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(2013). Inter-Vertebral Flexibility of the Ostrich Neck: Implications for Estimating Sauropod Neck Flexibility Cobley, M. J., Rayfield, E. J., & Barrett, P. M. (2013). Inter-vertebral flexibility of the ostrich neck: implications for estimating sauropod neck flexibility. PLoS ONE, 8(8), [ e72187]. https://doi.org/10.1371/journal.pone.0072187 Publisher's PDF, also known as Version of record License (if available): CC BY Link to published version (if available): 10.1371/journal.pone.0072187 Link to publication record in Explore Bristol Research PDF-document This is the final published version of the article (version of record). It first appeared online via PLOS at http://dx.doi.org/10.1371/journal.pone.0072187 Please refer to any applicable terms of use of the publisher. University of Bristol - Explore Bristol Research General rights This document is made available in accordance with publisher policies. Please cite only the published version using the reference above. Full terms of use are available: http://www.bristol.ac.uk/red/research-policy/pure/user-guides/ebr-terms/ Inter-Vertebral Flexibility of the Ostrich Neck: Implications for Estimating Sauropod Neck Flexibility Matthew J. Cobley1*¤, Emily J. Rayfield1, Paul M. Barrett2 1 School of Earth Sciences, University of Bristol, Bristol, United Kingdom, 2 Department of Earth Sciences, The Natural History Museum, London, United Kingdom Abstract The flexibility and posture of the neck in sauropod dinosaurs has long been contentious. Improved constraints on sauropod neck function will have major implications for what we know of their foraging strategies, ecology and overall biology. Several hypotheses have been proposed, based primarily on osteological data, suggesting different degrees of neck flexibility. This study attempts to assess the effects of reconstructed soft tissues on sauropod neck flexibility through systematic removal of muscle groups and measures of flexibility of the neck in a living analogue, the ostrich (Struthio camelus). The possible effect of cartilage on flexibility is also examined, as this was previously overlooked in osteological estimates of sauropod neck function. These comparisons show that soft tissues are likely to have limited the flexibility of the neck beyond the limits suggested by osteology alone. In addition, the inferred presence of cartilage, and varying the inter- vertebral spacing within the synovial capsule, also affect neck flexibility. One hypothesis proposed that flexibility is constrained by requiring a minimum overlap between successive zygapophyses equivalent to 50% of zygapophyseal articular surface length (ONP50). This assumption is tested by comparing the maximum flexibility of the articulated cervical column in ONP50 and the flexibility of the complete neck with all tissues intact. It is found that this model does not adequately convey the pattern of flexibility in the ostrich neck, suggesting that the ONP50 model may not be useful in determining neck function if considered in isolation from myological and other soft tissue data. Citation: Cobley MJ, Rayfield EJ, Barrett PM (2013) Inter-Vertebral Flexibility of the Ostrich Neck: Implications for Estimating Sauropod Neck Flexibility. PLoS ONE 8(8): e72187. doi:10.1371/journal.pone.0072187 Editor: Richard J Butler, University of Birmingham, United Kingdom Received April 19, 2013; Accepted July 5, 2013; Published August 14, 2013 Copyright: ß 2013 Cobley et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was completed as part of an MSc thesis at the University of Bristol, UK. No outside funding was received. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] ¤ Current address: Department of Biology, University of Utah, Salt Lake City, Utah, United States of America Introduction their relatively short necks, sauropod necks can reach up to 15 m in length [20], meaning small differences in the angle at which the The sauropods were the largest terrestrial animals ever to have neck is held can lead to differing head heights of a metre or more. existed. The clade Sauropoda, a group of saurischian dinosaurs, Sauropods display a wide array of body sizes and neck was immensely successful from the Late Triassic to the very end of morphologies, but broadly speaking if they were to have a gentle the Cretaceous, in terms of both species-richness and numerical downward curve, the heads of many sauropods would reach abundance, with representatives found on all continents [1,2]. heights of 2–4 m, whilst an extreme vertical ‘swan-like’ posture Whilst their general morphology is well understood, the issue of would lead to some species with head heights of 16–20 m their neck posture is still contentious. Some recent studies have [11,21,22]. Establishing the flexibility of sauropod necks allows proposed that the long necks of sauropods evolved by sexual estimation of the ‘feeding envelope’ of a given species. This selection [3]; however, the lack of evidence for this theory [4] envelope is the maximum range over which an individual could reinforces the long held view that long necks evolved for feed while standing still, and along with previous work on the flora maximising the feeding envelope, either for high browsing [5–7] present at the time [23–25] and sauropod dentition [11,13,26–32], or a wider lateral range of low browsing [8–10]. Species- or clade- allows an inference of possible feeding ecologies. Establishing specific variations in neck morphology have also been proposed as sauropod diet is extremely important; because sauropods were so the basis for ecologically significant differences in foraging large, adults may have required up to 400 kg of dry plant matter behaviour, mediated by changes in relative and/or absolute neck length as well as differences in neck flexion capabilities [11]. per day [24]. Reducing the resources in a given area would force Various theories on the posture and flexibility of the neck have other species present to adapt by either feeding on different been presented [8,9,11–15], with differing approaches leading to material, or through temporal or spatial niche partitioning of the various implications for overall biology. Whilst heart size and same vegetation [11]. output [16,17], the structure of the respiratory system [18,19], risk Previous work on sauropod neck posture and flexibility has of predation, and intraspecific niche partitioning [13] are all led to three general theories. Initially, qualitative 2D and 3D affected by neck function, there are also major implications for comparisons were made on sauropod cervical vertebrae in order sauropod diet and ecology [11]. Whilst neck posture and flexibility to assess the potential osteological limits of neck flexibility (e.g., in most species has relatively little effect on their ecology due to effects of zygapophyseal overlap, centrum articular surface PLOS ONE | www.plosone.org 1 August 2013 | Volume 8 | Issue 8 | e72187 Inter-Vertebral Flexibility of the Ostrich Neck morphology, cervical rib length, neural spine orientation, etc.). Materials and Methods This work suggested varying degrees of dorsoventral and mediolateral flexion in different taxa [8,9,11]. A second method Animals Studied introduced computer modelling of the neck [12]. The latter Struthio camelus was chosen as an analogue for the sauropod neck study was the first to propose that vertebrate necks are held in using the EPB approach [41,42]. Sauropods are stem avians, and an ‘osteological neutral pose’ (ONP), where two adjacent as the Struthioniformes are the largest birds to exhibit elongate vertebrae are habitually held with 100% overlap between the necks, and the overall morphologies of ostrich vertebrae and pre- and post-zygapophyses. This study also asserted that neck cervical axial musculature are broadly comparable to those of vertebrae could not be flexed beyond a minimum of 50% sauropods (in terms of musculature present, high number of overlap between the zygapophyses of adjacent vertebrae, a cervical vertebrae, presence of pneumaticity, etc.), ostriches are a measure referred to hereafter as ONP50 [12]. Application of suitable candidate for comparative study. However, it should be this method led to low flexibility estimates for sauropod necks, noted that there are some differences in inter-vertebral articula- and the conclusion that species such as Diplodocus and Apatosaurus tions between these taxa (heterocoelous in ostriches, opisthocoe- held their necks in a downward sloping fashion [12,13,21,33]. lous in sauropods) that would affect direct comparisons of their However, this work was questioned following by a study making flexibility. It is thought that ratites evolved elongate necks direct comparisons between neck postures in extant species: this independently on several occasions [43]. Three female ostrich study hypothesized that as many extant amniotes habitually necks were used in this study, donated by MNS Ostriches Ltd, hold their necks in poses that are flexed dorsally at the U.K. All three were humanely destroyed at around the same age (, 6 months). All three necks had been separated from the torso cervicodorsal junction, and that this is likely the primitive prior to being obtained; two had been pre-skinned and decapi- condition for amniotes [15]. As such it was considered most tated, whilst one had its head and skin intact. The necks were parsimonious to reconstruct sauropod necks with a more vertical frozen immediately after amputation to minimize decomposition, ‘swan-like’, ‘S’-shaped posture [15]. Thirdly, mechanical models and to reduce the effects of rigor mortis. These specimens are have also been implemented, which have supported a middle available for examination and other use via contact with the ground between these two extremes, with the neck being held corresponding author. slightly above horizontal and permitting a reasonable amount of lateral and dorsoventral flexibility [34–40].
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