Scheyer & Anquetin — Pleurosternid from Kirtlington
/ 1 13
POSTPRINT
This is a postprint of the following peer-reviewed publication (definitive version available at www.blackwell-synergy.com):
Scheyer TM, Anquetin J. 2008. Bone histology of the Middle Jurassic turtle shell remains from Kirtlington,
Oxfordshire, England. Lethaia 41: 85–96.
DOI of the peer-reviewed publication: 10.1111/j.1502-3931.2007.00044.x
Bone histology of the Middle Jurassic turtle shell
remains from Kirtlington, Oxfordshire, England
Torsten M. Scheyer
1,2
*, Jérémy Anquetin
3
1
Institute of Palaeontology, University of Bonn, Nussallee 8, D-53115 Bonn, Germany
2
Current address: Paläontologisches Institut und Museum, Universität Zürich, Karl Schmid-Strasse 4, CH-8006 Zürich,
Switzerland
3
Department of Palaeontology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
*Corresponding author: tscheyer@pim.uzh.ch
Abstract
The Middle Jurassic (Bathonian) turtle material from the Mammal Bed at Kirtlington, Oxfordshire, England, has recently
been tentatively referred to the Pleurosternidae, although the known synapomorphies of this clade were absent from the
specimens. Here we present new evidence from shell bone histology that corroborates reports of pleurosternids at
Kirtlington and further reveal that two different histomorphs (= two different taxa) are present in this locality. The first
histomorph presents the distinctive histological structure of pleurosternids, which is described herein for the first time:
the external cortical bone layers are differentiated into an inner zone of coarse, irregularly interwoven structural fibre
bundles and an outer fine-fibred zone. The second histomorph has a more plesiomorphic structure and can only be
assigned to Cryptodira indet. A morphological reassessment of the Kirtlington material fails to recognize two different
taxa and shows that only sparse evidence supports the presence of pleurosternids in this locality. Shell bone histology
thus appears as a powerful tool to study poorly preserved specimens and may in some case (like with pleurosternids)
help resolve phylogenetic relationships. According to our results, the stratigraphic appearance of the Pleurosternidae is
adjusted from the Kimmeridgian (Late Jurassic) to the Bathonian (Middle Jurassic), which significantly reduces the ghost
lineage of Paracryptodira.
This work is licensed under the Creative Commons Attribution 4.0 International License.
CC-BY 4.0
© 2017 Scheyer and Anquetin
Scheyer & Anquetin — Pleurosternid from Kirtlington
/ 2 13
POSTPRINT
Pleurosternidae are well known from the Late Jurassic
and Early Cretaceous of Western Europe and North
America (e.g. Bräm 1973; Gaffney 1979a; Brinkman et al.
2000; Milner 2004), and may be also present in the Late
Cretaceous and Early Palaeocene of North America
(Hutchison & Holroyd 2003). Together with the exclusively
North American Baenidae they form the monophyletic
Paracryptodira, the sister group of the Eucryptodira (the
clade containing the crown-group cryptodires). The
Pleurosternidae primarily include the two genera Glyptops
and Pleurosternon (= Mesochelys Evans & Kemp 1975).
Based on an association of skull and shell, Brinkman et al.
(2000) included Dinochelys whitei Gaffney (1979a) (Late
Jurassic, USA) into the Pleurosternidae. Gaffney (1979a)
noted similarities between Dinochelys and Desmemys
Wegner, 1911 (Early Cretaceous, Germany), and Brinkman
et al. (2000) expressly included Desmemys within the
Pleurosternidae. Hutchison (1987) proposed a possible
relationship of Compsemys Leidy, 1856 with the
Pleurosternidae, but it is only recently that cranial
material was associated with the type species Compsemys
victa (Hutchison & Holroyd 2003).
Pleurosternidae are mainly supported by a single
synapomorphy, which is the absence of medial contact
between the pterygoids that allows the basisphenoid to
contact the vomer (Gaffney 1979a, 1996; Gaffney &
Meylan 1988; Joyce 2007). In addition, the presence of an
anterior projection of the frontals that partly separates
the nasals medially is also considered a synapomorphy of
p l e u r o s t e r n i d s ( Jo y c e 2 0 0 7 ) . P a r a c r y p t o d i r a
(Pleurosternidae + Baenidae) are supported by three
synapomorphies: (1) the reduction of the prefrontal
exposure on the dorsal surface of the skull; (2) a reduced
fenestra perilymphatica; and (3) a secondary reduction of
the supraoccipital crest ( Joyce 2007). The clade
Paracryptodira was originally based on the location of the
foramen posterius canalis carotici interni (fpcci) halfway
along the suture between the basisphenoid and the
pterygoid (Gaffney 1975). Two contradictory scenarios are
still currently debated regarding the evolution of this
character (Jamniczky et al. 2006): some authors interpret
the position of the fpcci in paracryptodires as ancestral
regarding the condition seen in eucryptodires (Evans &
Kemp 1976; Rieppel 1980; Joyce 2007), whereas others
think that the position of the fpcci evolved independently
f r o m t h e s a m e p r i m i t i v e c o n d i t i o n i n b o t h
paracryptodires and eucryptodires (Gaffney 1975, 1996;
Brinkman & Nicholls 1993). However, in the current state
of knowledge, a fpcci placed halfway along the
basisphenoid–pterygoid suture is a synapomorphy of
Paracryptodira + Dorsetochelys delairi Evans & Kemp, 1976
(Joyce 2007, p. 27).
The Middle Jurassic turtle material from the UK was
regularly referred to the pleurosternids, although often
without convincing support. The turtle known as
Protochelys Lydekker, 1889 from the Bathonian
Stonesfield Slate was placed within the pleurosternids
(e.g. Bergounioux 1955; Romer 1956, 1966), but a
reassessment of the material shows that this turtle could
either be a stem turtle, a basal pleurodire or a basal
cryptodire (Anquetin 2007). Turtle remains from the
Kilmaluag Formation (Bathonian), Isle of Skye, Scotland,
were also referred to the pleurosternids (Savage 1984);
however, we found this assignment to be incorrect and
ongoing research suggests that this turtle may be a stem
taxon (J. Anquetin, personal observation). Finally, the
turtle material from the Bathonian microvertebrate
locality of Kirtlington, Oxfordshire, was described by
Gillham (1994) and tentatively assigned to the
Pleurosternidae, although the aforementioned
synapomorphies of pleurosternids are not preserved on
the specimens. The purpose of this paper is to present
new results from bone histology that allow Gillham’s
(1994) referral to be tested.
This study is part of a larger project on the bone
microstructures of fossil and recent turtle shells (Scheyer
in press). Based on a comprehensive and representative
sampling, characteristic microstructures were found to be
apomorphic for certain turtle clades (Scheyer & Sánchez-
Villagra 2007; Scheyer et al. 2007). It was found that
Pleurosternidae share a unique shell bone histology. In a
first step, thin-sections of Glyptops plicatulus from the
Late Jurassic Morrison Formation, Wyoming, USA,
Compsemys sp. from the Early Palaeocene of the Hell
Creek Formation, Montana, USA, and Pleurosternidae
indet. from the Late Jurassic of the Guimarota Coal Mine,
Portugal, are described to illustrate the characteristic
bone histology of pleurosternid shells. In a second step,
the pleurosternid shell microstructures are compared
with those of samples from the Bathonian locality of
Kirtlington. In a third step, the anatomy of the Kirtlington
remains is reassessed in light of the new bone histological
data.
Material and Methods
To analyse the shell bone histology, standard
petrographic thin-sections were prepared of the bone
samples. The nomenclature of shell elements follows
Zangerl (1969), and the histological descriptions are
mainly based on Francillon-Vieillot et al. (1990), Scheyer &
Sánchez-Villagra (2007), and Scheyer et al. (2007). The
terms ‘costal’ and ‘pleural’, which both occur extensively in
the literature, are treated as synonymous. The terms
‘external’ and ‘internal’ are used throughout the text
Scheyer & Anquetin — Pleurosternid from Kirtlington
/ 3 13
POSTPRINT
instead of ‘dorsal’ and ‘ventral’ to prevent confusion
between dorsal carapacial and ventral plastral bones of
the turtle shell (e.g., the ‘dorsal’ surface of a carapace
bone corresponds to the external surface of the bone,
whereas the ‘dorsal’ surface of a plastral bone
corresponds to the visceral surface of the bone). The
term ‘interior’ refers to the core or centre of the shell
bone (i.e., cancellous bone) that is usually framed by the
external and internal cortex.
Glyptops plicatulus (Cope, 1877)
The studied specimens of G. plicatulus were found in
Quarry 9, Como, Wyoming, USA (Morrison Formation,
Late Jurassic). The sample comprises a neural (YPM
57160), a medial part of a costal (YPM 57161), a costal
(YPM 57162), a peripheral (YPM 57163), and a plastron
fragment (hyo- or hypoplastron, YPM 57164). The external
surface of the shell elements is sculptured with low
vermiculate ridges and tubercles framed by elongate low
ridges extending perpendicular to the plate margins.
Compsemys sp.
The material of Compsemys sp. derives from the Early
Palaeocene part of the Hell Creek Formation, McCone
County, Montana, USA. A neural (UCMP V90077/ 150197),
t w o c o s t a l s ( U C M P V 9 0 0 7 7 / 1 5 0 1 9 5 ; U C M P
V90077/150196), a peripheral (UCMP V87192/150199),
and a plastron fragment (hyo- or hypoplastron; UCMP
V87192/150198) are included. The external surface of the
shell bones is sculptured with low small tubercles that
occasionally form short low ridges. At the margins,
isolated tubercles fuse to form parallel short ridges that
extend perpendicular to the sutures of the bones. It is
noteworthy that the sculpturing pattern of these samples
is generally fainter than that of G. plicatulus.
Pleurosternidae gen. et sp. indet
Three specimens come from the Kimmeridgian (Late
Jurassic) beds of the Guimarota Coal Mine near Leiria,
Portugal (e.g. Bräm 1973; Gassner 2000). These include a
costal (GUI-CHE-53), the medial part of a costal (GUI-
CHE-54) and a plastron fragment (hyo- or hypoplastron;
GUI-CHE-55). Furthermore, two specimens, a neural
(IPFUB P-Barkas-20) and a peripheral (IPFUB P-Barkas-21),
from the Late Jurassic (Tithonian-?Berriasian) alluvial fan
deposits of Porto das Barcas, Lourinhã, Portugal, were
sampled. The external surface of the neural is weathered
and strongly pitted. The external surface of the other
shell elements is sculptured with low vermiculate ridges
and tubercles framed by low ridges extending
perpendicular to the plate margins. The internal surface
of all shell elements is smooth.
Kirtlington turtle shell material
The fragmentary turtle shell material was found in the
Kirtlington Cement Quarry (Mammal Bed, 3p layer of
McKerrow et al. 1969), Bathonian (Middle Jurassic),
Kirtlington, Oxfordshire, UK. The sample includes six
small shell fragments (IPB R583 to 589) that could only be
tentatively assigned to a location on the shell (i.e.,
carapace or plastron fragment). One of the shell bone
fragments has a sculptured external surface (IPB R586),
which is, based on its weathered state, not diagnostic.
The other fragments appear to have fairly smooth
external surfaces, but the material is also strongly
weathered.
Taxa used for comparison
The external cortex structure of the aforementioned
species has been compared with that of the following
cryptodires: aff. Naomichelys sp. (FM PR 273, TMP
90.60.07, TMP 2000.16.01; Solemydidae), Basilemys sp.
(FM P27371, TMP 80.08.296, TMP 2003.12.278, YPM 9703;
Nanhsiungchelyidae); cf. Aspideretoides sp. (IPB R533a–e;
Trionychidae); Rupelchelys breitkreutzi (SMNS 87218;
Cheloniidae sensu lato); Xinjiangchelys chowi (SGP
200134a–c; Xinjiangchelyidae) and Xinjiangchelys sp. (SGP
2002/4a–d; Xinjiangchelyidae). Note that the phylogenetic
position of Solemydidae is still unclear (Danilov 2005).
Abbreviations
BMNH, The Natural History Museum, London, UK; FM,
Field Museum, Chicago, Illinois, USA; IPB, Goldfuss-
Museum, Institute of Paleontology, University of Bonn,
Germany; IPFUB, Institut für Geowissenschaften [formerly
Institut für Paläontologie], Freie Universität Berlin,
Germany; GUI-CHE, Testudinate material from Guimarota
Coal Mine currently housed in the collections of the
Institut für Geowissenschaften – Fachrichtung
Paläontologie, Freie Universität Berlin, Germany (material
will be finally deposited in the collections of the Servicio
Geológico de Portugal, Lisboa (Geological Survey of
Portugal, Lisbon)); SMNS, Staatliches Museum für
Naturkunde, Stuttgart, Germany; SGP, Sino-German
Project, material currently housed at the Institute and
Museum of Geology and Palaeontology, University of
Tübingen, Germany; TMP, Royal Tyrrell Museum of
Palaeontology, Drumheller, Canada; UCMP, Museum of
Paleontology, University of California at Berkeley,
California, USA; YPM, Peabody Museum of Natural History
at Yale University, New Haven, Connecticut, USA.
Scheyer & Anquetin — Pleurosternid from Kirtlington
/ 4 13
POSTPRINT
Scheyer & Anquetin — Pleurosternid from Kirtlington
/ 5 13
POSTPRINT
Bone histology of pleurosternid turtles
The bone histology of G. plicatulus, Compsemys sp.,
and Pleurosternidae gen. et sp. indet. from Guimarota
and Porto das Barcas is very similar and is thus described
in one section. Variations among taxa are stated where
appropriate. All three taxa share a diploe makeup of the
shell, with well-developed external and internal cortices
framing interior cancellous bone.
External cortex
The external cortex of the shell elements of all three
taxa is formed by a thick layer of compact bone. The
cortical bone has a regular, wavy external surface
because of the regular external ornamentation pattern of
the bone. Few foramina are present in the bone tissue at
the interstitial areas adjacent to the vermiculate low
ridges and tubercles. The bone tissue consists of
interwoven structural collagenous fibre bundles, and can
be divided into two zones (Fig. 1A–C). The more external
zone is less vascularized and it is dominated by fine
interwoven structural fibre bundles. The second, more
internal zone has higher levels of vascularization and it is
characterized by coarse, irregularly interwoven structural
fibre bundles. These fibre bundles can differ significantly
in length and diameter. The thickness of the more
external zone compared to the more internal zone varies
among the taxa and is strongly dependent of surface
preservation. Growth marks are present throughout the
external cortex; however, they become more diffuse and
cannot be distinguished in the more internal zone.
Growth marks are seen as highly birefringent lines in
polarized light in Compsemys sp. but appear as dark lines
in G. plicatulus and Pleurosternidae gen. et sp. indet. from
Portugal. Besides the aforementioned foramina, the more
external zone of the external cortex is mainly avascular,
whereas the more internal zone is characterized by few
scattered primary osteons and short and round primary
vascular canals. Additionally, reticular primary vascular
canal patterns can be developed.
Cancellous bone
The cancellous bone constitutes short and thick bone
trabeculae and mostly vascular spaces of small to
medium size (generally between 0.2 and 1.0 mm in
diameter, Fig. 1D). Towards the sutured margins of the
plates, vascular spaces are often slightly externo-
internally flattened and elongated. Larger vascular spaces
of circular or irregular shape are found in the proximal
parts of the sampled peripheral and in the costal
fragments (YPM 57161 to 57163) of G. plicatulus. Whereas
a few erosion cavities lack secondary lamellar bone, the
majority of the walls of the bone trabeculae constitute
lamellar bone. Primary interstitial bone is preserved in
most trabecular branching spots, besides the very thin
trabeculae of the sampled peripheral of G. plicatulus.
Internal cortex
The internal cortex is well developed but generally
thinner than the external cortex. In G. plicatulus and
Compsemys sp., the internal cortex is usually avascular.
However, small scattered primary vascular canals (mostly
ranging between 0.01 and 0.04 mm in diameter) can be
present in the location of the incorporated rib of the
costal elements. In the sample of Pleurosternidae gen. et
sp. indet. from Portugal, the internal cortex can be weakly
vascularized with primary vascular canals. In G. plicatulus,
the internal cortex constitutes homogenous and ordered
layers of parallel fibred bone. In Compsemys sp. (Fig. 1E)
and Pleurosternidae gen. et sp. indet. from Portugal, the
fibre bundles of the parallel-fibred bone are coarser and
vary in extension and orientation, giving the bone tissue a
less ordered appearance. Sharpey’s fibres can be visible
as fibres or fibre bundles that extend perpendicular or in
angles into the parallel-fibred bone matrix.
Sutures
Sutures are generally well developed in the sampled
pleurosternid turtles. Growth marks, which are deflected
from the external cortex, can be distinguished in the
bone tissue of the sutures, thus showing an increasing
sutural relief during ontogeny. Fibre bundles that extend
Figure 1 (previous page) — Shell bone histology of pleurosternid turtle taxa (A–E) and Kirtlington histomorph I (F–H). A, B. Close-
up of the external cortex of the peripheral (YPM 57163) of Glyptops plicatulus. A. Normal transmitted light. B. Polarized light. The more
external zone of the external cortex is fine-fibred and growth marks are clearly visible, while the more internal zone is coarse-fibred and
almost completely lacks growth marks. C. Close-up of the two external cortical zones of peripheral IPFUB P-Barkas 21 of Pleurosternidae
gen. et sp. indet. in polarized light. D. Close-up of the interior cancellous bone of the plastron fragment (YPM 57164) of G. plicatulus in
polarized light. E. Detail of the internal cortex of costal UCMP V90077/150195 of Compsemys sp. in polarized light. Note Sharpey’s fibres
inserting into the parallel-fibred bone. F, G. Close-up of the external cortex of the carapace fragment IPB R586. F. Normal light. G.
Polarized light. H. Detail of the transition from interwoven structural fibre bundles to parallel-fibred bone in the internal cortex of shell
fragment IPB R583 in polarized light. Abbreviations: CL, bone cell lacunae; EC, erosion cavity; FB, fibre bundle; GM, growth mark; ISF,
interwoven structural collagenous fibre bundles; LB, lamellar bone; lsFB, longitudinally sectioned fibre bundle; PC, primary vascular canal;
PFB, parallel-fibred bone; PO, primary osteon; ShF, Sharpey’s fibres; trFB, transversely sectioned fibre bundle.
