor et al. (2009) refuted the hypothesis that the osteological neutral their necks—evidence pose was commonly adopted in life. Strong physiologi- cal arguments against high browsing have been for high browsing in formulated by Seymour (2009a,b). Seymour (2009a) Euhelopus zdanskyi points out that high browsing results in high stress on the cardiovascular system because a very high blood Andreas Christian* pressure is required for supplying the brain with Universita¨t Flensburg, Institut fu¨r Biologie und ihre Didaktik, blood if the head is several metres above the heart. Auf dem Campus 1, 24943 Flensburg, Germany According to Seymour (2009b), energy expenditures *christian@uni-flensburg.de due to a higher blood pressure increase greatly with A very long neck that is apparently suitable for feeding height, whereas maximum food intake feeding at great heights is a characteristic feature decreases, so that high browsing is not worthwhile. of most sauropod dinosaurs. Yet, it remains con- In the light of these arguments, maintaining the concept troversial whether any sauropods actually raised of high-browsing sauropods requires strong evidence. their necks high. Recently, strong physiological Such evidence is given here for Euhelopus zdanskyi arguments have been put forward against the (Wiman 1929), a moderately sized sauropod with an idea of high-browsing sauropods, because of the excellently preserved neck skeleton (Wilson & very high blood pressure that appears to be inevi- Upchurch 2009). For the much larger Brachiosaurus table when the head is located several metres brancai, biomechanical arguments also support the above the heart. For the sauropod Euhelopus zdanskyi, however, biomechanical evidence idea of high browsing (Christian & Dzemski 2007). clearly indicates high browsing. Energy expendi- Additional mechanisms like ‘neck hearts’ that might ture owing to high browsing is compared with have enabled sauropods to increase the blood pressure energy costs for walking a distance. It is demon- in the head and neck independently from the body strated for Euhelopus as well as for the much remain speculative. It will be demonstrated that even larger Brachiosaurus that despite an increase in without such mechanisms high browsing was also the metabolic rate, high browsing was worthwhile worthwhile for Brachiosaurus if food sources were for a sauropod if resources were far apart. widely spaced. Keywords: sauropod; dinosaur; neck; feeding; energy expenditures 2. MATERIAL AND METHODS Measurements of the skeletal dimensions of Euhelopus zdanskyi were taken from specimen PMU 233, exhibited at the University Uppsala, 1. INTRODUCTION Sweden. Additional data were taken from description and illus- trations by Wiman (1929). Data lacking due to damaged vertebrae Because of their extreme size, sauropods attract much were interpolated. Based on the dimensions of the neck skeleton, interest from scientists of various disciplines. The lar- the mass distribution along the neck was reconstructed under the gest sauropods might have almost reached assumption of a low neck density owing to strong pneumatization (Henderson 2004, 2006; Wedel 2005, 2009; Wilson & Upchurch biomechanical and physiological limits. Recent find- 2009; see electronic supplementary material). For different hypothe- ings indicate fast growth and high metabolic rates in tical neck postures, the stress in the intervertebral cartilage was sauropods (Sander & Clauss 2008). Consequently, calculated along the neck (Christian 2002; see electronic supplemen- the rate of food intake must have been very high. A tary material). Habitual positions of the neck at rest are characterized by approximately constant stress values along the neck (Christian selective advantage of the usually very long sauropod 2002). Body mass was assumed to equal 3.8 metric tons (Mazzetta neck for feeding appears unquestionable. Yet, the pos- et al. 2004). Energy expenditures were calculated from the literature ture and the utilization of sauropod necks remain the (Schmidt-Nielsen 1984; Seymour 2009b; White et al. 2009; see focus of a long debate. The neck may have been used electronic supplementary material). for increasing the horizontal feeding range (Martin 1987) or for high browsing (Bakker 1986; Paul 1988). 3. RESULTS Whereas most researchers agree on low browsing in The estimated combined mass of neck and head of some forms like Diplodocus, Apatosaurus (Stevens & Euhelopus was about 210 kg (see electronic supplemen- Parrish 1999)andNigersaurus (Sereno et al. 2007), tary material). With a straight neck, the distance the question remains open if any sauropod actually between the snout and the base of the neck was exploited resources at great heights. about 4.6 m. Nearly constant stress values in the inter- The assumption of ecological niche partitioning vertebral cartilage along the neck were only obtained in among sauropods (Dodson 1990) with different nearly straight neck poses with an angle between the species of the same habitat browsing at different neck and the horizontal of between 408 and 508. heights appears reasonable and fits the observed vari- Taking errors into account, especially in the estimated ation in tooth and jaw morphology (Upchurch & distribution of the neck mass, a slightly lower resting Barrett 2000; Sereno & Wilson 2005). However, position of the neck is possible, but the results are Electronic supplementary material is available at http://dx.doi.org/ neither in accordance with a fully vertical nor with a 10.1098/rsbl.2010.0359 or via http://rsbl.royalsocietypublishing.org. horizontal position of the neck (figure 1). Curved Received 15 April 2010 Accepted 12 May 2010 823 This journal is q 2010 The Royal Society 824 A. Christian High-browsing sauropods 2 100 90 80 70 1 60 stress (MPa) 50 40 energy (kJ) energy 30 20 0 1234 10 distance from the head (m) Figure 1. Stresses in the intervertebral joints along the neck 0 10 20 30 40 50 60 70 80 90 of Euhelopus zdanskyi calculated for some hypothetical neck neck inclination angle (°) postures. Inclined postures yield the least variation in stress. Slightly lower values in the foremost neck section are Figure 2. Energy expenditures for feeding at different heights usual because of additional muscle force for moving the for 5 min compared with the net energy costs for travelling head (Christian & Dzemski 2007). High values at the hind- different distances. The additional metabolic rate owing to most neck section indicate tensile structures that lay high an increased blood pressure is related to a resting posture above the vertebrae. of the neck with an inclination angle of 408 between the neck and the horizontal plane. Yellow line, raising the neck from the resting position; red line, keeping the neck for postures were also tested but did not yield constant 5 min in position; green line, energy cost of transport: walk- stress values. Neck flexibility appears to have been gen- ing distance 10 m; blue line, energy cost of transport: walking erally low, except for the most distal and proximal neck distance 20 m; dark blue line, energy cost of transport: regions, where lateral as well as dorsoventral motions walking distance 30 m. were less restricted than in the long midsection of the neck. The dorsal spines of the vertebrae are very low or even lacking at the neck–trunk transition, indicating Table 1. Estimates of time intervals for browsing with a fully an upward bend in the vertebral column and long vertical neck that are energetically equivalent to walking a distance of 100 m: T , time interval assuming a horizontal muscles or tendons that lay well above the vertebrae 1 resting position of the neck; T2, time interval assuming an in this region. inclined (408) resting position. For Euhelopus, the energy costs for walking given distances are compared with the energy expenditure T1 (min) T2 (min) for raising the neck from a horizontal to an inclined position and the energy expenditures for maintaining Euhelopus zdanskyi 11.6 32.2 a high blood pressure for 5 min during high browsing Brachiosaurus brancai 3.8 12.9 (figure 2). Mechanical work for raising the neck from an inclined to a vertical position is rather low and can be neglected if the head were raised only once mainly moving the distal parts of the neck during during the time interval. In table 1, the energy costs browsing, whereas the height of the heavy hindmost for Euhelopus and Brachiosaurus for walking a distance neck section does not change very much. This feeding of 100 m are compared with the energy expenditures strategy can be observed among living vertebrates and for high browsing starting either from a horizontal or has also been proposed for some sauropods, like from a 408 inclined position of the neck. Raising the Diplodocus carnegii (Dzemski & Christian 2007). It is neck and feeding for the time intervals given in expedient for high browsing to use the full length of table 1 would have cost approximately the same as the neck as giraffes do. For this feeding strategy, a that of walking the distance of 100 m. rather rigid neck with reduced muscle mass is advan- tageous. In Euhelopus, the very long cervical ribs allowed transmission of forces in a controlled way 4. DISCUSSION over a long distance, thus shifting the muscle mass The biomechanically reconstructed neck posture of further back towards the trunk, as suggested by Euhelopus is similar to that of a giraffe (Giraffa Christian & Dzemski (2007) for Brachiosaurus. camelopardalis). As in giraffes, the neck of Euhelopus For Euhelopus, the static analysis and the flexibility appears to have been kept rather straight, and changes pattern along the neck indicate browsing at medium in its position were mainly generated by flexion and great heights.
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