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Data Descriptor: X-ray computed tomography library of shark anatomy and lower jawsurface models

Received: 8 December 2016

Accepted: 8 March 2017

Published: 11 April 2017

Pepijn Kamminga1,2, Paul W. De Bruin3, Jacob Geleijns3 & Martin D. Brazeau4

The cranial diversity of sharks reects disparate biomechanical adaptations to feeding. In order to be able to investigate and better understand the ecomorphology of extant shark feeding systems, we created a x-ray computed tomography (CT) library of shark cranial anatomy with three-dimensional (3D) lower jaw reconstructions. This is used to examine and quantify lower jaw disparity in extant shark species in a separate study. The library is divided in a dataset comprised of medical CT scans of 122 sharks (Selachimorpha, Chondrichthyes) representing 73 extant species, including digitized morphology of entire shark specimens. This CT dataset and additional data provided by other researchers was used to reconstruct a second dataset containing 3D models of the left lower jaw for 153 individuals representing 94 extant shark species. These datasets form an extensive anatomical record of shark skeletal anatomy, necessary for comparative morphological, biomechanical, ecological and phylogenetic studies.

Design Type(s) data integration objective species comparison design

Measurement Type(s) morphology

Technology Type(s) computed tomography

Factor Type(s) animal body part organism

whole body lower jaw region head pectoral n tail Brachelurus waddi Echinorhinus brucus Centrophorus uyato Chlamydoselachus anguineus Pristiophorus japonicus Centrophorus seychellorum

Cetorhinus maximus Orectolobus japonicus Apristurus laurussonii

Centroscymnus crepdidater Sphyrna tudes Euprotomicrus bispinatus

Etmopterus spinax Mustelus higmani Galeus melastomus Galeorhinus galeus Scyliorhinus stellaris Squatina squatina Carcharhinus leucas

Scyliorhinus canicula Chiloscyllium punctatum Halaelurus boesemani

Atelomycterus marmoratus Hemiscyllium strahani Prionace glauca

Squalus megalops Atelomycterus macleayi Carcharhinus hemiodon

Hemiscyllium trispeculare Chiloscyllium arabicum Sphyrna tiburo

Sphyrna corona Mustelus mustelus Isistius brasiliensis Scymnodalatias albicauda Deania calcea Chiloscyllium griseum Heterodontus japonicus Eusphyra blochii Sphyrna zygaena y

1Naturalis Biodiversity Center Leiden, Darwinweg 2, Leiden 2333 CR, The Netherlands. 2Institute Biology Leiden, Leiden University, Sylviusweg 72, Leiden 2333 BE, The Netherlands. 3Department of Radiology, Leiden University Medical Center, Albinusdreef 2, Leiden 2300 RC, The Netherlands. 4Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Rd., Ascot SL5 7PY, UK. Correspondence and requests for materials should be addressed to P.K. (email: mailto:[email protected]

Web End [email protected] ).

SCIENTIFIC DATA | 4:170047 | DOI: 10.1038/sdata.2017.47 1

Sample Characteristic(s)

Background & Summary

Computed tomography (CT) scanning has opened new ways for studying various parts of an organisms biology. This technique has been used in sharks to elucidate the development1, function25 and morphology of their feeding mechanics68. The majority of these studies have focused on small taxonomic subsets to gain detailed anatomical knowledge. However, phylogenetically broad statistical analyses of shark cranial mechanics are still lacking. The lead author of this work is currently undertaking such studies. This contribution provides a descriptor of a large CT dataset of shark anatomy. We used whole specimens from museum collections (a few specimens only comprise the head due to their conservation) to create a dataset of medical CT scans which covers approximately 75% of all extant shark families9.

The x-ray computed tomography library presented here was created for investigating the ecomorphological diversity of shark feeding systems. The data from the CT scans were used to create a second dataset comprising three-dimensional (3D) models of the lower jaw. These models were used to examine lower jaw disparity in extant sharks species in a separate study by quantifying jaw shape using landmark based geometric morphometrics. The lower jaw was selected because it displays a diversity of jaw morphologies between shark species1015. Lower jaws present biomechanically important features related to jaw closing mechanics and are therefore expected to function as a predictor of ecological specialisation1621.

This tomography and virtual 3D dataset can be applied to or used to supplement further comparative and functional analyses of shark morphology. These may include investigations of (a)symmetry, development, integration and modularity or shape change through evolutionary time22. Furthermore, 3D anatomical models provide an excellent visual resource for outreach and education. For example, 3D models can be integrated into 3D PDF documents as interactive gures or can be physically reproduced using rapid prototyping (also referred to as stereolithography or 3D printing)23.

Methods

Specimens

122 individuals representing 73 extant species of 25 out of 34 families from all 9 orders of extant sharks9 (Selachimorpha, Chondrichthyes) are used in the CT scan dataset (Data Citation 1). The specimens are, at the time of CT scanning, formalin preserved and stored in 70% alcohol except for 4 specimens which were stored frozen (RMNH.PISC.36345, RMNH.PISC.verznr.2, 3 and 7). All CT scanned specimens are curated in the spirit collections of the British Museum of Natural History (BMNH) and Naturalis Biodiversity Center (NBC) (see the accompanying metadata for a complete list of specimens). The NBC collections comprise material from the Rijksmuseum van Natuurlijke Historie (RMNH) and the Zologisch Museum Amsterdam (ZMA); those institutional identiers continue to be used here.

CT scanning

CT scans of the specimens housed in the NBC collections were made at the Leiden University Medical Center, the Netherlands (LUMC) with a Toshiba Aquilion 64 medical scanner (Toshiba Medical Systems, Otawara, Japan) using a for the sharks customized scanning and reconstruction protocol (100 kV tube voltage, 150 mAs tube charge per rotation, 64 active channels, acquisition and reconstructed slice thickness 0.5 mm, reconstructed slice increment 0.5 mm, FC03 reconstruction lter, pitch factor 0.83). Specimens from the BMNH collection were scanned at the CT scanning facility of the Royal Brompton and Hareeld NHS Trust (RBH), London, United Kingdom, with a Siemens Somatom Sensation 64 medical scanner using a customized scanning protocol with a variable reconstructed slice increment (100 kV tube voltage, 210 mAs tube charge per rotation, acquisition and reconstructed slice thickness1.0 mm, B30f reconstruction lter).

3D segmentations

The image series from the CT scans were imported into Mimics, v 15.01, (Materialise Software) for segmentation and 3D modelling. We used manual segmentation with a threshold edit of Hounseld units(i.e., grey values) that are associated to the calcied cartilage of the lower jaw (Fig. 1). The Hounseld units produced by the medical CT scanners are calibrated according to standard procedures of the manufacturer. The structures of calcied cartilage are not very dense in the scans (meaning relatively low hounseld units, ranging from 400 to 1,500), and at the border between calcied cartilage and soft tissue, there will always be a partial volume effect that give a 'smoothed' transition from calcied cartilage to soft tissue. Structures with high density, such as the lower jaws, are depicted bright, while structures with low or intermediate density are depicted as dark using optimized greyscales (Fig. 1a). A mask based on measured threshold values of the Hounseld units, which aligned very closely with the high relative density of the calcied cartilages of the lower jaw is set to produce an exact overlay on the slice images (Fig. 1b). We used these masks to create 3D models of the left lower jaws (Fig. 1c). Threshold values couldnt be standardised across different scans due to variable tissue densities across specimens. Most 3D models could be modeled without ambiguity. Where manual thresholds were required, ambiguity was checked against left-right symmetry of the skeleton.

SCIENTIFIC DATA | 4:170047 | DOI: 10.1038/sdata.2017.47 2

Figure 1. 3D segmentation workow in RMNH.PISC.24047 (Squatina squatina). (a) Each CT scan is build up of multiple slices (tomograms) showing structures with high attenuation of X-rays bright and structures with low attenuation dark, using a grey scale. Each pixel in the tomogram is associated with a Hounseld unit. (b) A mask (green) is superimposed on the left lower jaw. This mask is based on predetermined threshold values of the Hounseld unit of to produce an exact overlay on each tomogram. (c) When in each slice a mask is superimposed on the left lower jaw a 3D model is calculated based on the mask. The black line through the 3D model indicates the location of the tomogram in (a,b), mc l = left lower jaw.

Subsequently, each 3D model of the left lower jaw was exported as a *.PLY le from MIMICS (Data Citation 1).

Thirty-one additional 3D models of the left lower jaw were segmented using CT scans provided by other researchers (Table 1), resulting in a total of 153 3D models of 94 extant shark species.

Data Records

Data record 1The data for this manuscript have been deposited in a Figshare repository (Data Citation 1). It comprises a dataset of 121 of volumes that consist of tomography images (slices) in DICOM format reconstructed from medical computed tomography (CT) scans of sharks. The matrices of voxels in the dataset represent the Hounseld units of the corresponding materials and tissues. The Hounseld unit is associated with a well-dened physics quantity, being the linear attenuation coefcient of these materials and tissues. The majority of the data are whole body CT scans, while a few are CT scans of the head. From the CT scans we generated 153 3D models of the left lower jaws. The accompanying metadata describes the list of CT scanned specimens, their scan parameters and the derived 3D models included in Data record 1. Table 1 describes the specimen list and scan parameters of the additional 3D models of the left lower jaws that are created from CT scans provided by other researchers.

Technical Validation

CT scanner

Medical CT scanners are subject to a regular program for quality control and maintenance under the responsibility of a qualied medical physicist. However, discrepancies between the reconstructed values in an image and the true attenuation coefcients of the scanned object (i.e., image artifacts) can occur.

SCIENTIFIC DATA | 4:170047 | DOI: 10.1038/sdata.2017.47 3

Registration number

Scan dose (kV)

Scan exposure time (mAs)

Slice increment (mm)

Slice thickness (mm)

Species

Family

Sex

TL (cm)

Scanned by

Institute

Scanner

Algorithm

ERB 0854 Lamna ditropis Lamnidae f 234 F. Mollen ZNA hospital Antwerp