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doi: 10.7717/peerj.124. Print 2013.

The variability of inner ear orientation in saurischian dinosaurs: testing the use of semicircular canals as a reference system for comparative anatomy

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The variability of inner ear orientation in saurischian dinosaurs: testing the use of semicircular canals as a reference system for comparative anatomy

Jesús Marugán-Lobón et al. PeerJ..

Abstract

The vestibular system of the inner ear houses three semicircular canals-oriented on three nearly-orthogonal planes-that respond to angular acceleration stimuli. In recent years, the orientation of the lateral semicircular canal (LSC) has been regularly used to determine skull orientations for comparative purposes in studies of non-avian dinosaurs. Such orientations have been inferred based on fixing the LSC to a common set of coordinates (parallel to the Earth's horizon), given that the orientation to gravity of this sensory system is assumed constant among taxa. Under this assumption, the LSC is used as a baseline (a reference system) both to estimate how the animals held their heads and to describe craniofacial variation among dinosaurs. However, the available data in living birds (extant saurischian dinosaurs) suggests that the orientation of the LSC in non-avian saurischian dinosaurs could have been very variable and taxon-specific. If such were the case, using the LSC as a comparative reference system would cause inappropriate visual perceptions of craniofacial organization, leading to significant descriptive inconsistencies among taxa. Here, we used Procrustes methods (Geometric Morphometrics), a suite of analytical tools that compares morphology on the basis of shared landmark homology, to show that the variability of LSC relative to skull landmarks is large (ca. 50°) and likely unpredictable, thus making it an inconsistent reference system for comparing and describing the skulls of saurischian (sauropodomorph and theropod) dinosaurs. In light of our results, the lateral semicircular canal is an inconsistent baseline for comparative studies of craniofacial morphology in dinosaurs.

Keywords: Anatomy; Dinosaurs; Geometric morphometrics; Inner ear; Reference system; Saurischia; Skull.

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Figures

Figure 1
Figure 1. Differences in reference systems in skulls.
(A) In the human skull there is a 30° difference between the Frankfurt plane and that of the LSC, thus yielding substantially different head orientations (from de Beer, 1947). (B) When a stork is in alert its LSC is oriented 19° above the horizon, thus when putting the LSC at 0° (horizontal) head posture differs from its alert posture (from Duijm, 1951).
Figure 2
Figure 2. Schematic depiction of the semicircular canals and polar histogram of LSC orientations in extant birds, measured in alert posture.
The semicircular canals are three interconnected tubes that define three nearly-orthogonal planes, and are part of the bony labyrinth of the inner ear. The measurements were obtained relative to the Earth’s horizon by Duijm (1951) when the birds were in a stereotyped alert posture at a zoological garden (n = 29). Notice that the orientation of the lagena and the cochlear duct in the vestibular apparatus normally varies among species; in our scheme they are steady for simplicity. Although the average orientation was close to zero, LSC angles when birds are in alert approximately ranges from −19° to 30° relative to the horizon.
Figure 3
Figure 3. Landmarks and Procrustes alignment of dinosaur skulls.
(A) Example of the configuration ofp = 5 landmarks in lateral view of the skull of a crocodile (C. johnstoni), as it leans on its mandibles over a flat surface. Landmarks are: 1-tip of premaxilla, 2-margin of nasal opening closer to tip of premaxilla, 3-margin of nasal opening further from tip of premaxilla, 4-junction between supraoccipital and parietal at cranial roof, 5-mandibular articulation of quadrate. In this crocodile the orientation of the LSC relative to the horizon is ∼0° (Witmer et al., 2008). (B) Superimposed configurations of landmarks using Geometric Morphometrics (Generalized Procrustes methods, or GPA). The enlarged black landmarks correspond to the Procrustes mean (the consensus reference system). Thex–y crosses at each landmark are depicted to illustrate the concomitant correspondence with the spatial directions determined by the morphological plan of the crocodile relative to the Earth’s axes.
Figure 4
Figure 4. Distribution of estimated measurements after Generalized Procrustes Analysis (GPA) of semicircular canal orientations for the studied dinosaur skulls.
In the distribution, the maximal range of angular variance spans between the skull ofNigersaurus (−51.1°) and that ofIncisivosaurus (4.6°). The schematic skulls are shown in the posture obtained by the Procrustes alignment, and LSC orientations are measured relative to the horizon and as the difference between 0° and the new GPA orientation. Obtained LSC orientations for all dinosaurs after GPA are listed in Table 1.
Figure 5
Figure 5. UPGMA phenograms grouping dinosaur skulls by geometric similarity.
Separate columns illustrate the different skull postures obtained using Procrustes methods (left column) or by aligning the LSC with the horizon (right column). The branching diagram on the right column groups skulls comparing landmark data for which only translation and scale were filtered out, but not rotation (i.e., this data includes skull posture as morphological information, determined by the LSC set to 0°). The large white dots at the nodes are highlighting cases of notable grouping differences, such as considering the skull geometry ofNigersaurus as that of either a sauropod (left) or a bizarre dinosaur (right), and that ofNanotyrannus (presumably a juvenileT. rex) as different from that ofTyrannosaurus. The grouping in the right column indicates that rotation is a main source of morphological difference among skull geometries. The numbered terminal branches denote the taxa listed in Table 1; the LSC orientation is known for those with an asterisk.
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Grants and funding

Funding for this research was provided by a Collection Study Grants of the American Museum of Natural History (New York), the MECD/Fulbright Posdoctoral Mobility Program (Spain), project DGCYT CGL2009_11838 BTE from the Ministerio de Economia y Competitividad (Spain), and the Dinosaur Institute of the Natural History Museum of Los Angeles County (Los Angeles). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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