A new specimen of Manchurochelys

Zhou et al. BMC Evolutionary Biology 2014, 14:77
Open Access
A new specimen of Manchurochelys manchoukuoensis
from the Early Cretaceous Jehol Biota of Chifeng,
Inner Mongolia, China and the phylogeny of
Cretaceous basal eucryptodiran turtles
Chang-Fu Zhou1*†, Márton Rabi2,3† and Walter G Joyce4
Background: Manchurochelys manchoukuoensis is an emblematic turtle from the Cretaceous Yixian Formation of
Liaoning, China, a geological rock unit that is famous for yielding perfectly preserved skeletons of fossil vertebrates,
including that of feathered dinosaurs. Manchurochelys manchoukuoensis was one of the first vertebrates described
from this fauna, also known as the Jehol Biota. The holotype was lost during World War II and only one additional
specimen has been described since. Manchurochelys manchoukuoensis is a critical taxon for unraveling the
phylogenetic relationships of Cretaceous pancryptodires from Asia, a group that is considered to be of key
importance for the origin of crown-group hidden-neck turtles (Cryptodira).
Results: A new specimen of Manchurochelys manchoukuoensis is described here from the Jiufotang Formation of
Qilinshan, Chifeng, Inner Mongolia, China. This is the third specimen described and expands the range of this taxon from
the Yixian Formation of the Fuxin-Yixian Basin in Liaoning to the Jiufotang Formation of the Chifeng-Yuanbaoshan
Basin. A possible temporal extension of the range is less certain. The new finding adds to our understanding of the
morphology of this taxon and invites a thorough revision of the phylogeny of Macrobaenidae, Sinemydidae, and
closely allied forms.
Conclusions: Our comprehensive phylogenetic analyses of Cretaceous Asian pancryptodires yielded two main
competing hypotheses: in the first these taxa form a paraphyletic grade, whereas in the second they form a monophyletic
clade. The inclusion of problematic tree changing taxa, such as Panpleurodires (stem + crown side-neck turtles) has a major
influence on the phylogenetic relationships of Sinemydidae and closely allied forms. Manchurochelys manchoukuoensis
nests within Sinemydidae together with Sinemys spp. and Dracochelys bicuspis in the majority of our analyses.
To date, three turtle taxa have been recognized in the
Early Cretaceous Jehol Biota of western Liaoning and adjacent areas: Manchurochelys manchoukuoensis Endo and
Shikama 1942 [1]; Ordosemys liaoxiensis (Ji 1995) [2,3];
and Liaochelys jianchangensis Zhou 2010 [4]. Of these,
M. manchoukuoensis is notable because it was one of the
first tetrapod fossils to be described from the Jehol Biota,
together with the choristodere Manchurosuchus splendens
and the lizard Yabeinosaurus tenuis. Unfortunately, the
* Correspondence: [email protected]
Equal contributors
Paleontological Institute, Shenyang Normal University, 253 North Huanghe
Street, Shenyang, Liaoning 110034, People’s Republic of China
Full list of author information is available at the end of the article
holotype, a partial shell, appears to have been lost during
World War II [5]. Our knowledge regarding the anatomy
of this species was nevertheless recently expanded by the
referral of a second specimen, which consists of a nearly
complete skeleton [5], but much remains to be learned
about this taxon, in particular in regards to its skeletal
anatomy, phylogenetic relationships, and its geographic
and temporal distribution.
In the present paper, a new partial skeleton of M.
manchoukuoensis is described from a new site in the
Jiufotang Formation of Qilinshan, Chifeng, Inner Mongolia
(Figure 1). In addition to expanding the geographical distribution of M. manchoukuoensis to Inner Mongolia, this specimen is interesting because it allows a reassessment of the
© 2014 Zhou et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain
Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article,
unless otherwise stated.
Zhou et al. BMC Evolutionary Biology 2014, 14:77
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Figure 1 Map showing the known localities of Manchurochelys manchoukuoensis, in Qilinshan (=Heishangou; marked by a red asterisk;
E118°50′46.4″, N42°08′33.3″), Chifeng City, Inner Mongolia; and in Yixian (marked by a blue asterisk), Jinzhou City, Liaoning Province.
morphology and phylogenetic relationships of this enigmatic species.
Asian Cretaceous basal eucryptodires, such as M.
manchoukuoensis, are widely recognized as a critical group
for resolving the early evolution of pancryptodires [6-20], a
clade that represents about 75% of extant turtle diversity.
There currently is no consensus on the phylogenetic arrangement of Cretaceous pancryptodires, but most workers
historically distinguished two primary groups with doubtful
monophyly: Sinemydidae and Macrobaenidae [6,8-10,21-26].
There historically also was little agreement on the content of
these taxa, but recent phylogenetic definitions provided
some level of nomenclatural stability [27]. In particular,
Sinemydidae is now defined as referring to the most inclusive clade containing Sinemys lens but not Xinjiangchelys
junggarensis, Macrobaena mongolica, or any species of recent turtle, whereas Macrobaenidae is defined as referring
to the most inclusive clade containing Macrobaena mongolica but not Xinjiangchelys junggarensis, Sinemys lens, or
any species of Recent turtle. A summary of the taxonomic
history of these groups is provided in Rabi et al. [19,27].
There have been numerous attempts to resolve the phylogeny and position of Macrobaenidae and Sinemydidae,
but these either suffered from low taxon sampling and/or
lack of specific characters and/or use of literature based
data rather than actual observations on fossil specimens
[4,5,11,12,14,17,18,20,28-36]. Here, we considerably improve upon previous analyses by rescoring taxa based
on our own observations of specimens, by adding six
new taxa and new characters, and by testing for tree
changing and wildcard taxa.
The fossil described herein is housed in the Paleontological
Museum of Liaoning (= Liaoning Paleontological Museum,
PMOL), Shenyang Normal University, with the number
PMOL-AR00180. The specimen was obtained in two
blocks that were subsequently glued together during the
preparation process at PMOL. The surrounding sediment
was then removed to expose the skeleton in dorsal and
ventral views.
The following fossil taxa were studied first hand for
comparative purposes and for the phylogenetic analysis:
Dracochelys bicuspis Gaffney and Ye, 1992 [8] (IVPP
V4075 holotype); Kirgizemys (= Hangaiemys) hoburensis
(Sukhanov and Narmandakh, 1974) [6,15] (PIN 3334-4,
PIN 3334-1, PIN 3334-5, PIN 3334-16, PIN 3334-34,
PIN 3334-35, PIN 3334-36, PIN 3334-37); Judithemys
sukhanovi Parham and Hutchison, 2003 [14] (TMP 87.2.1
holotype); Liaochelys jianchangensis Zhou, 2010 [4]
(PMOL-AR00140 holotype, PMOL-AR00160); Manchurochelys manchoukuoensis Endo and Shikama, 1942 [1]
(PMOL AR00008); Ordosemys leios [10] (IVPP V9534-1
holotype, and material listed in Brinkman and Peng 1993
[10]); Sinemys gamera Brinkman and Peng 1993 [9] (IVPP
V9532-1 holotype, IVPP V9532-11 and the material listed
in Brinkman and Peng 1993 [9]); Sinemys brevispinus
Tong and Brinkman, 2013 [37] (IVPP V9538-1 holotype);
Wiman, 1930 [38] (IVPP V8755, IVPP V9533-1).
The cranial carotid circulation nomenclature follows Rabi
et al. [36] and taxonomic nomenclature follows the
phylogenetic definitions of Rabi et al. [27].
Phylogenetic analysis
Four separate phylogenetic analyses were run in order to
test the relationships of Cretaceous basal eucryptodires
from Asia and North America. All analyses used a modified
version of the latest global turtle character-taxon matrix by
Rabi et al. [36], which in turn is based on Rabi et al. [27],
Sterli and de la Fuente [20,23], Sterli [30], and Joyce [18]. In
Zhou et al. BMC Evolutionary Biology 2014, 14:77
addition to the taxa sampled in Rabi et al. [36], the matrix
includes Liaochelys jianchangensis, Changmachelys bohlini
Brinkman et al., 2013 [35], Sinemys gamera, Sinemys lens,
Sinemys brevispinus, and the skull of Ordosemys sp. [12].
The taxon Ordosemys leios is only considered to consist of
material described in Brinkman and Peng [10]. Manchurochelys manchoukuoensis was scored on the basis of three
specimens: the specimen described herein (PMOLAR00180), the one described by Zhou [5]; PMOLAR00008), and the lost holotype [1]. Several scorings were
changed for Kirgizemys hoburensis, Sinemys lens, Dracochelys bicuspis, and Ordosemys leios, among others,
based on personal observations of the relevant material
(see Appendix 1 for list of changes).
The following characters were treated as ordered: 7
(Nasal A), 19 (Parietal H), 27 (Squamosal C), 40 (Maxilla
D), 42 (Vomer A), 50 (Quadrate B + C), 52 (Antrum
Postoticum A), 59 (Pterygoid B), 81 (Opisthotic C), 82
(Opisthotic D), 89 (Stapedial Artery B), 98 (Canalis
Caroticum F), 120 (Carapace A), 121 (Carapace B), 130
(Peripheral A), 133 (Costal B), 138 (Supramarginal A), 158
(Hyoplastron B), 159 (Mesoplastron A), 161 (Hyoplastron
B), 176 (Abdominal A), 213 (Cleithrum A), 214 (Scapula
A), 232 (Manus B), 233 (Manus C). Sphenodon punctatus,
Owenetta kitchingorum, Simosaurus gaillardoti, and Anthodon serrarius were designated as outgroups.
In each analysis we omitted the following characters:
Maxilla B, Basioccipital B, Pterygoid M, and Cervical
Vertebra D and K. Maxilla B was omitted because we
cannot reproduce the meaning or scoring of this character
as provided by Sterli and de la Fuente [20]. As scored, this
character does not show any variation within Cretaceous
basal eucryptodires and we therefore do not expect any
impact from its omission.
Basioccipital B is omitted for similar reasons: the definition of a deep, C-shaped concavity on the basioccipital
is quite vague since almost all turtles with basioccipital
tubera have some sort of C-shaped concavity, but were
scored as absent by Sterli and de la Fuente.
Pterygoid M is omitted because, unlike as stated [20],
the derived state of this character (basisphenoid and
pterygoid in different levels) is present in many basal taxa
(actually being the ancestral state for turtles, e.g. Proganochelys quenstedti) and therefore the character should be
rescored in the future.
Cervical D is omitted once again because we cannot
reproduce the meaning of ‘triangular diapophysis’ and
because the current distribution of this character does
not help us either (scored as present for panpleurodires,
Chubutemys copelloi, Glyptops plicatulus and baenids).
Finally, Cervical vertebra K is omitted because we find
it redundant with Cervical Vertebra B (both characters
pertain to the depth of the ventral keel on posterior
Page 3 of 16
The taxon-character matrix, the TNT file and strict
consensus trees are deposited on the website of the journal as Additional files 1, 2 and 3 and in TreeBase (Study
Accession URL: http://purl.org/phylo/treebase/phylows/
Analysis A
For this analysis, a simple heuristic search was performed
in TNT [39,40] using the tree-bisection-reconnection
swapping algorithm with thousands of random addition
sequence replicates and 10 trees saved per replicate. Wildcard taxa were removed following the search to improve
resolution within the strict consensus tree.
Analysis B
The protocol from ‘Analysis A’ was repeated, but this
time the relationship of the major crown-cryptodire clades
(not only Durocryptodira as in Rabi et al. [36]) were constrained following the current molecular consensus [41]:
(Trionychia (Emydidae (Geoemydidae + Testudinidae)) +
(Chelonioidea (Chelydridae + Kinosternoidea)))). The internal relationships of these clades were left unconstrained and Platysternon megacephalum was
considered a stem-emydid. Heuristic searches were repeated until the most parsimonious trees (MPT) were
found 30 times during each replicate (using the command
“xmult = hits 30”).
Analysis C
The protocol from ‘Analysis B’ was repeated, but nine
new characters that are thought to be relevant for the
interrelationships of Cretaceous basal eucryptodires were
added (see Appendix 2 for character definitions). Heuristic
searches were repeated until the most parsimonious trees
(MPT) were found 30 times during each replicate.
Analysis D
This analysis differs from ‘C’ in that Basilochelys macrobios and most pan-pleurodires except for Podocnemis
expansa and Pelomedusa subrufa were excluded a priori
before running the heuristic search. This experimental
approach is justified by the work of Rabi et al. [27,36] in
which the position of pan-pleurodires proved to be
problematic in that xinjiangchelyids, sinemydids, and
other, widely recognized Mesozoic stem-cryptodires
were unorthodoxly placed outside of Testudines and in
that Cryptodira was not found to be monophyletic relative to Pleurodira. As such, we were interested in testing
how the removal of most pan-pleurodires affects tree topology, especially in the case of Mesozoic basal eucryptodires. The search was again repeated until the most
parsimonious trees (MPT) were found 30 times during
each replicate.
Zhou et al. BMC Evolutionary Biology 2014, 14:77
Systematic Paleontology
TESTUDINES Batsch [43]
PANCRYPTODIRA Joyce, Parham, and Gauthier [44]
Manchurochelys manchoukuoensis Endo and Shikama
[1] (Figures 2 and 3)
Referred specimen
PMOL-AR00180 (Figures 2 and 3), a partial articulated
skeleton, including the skull, the first six cervical vertebrae,
the anterior part of the carapace, two fragmentary scapulae,
and a proximal end of the right humerus.
Locality and Horizons
The fossil is from a site near Qilinshan (Heishangou),
Chifeng City, Inner Mongolia (E118°50′46.4″, N42°08′
33.3″; Figure 1); the Early Cretaceous Jiufotang Formation
[45]. Given the novelty of this site, detailed information is
not yet available regarding its precise age or accompanying
Revised Diagnosis
Manchurochelys manchoukuoensis is diagnosed as a
primitive pancryptodire by the presence of a low domed
shell and a ligamentous connection between the plastron and carapace. It is distinguished from other basal
pancryptodires by the following unique combination of
characters: prefrontals contact one another along the
midline, postorbital-squamosal contact absent, parietal
and squamosal separated, crista supraoccipitalis relatively
long, foramen palatinum posterius large, nuchal emargination shallow, cervical scale present, vertebral scales 2-4
longer than wide, first vertebral wider than nuchal, preneural absent, eight neurals present, peripheral 1 - costal
contact present, costal 3 with parallel anterior and posterior
sides, process or spine on peripheral 7 absent, two suprapygals present of which the posterior one is much larger than
the anterior one, pygal present, central and posterior fontanelles absent, posterior lobe of plastron long and narrow.
The skull is exposed in dorsal and ventral views (Figures 2
and 3). The cranial elements can be readily distinguished
from one another although some cracks are present due
to diagenetic compression. The skull is slightly elongated
and similar in its proportions to the skull of PMOLAR00008. The skull roof is ornamented with a rugose surface and there are no apparent cranial scale sulci.
Dermal roofing elements The nasals are not preserved,
but were likely present by comparison to PMOL-AR00008.
The dorsal plate of the right prefrontal is preserved, but its
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left counterpart is missing completely. The descending
process cannot be observed on either side. Anteriorly, the
right prefrontal is partially hidden by the right maxilla and
the anterior contacts of the prefrontal with the adjacent elements are therefore uncertain. It seems that the prefrontals
contact one another along the midline in PMOL-AR00180.
In the description of PMOL-AR00008, the prefrontals were
interpreted as being separated due to the anterior processes
of the frontals [5]. However, a revision of this specimen
reveals that the component of the frontal process that
was actually exposed in the skull roof is short and did
not separate the prefrontals completely.
Much of the frontal is well exposed except for the anterior process, which is only partially preserved on the
left side. The anterior process is slender and a notch on
its lateral side indicates an insertion for the prefrontal.
Posterior to the notch, the frontal provides a small contribution to the dorsal rim of the orbit that is greater
than that of PMOL-AR00008 [5]. More posteriorly, the
frontal has a slightly curved suture that contacts the
postorbital laterally. The frontal reaches its greatest width
at the straight, posterior suture with the parietal.
The parietals are well exposed in dorsal view, forming
an irregular pentagon in outline. They contact each other
along their entire length, except for their distal ends,
which are separated by the supraoccipital. On the skull
surface the parietal contacts the frontal anteriorly, the
postorbital laterally, and the supraoccipital posteriorly.
Posterolaterally, the parietal contributes to the upper
temporal emargination. As in Sinemys spp. the upper
temporal emargination is well developed and the processus trochlearis oticum is therefore fully exposed in dorsal
view. The deepest portion of the upper temporal emargination coincides with the parietal-postorbital suture. This
condition is similar to that present in Sinemys spp. and M.
manchoukuoensis, but contrast that present in Ordosemys
spp., Kirgizemys hoburensis, and Liaochelys jianchangensis,
where the parietal frames the deepest part of the upper
temporal emargination by a distinct posterolateral process.
The long and narrow processes of the parietals that surround the supraoccipital posteriorly are longer than those
of PMOL-AR00008 ([5]: Figure 3ab), but this might be a
preservational difference. The parietal has an additional
lateral contact with the prootic within the upper temporal
The right jugal is preserved along the posteroventral
corner of the fossa orbitalis. It has a long and slender
anterior process that forms the ventral rim of the orbit
together with the maxilla. Dorsally, the jugal has a curved
sutural contact with the postorbital. Other, potential posterior contacts of the jugal with other elements are uncertain
due to compression.
The presence of the quadratojugals is uncertain due to
compression in the temporal area.
Zhou et al. BMC Evolutionary Biology 2014, 14:77
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Figure 2 New material of Manchurochelys manchoukuoensis (PMOL-AR00180) in dorsal view, from the Early Cretaceous Jiufotang
Formation of Qilinshan, Chifeng, Inner Mongolia, China. Abbreviations: c1, costal Plate 1; cs, cervical scale; ce1-4, cervical vertebrae 1-4; f,
frontal; fst, foramen stapedio-temporale; hy, hyoid; m, maxilla; m1-2, marginal scales 1–2; nu, nuchal; op, opisthotic; p1-2, peripheral Plates 1–2;
pa, parietal; pf, prefrontal; pm, premaxilla; po, postorbital; pro, prootic; ps1, pleural scale 1; q, quadrate; so, supraoccipital; sq, squamosal; v1,
vertebral scale 1.
Figure 3 New material of Manchurochelys manchoukuoensis (PMOL-AR00180) in ventral view, from the Early Cretaceous Jiufotang
Formation of Qilinshan, Chifeng, Inner Mongolia, China. Abbreviations: bo, basioccipital; bs, basisphenoid; cd, central depression of
basisphenoid (maybe taphonomic); ce1-7, cervical vertebrae 1-7; d, dentary; ex, exoccipital; fc, fenestra caroticus; fjp, foramen jugulare posterius;
h, humerus; hy, hyoid; lar, labial ridge of the triturating surface in maxilla; lir, lingual ridge of the triturating surface in maxilla; m, maxilla; nu,
nuchal; op, opisthotic; p1-2, peripheral Plates 1-2; pal, palatine; pt, pterygoid; q, quadrate; s, scapula; sq, squamosal; st, stapes; XII, foramina of
cranial nerve XII.
Zhou et al. BMC Evolutionary Biology 2014, 14:77
The squamosal is positioned at the posterolateral corner
of the skull. A posteromedially directed low crest extends
along the dorsal plate of the squamosal that frames the
lateral aspects of the upper temporal emargination. The
squamosal crest is short relative to the elongated crista
supraoccipitalis and therefore similar to PMOL-AR00008.
The posteriormost tip of the squamosal is pinched and
directed posterolaterally, as in K. hoburensis and PMOLAR00008. Medial to the crest, the squamosal contacts the
quadrate anteriorly and the opisthotic posteromedially.
The left squamosal is exposed in ventral view and reveals
the anteromedial contacts with the quadrate and the
The right postorbital is preserved in articulation,
whereas the left one is slightly offset from its original
position. Anteriorly, the postorbital forms the posterior
rim of the fossa orbitalis and contacts the frontal and parietal medially and the jugal laterally. The postorbital is the
largest element in the temporal region and helps framing
the deep upper temporal emargination together with the
Palatal elements A slender and laminar fragment between the two maxillae is presumed to be the premaxilla.
The maxilla is the largest element of the snout. The
vertical (prefrontal) process contacts the prefrontal dorsally and forms the lateral rim of the apertura narium
externa and the anterior rim of the fossa orbitalis. The
maxilla contacts the jugal posterodorsally. The horizontal
(palatine) plate of the maxilla forms the triturating surface.
The triturating surface consists of a longitudinal depression
bordered by the labial ridge and a single lingual ridge. Both
ridges are comparable in height along their anterior third,
but the lingual ridge is distinctly higher than the labial one
along its posterior third. The medial contact of the maxilla with the palatine is obscured in ventral view by the
The vomer, an unpaired and elongate bone, is slightly
displaced from its original position. Its contact with the
adjacent elements is uncertain. The vomer is dumbbellshaped with bilaterally expanded anterior and posterior
ends and a keeled main body. The expanded ends are
notched, the posterior notch being slightly less developed
than the anterior one. These expansions coincide with
Y-shaped divergences of the ventral, keel-like ridge of
the main body. The posterior notch possibly received
the anterior processes of the pterygoids.
The palatines are partially exposed in ventral view and
slightly displaced from their original positions. The palatine
is a flat plate that encloses the foramen palatinum posterius
together with the maxilla and the pterygoid. The exact
outline of the foramen palatinum posterius is unclear, but
it was apparently large, as in D. bicuspis and Sinemys spp.,
which is different from the moderately sized condition
Page 6 of 16
seen in Ordosemys spp. and Kirgizemys dmitrievi. Posteromedially, the palatine has a broad and rounded edge to
contact the vomer and the pterygoid.
Palatoquadrate elements The quadrate is well exposed
in dorsal and ventral view. It forms the wall of the cavum
tympani. Within the temporal fossa, the quadrate has a
broad sutural contact with the prootic medially and the
squamosal posteriorly. Together with smaller contribution
from the prootic, the quadrate forms a thickening at the
anterior wall of the otic capsule, the processus trochlearis
oticum. The trochlear process is poorly developed and
therefore does not protrude significantly into the lower
temporal fossa. The quadrate portion of the processus trochlearis oticum is sculptured along the prootic-quadrate
suture by several small grooves and ridges, but it is unclear if these ridges had a particular function. In ventral
view, the condylus mandibularis are well preserved on
both sides of the skull except for a slight lateral twisting
caused by compression. The articular surface is a concave
facet. Posterior to the condylus mandibularis, a welldeveloped crest is apparent that runs parallel to the
incisura columella auris. In many derived turtles, this
crest contacts the posteroventral process of the quadrate to
enclose the incisura columella auris. In PMOL-AR00180,
however, such a contact is absent. However, this does
not logically imply that the incisura was completely
open posteriorly, since Sinemys gamera has a comparable
morphology in ventral view but nevertheless exhibits a
closed incisura in lateral view.
The pterygoid is a major element in ventral view. Anteriorly, the pterygoid has a short palatal process that is
subtriangular and pointed rostrally. The pterygoids
contact one another along their anterior thirds. More
posteriorly, the pterygoids are separated from one another
by the basisphenoid. Laterally, the pterygoid forms a horizontal plate with a concave posterior margin and a small,
recurving processus pterygoideus externus. At the posterior
margin of the skull, the pterygoid appears to have a contact
with the basioccipital and exoccipital. The foramen posterius canalis carotici interni is not visible.
Braincase elements The supraoccipital crest is notably
elongated when compared to Ordosemys liaoxiensis or
Liaochelys jianchangensis and reaches beyond the posterior tip of the squamosals, as in PMOL-AR00008. In lateral
view, the crista supraoccipitalis has a slightly convex
dorsal outline and a maximum height of approximately
3 mm. It contacts the parietals anterolaterally and the
opisthotic and exoccipital laterally.
The exoccipitals are well exposed ventrally and are
pierced by a pair of foramina nervi hypoglossi. More
laterally, together with the opisthotic, the exoccipital
encloses a large foramen, the foramen jugulare posterius,
Zhou et al. BMC Evolutionary Biology 2014, 14:77
Page 7 of 16
which is consistent with the condition seen in Sinemys
gamera. The exoccipital has an anterior contact with the
pterygoid. Medially, the exoccipital contacts the basioccipital and contributes to the condylus occipitalis.
The basioccipital forms the floor of the braincase together with the basisphenoid anteriorly and the exoccipitals posterolaterally. Anterolaterally, the basioccipital has a
contact with the pterygoid. More posteriorly, the paired,
horizontally oriented tubera basioccipitale are well developed and separated from one another by a deep midline
depression. The distal portion of the basioccipital forms
the ventral portion of the condylus occipitalis.
The prootic forms the processus trochlearis oticum
together with the quadrate. The foramen stapediotemporale is primarily enclosed by the prootic, but there
is also a small contribution from the quadrate.
The opisthotic contacts the prootic anteriorly, the
quadrate and squamosal laterally, and the supraoccipital
and exoccipital medially. Posteriorly it encloses the foramen
jugulare posterius together with the exoccipital.
The basisphenoid is pointed anteriorly and broadened
posteriorly and therefore has a triangular outline. Anteriorly, it is wedged between the pterygoids. In comparison
to closely related taxa, the basisphenoid appears to be
greatly elongated, but this may be a result of damage to
the pterygoids. Posteriorly, the basisphenoid contacts the
basioccipital along a straight transverse suture and with
the latter forms a smooth and flat braincase floor. The
basisphenoid is sculptured by a round median depression,
which may be a taphonomic artifact. The fenestra caroticus (sensu [36]) opens along the pterygoid-basisphenoid
suture, anteriorly to the basisphenoid pits. Anteriorly, the
fenestra ends in the foramen posterius canalis carotici
cerebralis. The basipterygoid process of the basisphenoid
and the foramen posterius canalis carotici palatinum
are not visible, probably due to the displacement of the
The left columella auris (stapes) is well preserved with
the basis columellae (footplate) and columella. As in
modern turtles, the columella auris has a well-expanded
basis columellae and a rod-like delicate columella. Medially, the basis columellae remains in situ and fits well
into the fenestra ovalis, but this is partially obscured
from ventral view by the hyoid bone. Laterally, the columella is well exposed between the fenestra ovalis and the
quadrate, with a length of approximately 5.5 mm. The
columella is broken at its middle point, and the distal
part is offset slightly. However, its terminal end still remains within the incisura columella auris. The terminal
end of the columella is slightly expanded.
Only the anterior part of the carapace is preserved, including the nuchal plate, first costal plates, first peripherals, left second peripheral, and a fragment of the
left third peripheral (Figure 2). The shell appears to be
low and is slightly sculptured by numerous tiny pits
and grooves.
There is a shallow nuchal emargination, as in PMOLAR00008 and Liaochelys jianchangensis but quite different from Sinemys lens and Dracochelys bicuspis where a
deeper emargination is present. The nuchal is a massive
element with a trapezoidal shape that contacts the first
peripherals laterally and the first costal plates posteriorly.
It is distinctly anteroposteriorly longer than that of
Sinemys brevispinus (the morphology is not entirely clear
in S. lens). The first costal plate shows a broad contact
with the subtriangular first peripheral, as in PMOLAR00008 and Sinemys spp., but unlike Dracochelys
bicuspis where the first peripheral is triangular and
does not contact the costal (Figures 2 and 3).
The sulci of the scales are clearly impressed on the
carapace, including the cervical scale, the first vertebral
scale, the anterior three marginal scales, and the first
pleural scale. The cervical scale is present, as in PMOLAR00008, but absent in Sinemys lens and Dracochelys
bicuspis. It is small and sub-trapezoidal, with a maximum
width of 15 mm and a minimum length of 4 mm. The first
vertebral scale is hexagonal and distinctly wider than long.
It contacts the cervical anteriorly, the first two marginals
anterolaterally, and the first pleural posterolaterally. The
first pleural is partially preserved on the left side. The anterior two marginal scales are identified on the right side,
while the anterior three scales are present on the left side.
The first marginal is much smaller than the second one.
Vertebral column
The mandibles are exposed in ventral view and form a
gentle V-shaped outline. They are occluding with the
The cervical series is well preserved in articulation between the skull and shell, but only the six anterior
skull. The left mandible appears to be nearly straight,
while the right one appears to be convex, but this is
likely a taphonomic artifact. Medially, the rami meet at a
short, fused symphysis.
The hyoids consist at least of a pair of cornu branchiale I, of which the left one is incomplete distally. The
cornu branchiale I is slender, elongated, and curved with a
slightly expanded proximal end. Its length is approximately
22 mm. We now interpret the hyoid element preserved in
PMOL-AR00008 as the cornu branchiale II because of its
greater thickness and its greatly expanded distal end. This
indicates that Manchurochelys manchoukuoensis probably
possessed two pairs of ossified cornu branchiale even
though these two pairs are not preserved in the available
Zhou et al. BMC Evolutionary Biology 2014, 14:77
cervicals can be identified with confidence. The articulation prohibits observing the development and orientation of the articular surfaces of the centra, and it is not
possible to recognize cervical ribs along the cervical series.
However, the centra are formed and the presence of a biconvex centrum can be excluded.
The atlas is displaced from its original position. The
atlas neural arch is positioned against the supraoccipital
and the left exoccipital and is slightly hidden by the latter
anteriorly. The arch is clearly shorter than the axis. As in
most crown cryptodires, the neural arch is a flat lamina. It
is expanded dorsally to bear a broad medial contact with
its counterpart. The neural arch bifurcates posteriorly with
a short lateral spine and a medial process. The lateral
spine is positioned slightly beyond the medial process.
Medially, the spine conjoins the process along a semicircular notch. The medial process is broad for articulating
with the prezygapophysis of the axis.
The axis is well preserved below the crista supraoccipitalis in articulation with the succeeding cervicals. As in
crown turtles, the prezygapophyses of the axis face dorsolaterally, whereas the prezygapophyses of the following
cervicals face dorsomedially. The axis is a large element
with a length of 10 mm and a width of 8 mm, comparable
to the following cervicals. In dorsal view, the axis is
dumbbell-shaped due to the lateral expansion of the
prezygapophyses and postzygapophyses. The prezygapophysis extends more anteriorly than laterally, thereby
forming a dorsolaterally facing articular surface. In contrast, the postzygapophyses are expanded more laterally
than posteriorly, thereby forming the maximum width of
the axis. Between the postzygapophyses, there is a posterior
notch with a gentle curvature. The neural spine is developed with a height of 1 mm, beyond the posterior notch.
In ventral view, a well-developed keel is present along the
entire length of the centrum. The keel is reduced posteriorly and disappears at the posterior margin of the
centrum. The transverse processes are well developed,
forming a maximum width of 10 mm. As in crown cryptodires, the transverse process is positioned along the
anterior half of the centrum. Posteriorly, the centrum is
compressed bilaterally.
The remaining cervicals are similar to each other in
morphology. The third and fourth cervicals are well
exposed in dorsal view. They are similar to the axis in
general morphology except for the dorsomedially-facing
prezygapophyses. The prezygapophyses are divergent laterally and comparable to the postzygapophyses in extent.
The right prezygapophysis of the fourth cervical is flat and
faces dorsally and medially. The anterior notch between
the prezygapophyses is comparable to the posterior one
between the postzygapophyses. This condition is different
from PMOL-AR00008, in which the anterior notch has an
angle of 120 degrees, and the posterior notch is anterior
Page 8 of 16
to the middle point of the neural arch with an angle of 70
degrees [5]. The neural spine is present on the whole
length of the neural arch, different from M. manchoukuoensis, in which the neural spine is limited to the anterior half of the neural arch [5].
In ventral view, the third and fourth cervicals are
comparable in size to the axis, while the fifth and sixth
cervicals appear to be prolonged. The transverse process
is positioned at the anterior portion of the centrum.
Along the cervical series, the transverse process increases
posteriorly in size. The posterior end of the centrum
broadens posteriorly along the cervical series. The ventral
keel is well developed along the whole length of the
centrum. Posteriorly, the keel increases in depth along
the cervical series.
Pectoral girdle
The scapulae are partially preserved on both sides in
ventral view. The scapula is triradiate with a dorsally
directed scapular process, a ventrally directed acromial
process, and a laterally directed glenoid process. The
scapular process is long and slender, but its distal end
is hidden by the cervical series on both sides. The scapular
process gradually expands proximally and forms a gentle
curve with the acromial process. The scapular process is
set at an angle of 87 degree relative to the acromial
process. Most of the acromial process is broken on both
sides. Its remains are slightly longer than the glenoid
process on the right side and confluent proximally to the
glenoid process and scapular process. In contrast, the
glenoid process is stout and bears a laterally facing glenoid
fossa. On the right side, the glenoid fossa is occupied by
the humeral head. The left glenoid fossa is exposed with a
concave facet. However, the precise configuration of the
glenoid fossa is uncertain because the coracoid portion is
The proximal head of the humerus is partially preserved
on the right side in articulation with the glenoid fossa.
The lateral process is identifiable as a ventrally directed
crest. Medially, there is a distinct intertubercular fossa
between the lateral and medial processes. The medial
process is expanded posteriorly and is larger than the
lateral process.
Phylogenetic Analysis
None of the four phylogenetic analyses placed xinjiangchelyids, sinemydids, or other Cretaceous basal eucryptodires
within Testudines, the crown-group of turtles. However,
the relationships of Cretaceous forms vary among three of
the analyses. All four analyses agree in that all Cretaceous
Zhou et al. BMC Evolutionary Biology 2014, 14:77
taxa are consistently placed in a derived position relative to
Analysis A (220 equally parsimonious trees, tree
length = 887): This analysis with no topological constraint
and no new characters resulted in a largely paraphyletic
arrangement of basal eucryptodires with a basally placed
Sinemydidae (sensu [27]) that is only composed of Sinemys
spp., an (Ordosemys leios + Liaochelys jianchangensis) clade
and a successively more derived clade including Judithemys
sukhanovi, Kirgizemys hoburensis and Changmachelys bohlini (the latter group roughly corresponds to the traditional
circumscription of Macrobaenidae). Manchurochelys manchoukuoensis is found in the next less inclusive node to
Sinemydidae. Dracochelys bicuspis occupies the most
derived position among these taxa. The skull of Ordosemys
sp. proved to be a wildcard taxon (Figure 4; Additional
file 3).
Analysis B (136 equally parsimonious trees, tree
length = 909): The constrained analysis obtained poor
resolution for Cretaceous basal eucryptodires, similarly
to the recent results of Rabi et al. [36]. However, a monophyletic Sinemydidae composed only of Sinemys spp. as
well as a Judithemys sukhanovi – Kirgizemys hoburensis Changmachelys bohlini clade was again recovered. Removal
of wildcard taxa, including Ordosemys sp. and Basilochelys
macrobios does not improve resolution (Additional file 3).
Analysis C (151 equally parsimonious trees, tree
length = 925): Inclusion of new characters into the constrained analysis further decreases resolution. However,
after pruning several Cretaceous taxa, a monophyletic
Sinemydidae was obtained including Sinemys spp., Manchurochelys manchoukuoensis, and Dracochelys bicuspis.
Removal of the constraint results in the basal placement
of M. manchoukuoensis within Sinemydidae and in a
(Liaochelys jianchangensis + Ordosemys leios) clade that
in turn forms a polytomy with other Cretaceous basal
eucryptodires (Additional file 3).
Analysis D (143 equally parsimonious trees, tree
length = 819): When most pleurodires and Basilochelys
macrobios are a priori excluded from the analysis a
monophyletic Sinemydidae (sensu [27]) is recovered
containing all Cretaceous forms. Manchurochelys manchoukuoensis is sister to a (Dracochelys bicuspis + Sinemys
spp.) clade and combined they are sister to an (Ordosemys
leios + Liaochelys jianchangensis) clade. Judithemys sukhanovi + Kirgizemys hoburensis are the most basal sinemydids in the context of this analysis. Ordosemys sp. and
Changmachelys bohlini turned to be acting as wildcards
and the inclusion of any of them sinks the J. sukhanovi +
K. hoburensis clade into a polytomy. Another notable
feature of these results that Xinjiangchelys (= Annemys)
levensis is no longer recovered as a xinjiangchelyid but
in the next less inclusive node to them (Figure 5). Exclusion
of new characters does not influence tree topology but
Page 9 of 16
decrease bootstrap support for the Sinemys spp. clade by
47%. Other changes in support are insignificant. A search
without constraints results in a basal polytomy of Cretaceous basal eucryptodires with Manchurochelys manchoukuoensis placed as sister to Sinemys spp. when most other
Cretaceous target taxa are pruned (Additional file 3).
Taxonomic comments
PMOL-AR00180 is assigned to Manchurochelys manchoukuoensis because no major differences are apparent in the
proportions and contacts in the skull and the shell with
those of the holotype [1] or the referred specimen PMOLAR00008 [5]. A striking similarity of PMOL-AR00180
with PMOL-AR00008 is the presence of a long supraoccipital crest that extends markedly more posteriorly than in
Liaochelys jianchangensis, Ordosemys liaoxiensis, Kirgizemys hoburensis, and Sinemys lens (unknown for other species of Sinemys). Although differences appear to be present,
at first sight, between the neck of PMOL-AR00008 and
PMOL-AR00180, particularly in the degree of separation
of the postzygapophyses, these are only because different
sections of the neck are exposed in the two specimens. As
in modern cryptodires, the postzygapophyses of the anterior cervicals in M. manchoukuoensis (as well as in Sinemys
brevispinus, Kirgizemys hoburensis) are more fused than
the posterior ones. In addition, the foramen posterius
canalis carotici cerebralis was illustrated in the pterygoid
in PMOL-AR00008 (labeled as foramen basisphenoidale
[5]) but a revision of the specimen reveals that the position of this foramen is unclear and preservation makes
comparison difficult with PMOL-AR00180 where it is on
the pterygoid-basisphenoid suture.
With the discovery of the new specimen, the number
of described M. manchoukuoensis fossils has increased
to three. Two of these originate from the Yixian Formation of Liaoning Province (including the lost holotype
[1,5]) whereas PMOL-AR00180 was recovered from the
Jiufotang Formation of Inner Mongolia. Both formations
are considered to be Lower Cretaceous, with the Yixian
being Barremian to Upper Aptian (129-122 Ma) and the
younger Jiufotang Formation being Aptian to Upper
Albian (122-110 Ma) in age. Thus, the range of M. manchoukuoensis is extended geographically and, less unequivocally, temporally by the new fossil from Chifeng.
However, given this difference in geography and perhaps
in age it is not excluded that more complete findings may
reveal distinct morphological features not preserved in the
specimen from Chifeng and arguing for a separate species
of Manchurochelys.
Relationships of Cretaceous basal eucryptodire turtles
A broad range of phylogenetic hypotheses of Cretaceous
basal eucryptodires has been proposed over the course
Zhou et al. BMC Evolutionary Biology 2014, 14:77
Page 10 of 16
Figure 4 Simplified strict consensus tree of Cretaceous basal eucryptodires retrieved from Analysis A (with no constraints and no new
characters added) showing a paraphyletic arrangement for the taxa in question. The inferred evolution of selected characters varying among
these taxa is shown on the tree. Ambiguous character states for a given taxon are indicated with ‘?’ in a color that is corresponding to the color of that
character. An alternative topology with Changmachelys bohlini not pruned from the strict consensus is shown in a box at the upper right corner.
Zhou et al. BMC Evolutionary Biology 2014, 14:77
Page 11 of 16
Figure 5 Simplified strict consensus tree of Cretaceous basal eucryptodires retrieved from Analysis D. In this analysis most pan-pleurodires
and Basilochelys macrobios was a priori removed, nine new characters were added and the relationships of cryptodires were constrained according to
molecular phylogenetic results. The inferred evolution of selected characters varying among these taxa is shown on the tree. Ambiguous character
states for a given taxon are indicated with ‘?’ in a color that is corresponding to the color of that character.
Zhou et al. BMC Evolutionary Biology 2014, 14:77
of the last decade. Some studies consider these turtles
to be a predominantly monophyletic clade [18,30,31,33]
whereas others interpret them as being a predominantly
paraphyletic assemblage [4,5,12,17,28,29,32,36]. Two analyses [20,34] obtained a monophyletic Sinemydidae to the
exclusion of Judithemys sukhanovi and Kirgizemys hoburensis. A more crown-ward position for J. sukhanovi and K.
hoburensis has been suggested in other studies as well
[4,5,14,17,29,32,35]. All of these analyses build either
on Gaffney [11] or Joyce [18]. The studies expanding
the matrix of Gaffney [11] are problematic in assuming
monophyly for many higher groups of turtles and for
using a small number of characters only (max. 45), but
they have the advantage of including many Cretaceous
basal eucryptodiran taxa. The matrices expanding the
work of Joyce [18] are improved in using single species
as terminals and a large number of characters, but they
are limited in taxon sampling, at least for the group in
question. Other downsides of all of these analyses are
the dominantly literature-based character scorings and the
lack of specific, phylogenetically relevant characters for
sinemydids, macrobaenids, and closely allied taxa.
We sought progress relative to previous analysis by
significantly expanding the sample of Cretaceous basal
eucryptodires, by utilizing a large, global matrix, by correcting several errors that are apparent in the scorings of
previous matrices, through the addition of new characters
relevant to this group, and by directly studying all relevant
specimens. Therefore, our new analysis is the most comprehensive and the most exhaustive attempt to resolve the
phylogeny of Cretaceous basal eucryptodires to date.
The results of our unconstrained phylogenetic analysis
(Analysis A, Figure 4) agree in its primary aspects with
the “paraphyletic hypothesis” of earlier global studies.
However, the molecular backbone constraint of crowncryptodire clades (Analysis B) collapses most of the nodes
containing Cretaceous basal eucryptodires. Addition of new
morphological characters places Manchurochelys manchoukuoensis and Dracochelys bicuspis within Sinemydidae
together with Sinemys spp. while leaving other taxa
largely unresolved. Interestingly, a priori exclusion of most
panpleurodires and Basilochelys macrobios (Analysis D,
Figure 5), results in the monophyly of all Cretaceous basal
The question remains unanswered whether the monophyletic or the paraphyletic hypothesis of basal eucryptodires
is a better estimate of the phylogeny of sinemydid and
macrobaenid turtles. From a parsimony point of view, the
monophyletic arrangement is better supported since it
requires five (or at least four, as two characters seem to
be correlated) steps less than the paraphyletic topology
as optimized within this part of the consensus trees of
Page 12 of 16
analysis A and D. However, most of these differences in
the number of steps correspond either to the loss of traits,
retention of juvenile characters (i.e. plastral fontanelles),
or the acquisitions of highly variable and homoplastic
characters (i.e. number of neurals). When only the acquisitions of more complex characters are taken into account,
the differences are far less obvious and the monophyletic
hypothesis appears to have less support. In this case, the
monophyletic hypothesis requires a reversal to separated
prefrontals (from medially contacting prefrontals) and the
absence of pterygoid-basioccipital (and exoccipital) contact.
On the other hand, the paraphyletic hypothesis requires
that opisthocoely in the neck evolved twice within this
group (Figures 4 and 5). In summary, until the position of
panpleurodires relative to basal eucryptodires is instable,
the phylogeny of sinemydids and macrobaenids remains
ambiguous as well.
There are some other noteworthy results of the present
contribution. The Mongolian Kirgizemys hoburensis and
the North American Judithemys sukhanovi form a clade in
all of our analyses (in agreement with some previous
works; [17,29,34]) and the Chinese Changmachelys bohlini
is part of the same clade in three of the analyses, though
their exact relationships are unresolved. In addition, Liaochelys jianchangensis is found as the sister taxon of Ordosemys leios in three of the analyses. As for the target taxon
of this work, Manchurochelys manchoukuoensis is placed
within Sinemydidae (sensu [27]) together with Sinemys spp.
and Dracochelys bicuspis in the majority of the analyses
or alternatively, it is more derived than Sinemydidae
and retained some typical characters of this group.
Appendix 1
Changes to the taxon-character matrix of Rabi et al. [36]
Taxa added:
Changmachelys bohlini, Manchurochelys manchoukuoensis,
Liaochelys jianchangensis, Sinemys brevispinus, Sinemys
gamera, Ordosemys sp. skull [12]. Unlike in all previous
analyses, Ordosemys leios is here treated separately
from the Ordosemys sp. skull because they likely
represent different species [12]. Most skull character
scorings were therefore removed from Ordosemys
leios, except for a few that could be deduced with
the help of the skull fragments associated with the
Characters omitted from this study:
Maxilla B, Pterygoid M, Basioccipital B, Cervical
Vertebra D, Cervical vertebra K (see explanation in
Characters modified in this study:
Zhou et al. BMC Evolutionary Biology 2014, 14:77
Pterygoid I. Vertical flange on processus pterygoideus
externus: (0) absent; (1) present all along the process;
(2) reduced.
New definition: Vertical flange of processus pterygoideus
externus: (0) absent, (1) present.
The character of Sterli and de la Fuente [20] pertains
to the vertical flange on the processus pterygoideus
externus. This character is modified and completely
rescored here because the definition of state 2 (reduced)
is not clear and the original scorings of [20] do not help
us to understand it either. For instance, Emys orbicularis
and trionychids are scored as reduced in [20], whereas
Carettochelys insculpta is not. In our opinion Emys
orbicularis has a fully developed vertical flange, whereas
C. insculpta and trionychids all have a reduced, barely
thickened vertical component. Moreover, Proganochelys
quenstedti and Palaeochersis talampayensis are scored 1
(vertical flange present almost all along the lateral
process) but cheloniid sea turtle were scored as not
having a vertical flange despite the clear presence of
such a flange (which is more developed than in P.
quenstedti and Pal. talampayensis). To assure better
reproducibility we modify this character to contain
only two states: vertical flange of processus pterygoideus
externus: (0) absent or (1) present. Under the new
definition P. quenstedti, Kayentachelys aprix and other
basal turtles, including Meiolaniiformes, are scored as
absent (0). And contrary to the previous scoring, we
code Carettochelys insculpta and Anosteira ornata as
present (1) because we see no difference from the
trionychid condition.
Cervical Vertebra I. Sterli and de la Fuente [20]
accidentally used “posteroventrally” not “anteroventrally”
for the direction of the postzygapophyses of the 8th
cervical. Caretta caretta and Chelonia mydas is changed
from 0 to 1 because they clearly show posteroventrally
directing postzygapophyses.
Character rescored in this study:
Pterygoid L. Processus pterygoideus externus: (0) like
in Proganochelys quenstedti; (1) like in testudinoids;
(2) like in Kayentachelys aprix. This character pertains
to the outline of the processus pterygoideus externus.
In state 0 the processus is reduced, in state 1 it is better
developed whereas in state 2 it is posteriorly recurved.
The character is completely rescored because Sterli and
de la Fuente [20] accidentally scored testudinoids with
state 2.
Changes to the character scorings of Rabi et al. [36]
(for justification see the corresponding character in
the taxon-character matrix (Additional file 1).
Prefrontal A: Dracochelys bicuspis: 1—›?
Page 13 of 16
Prefrontal D: Dracochelys bicuspis: 1—›?
Prefrontal E: Dracochelys bicuspis: 1—›?
Parietal A: Dracochelys bicuspis: 1—›?
Parietal G: Dracochelys bicuspis: ?—›1 ; Kirgizemys
hoburensis: ?—›1
Parietal H: Dracochelys bicuspis: 2—›?; Ordosemys
sp. skull: 2—›1
Jugal A: Dracochelys bicuspis: 1—›?; Ordosemys
sp. skull: ?—›1
Quadratojugal A: Sinemys lens: 0—›?
Premaxilla A: Xinjiangchelys wusu, Xinjiangchelys
(= Annemys) levensis, Xinjiangchelys radiplicatoides:
Premaxilla E: Ordosemys sp. skull: ?—›0
Maxilla A: Ordosemys sp. skull: ?—›0
Maxilla B: Kirgizemys hoburensis: 1—›0
Maxilla C: Ordosemys sp. skull: ?—› –
Maxilla D: Ordosemys sp. skull: ?—›0; Kirgizemys
hoburensis: ?—›0
Quadrate D: Sinemys lens: 0—›?
Quadrate F: Sinemys lens: 2—›?
Quadrate H: Sinemys lens: 1—›0
Epipterygoid A: Kirgizemys hoburensis: ?—›1
Pterygoid D: Kirgizemys hoburensis: 1—›0/1
Pterygoid G: Kirgizemys hoburensis: 1—›0
Pterygoid J: Judithemys sukhanovi: ?—›1
Supraoccipital A: Dracochelys bicuspis: 1—›?
Basioccipital A: Kirgizemys hoburensis: 1—›0
Basisphenoid A: Kirgizemys hoburensis: ?—›0
Basisphenoid B: Dracochelys bicuspis: ?—›0
Basisphenoid E: Kirgizemys hoburensis: ?—›0
Hyomandibular Nerve A: Xinjiangchelys radiplicatoides:
Foramen Jugulare Posterius A: Judithemys sukhanovi:
?—›1; Kirgizemys hoburensis: ?—›0
Foramen Nervi Hypoglossi: Xinjiangchelys wusu:
2—›0; Xinjiangchelys radiplicatoides: 2—›0
Fenestra Perilymphatica A: Sinemys lens: 0—›?
Cranial Scutes A: Judithemys sukhanovi: 1—›?
Dentary A: Kirgizemys hoburensis: ?—›0
Carapace D: Judithemys sukhanovi: ?—›0
Nuchal C: Kirgizemys hoburensis: ?—›0
Neural B: Kirgizemys hoburensis: ?—›1
Cervical A: Dracochelys bicuspis: ?—›1
Marginal A: Kirgizemys hoburensis: ?—›0
Entoplastron D: Dracochelys bicuspis: ?—›0
Entoplastron F: Kirgizemys hoburensis: 0—›1
Epiplastron A: Sinemys lens: – —›0
Cervical Rib A: Kirgizemys hoburensis: ?—›0
Cervical Vertebra B: Kirgizemys hoburensis: 0—›1
Cervical Vertebra C: Kirgizemys hoburensis: ?—›1;
Judithemys sukhanovi: ?—›1
Cervical Vertebra G: Sinemys lens: 0—›?
Cervical Vertebra H: Kirgizemys hoburensis: ?—›1
Zhou et al. BMC Evolutionary Biology 2014, 14:77
Cervical Vertebra I: Kirgizemys hoburensis: ?—›1;
Judithemys sukhanovi: 0—›0&1
Caudal B: Kirgizemys hoburensis: ?—›1
Pectoral Girdle A: Kirgizemys hoburensis: ?—›1
Cleithrum A: Kirgizemys hoburensis: ?—›2;
Judithemys sukhanovi: ?—›2
Scapula A: Kirgizemys hoburensis: ?—›2
Humerus C: Kirgizemys hoburensis: ?—›0
Humerus D: Kirgizemys hoburensis: ?—›0
Humerus E: Kirgizemys hoburensis: ?—›1
Illium A: Kirgizemys hoburensis: ?—›1
Pes A: Dracochelys bicuspis: – —›0
Appendix 2
Definitions of new morphological characters:
Posterior Plastral Fontanelle: posterior plastral
fontanelle between the xiphiplastra and/or the hypoplastra:
(0) absent in adult stage; (1): retained in adult stage.
Neural Number: number of neurals (0) less than 9
elements; (1) nine elements.
Plastron Lobe: posterior lobe of plastron (0) relatively
wide and short; (1) posterior lobe of plastron elongated
and narrow coupled with widely spaced plastral buttresses.
Comment: This character is included to capture the
characteristic proportions of the posterior lobe of
Manchurochelys manchoukuoensis, Sinemys lens and
Sinemys brevispinus (unknown for S. gamera). In these
taxa the posterior lobe is not simply just long and
narrow with subparallel lateral sides but the base of the
hyo- and hypoplastral buttresses are also placed wide
apart resulting in an extensive central part of the
plastron. Both these criteria have to be fulfilled in the
derived state.
Shape of Costal 3: costal 3 (0) tapering towards the
lateral side of the shell or with parallel anterior and
posterior borders; (1) costal 3 broadens towards the
lateral side of the shell. Comment: this character is shared
by Dracochelys bicuspis and Liaochelys jianchangensis
(especially marked in the latter).
Costal Rib: (0) distal portion of costal ribs not visible
within the costal; (1) distal portion of costal rib visible
on the surface of the costal.
Comment: In Liaochelys jianchangensis and Dracochelys
bicuspis the rib portion of the costal is visible distally
within the costal element. This is not to be confused
with the presence of free rib heads in taxa with
peripheral fontanelles which is a much more widespread
character. With this character the rib has to be visible
on the surface of the costals.
Carapacial Sutures: (0) carapacial elements finely
sutured or the contact is smooth; (1) carapacial sutures
strongly serrated in adult stage.
Page 14 of 16
Comment: This character is shared by Liaochelys
jianchangensis and Dracochelys bicuspis whereas other
Cretaceous pancryptodires have smooth contacts between
the elements of the carapace.
First Vertebral: (0) vertebral 1 does not enter anterior
margin of carapace; (1) enters anterior margin.
Comment: the derived state is present in Dracochelys
bicuspis (based on [37]), Sinemys spp. (unknown in
Sinemys gamera) and curiously also in the aberrant
pleurodire, Araripemys barretoi Price [46].
Peripheral Gutter: (0) peripheral gutter absent or only
anteriorly developed; (1) peripheral gutter extensively
developed along anterior and bridge peripherals.
Comment: extensive gutter along the anterior twothirds of the peripheral ring is characteristic for a
number of Mesozoic pancryptodires [47,48] but has
never been used in a phylogenetic analysis.
Costal Rib Distal End: (0) distal end of dorsal rib not
visible or only within costo-peripheral fontanelles on
the dorsal face of the carapace; (1) distal end of posterior
dorsal ribs visible and surrounded by the peripheral.
Comment: In sinemydids and a number of other related
taxa the distal end of the posterior dorsal ribs are exposed in dorsal view within the peripherals even though
these forms lack costo-peripheral fontanelles.
Additional files
Additional file 1: Taxon-character matrix in nexus format.
Additional file 2: Taxon-character matrix in tnt format.
Additional file 3: Strict consensus trees.
IVPP: Institute of Vertebrate Paleontology and Paleoanthropology, Beijing,
China; PIN: Paleontological Institute, Russian Academy of Sciences, Moscow,
Russia; PMOL: Paleontological Museum of Liaoning, Shenyang Normal
University, Shenyang, China; TMP: Royal Tyrrell Museum of Palaeontology,
Drumheller, Canada.
Competing interests
The authors declare no competing interests.
Authors’ contributions
CFZ initiated study, described and illustrated specimens. MR and WGJ
collected data and MR performed analyses. MR, CFZ and WGJ wrote the
manuscript. All authors read and approved the final manuscript.
The authors would like to thank the director of Paleontological Institute,
Shenyang Normal University, Prof. Ge Sun for his encouragement. The
following people kindly provided access to fossil specimens under their care:
Vladimir Sukhanov (PIN), Xu Xing, Liu Jun, Corwin Sullivan (IVPP), Donald
Brinkman and James Gardner (TMP). Juliana Sterli (CONICET), Igor Danilov,
Elena Syromyatnikova (ZIN) and Haiyan Tong (IVPP) provided useful
comments and assistance. MR would like to thank the MTA-ELTE Lendület
Dinosaur Research Group grant for support. Insights from three anonymous
reviewers and the editor, Diego Pol, greatly improved the quality of the
manuscript. The Willi Hennig Society is thanked for providing free access to
the program TNT. This project was in part funded by the Public Science and
Technology Research Funds Projects of Land and Resources (No. 201311120),
the National Natural Science Foundation of China (No. 40802007 and No.
Zhou et al. BMC Evolutionary Biology 2014, 14:77
41202014), the Program for Liaoning Excellent Talents in University (No.
LJQ2011120), and Deutsche Forschungsgemeinschaft grant to WGJ (JO 928/
2). We acknowledge support by Deutsche Forschungsgemeinschaft and
Open Access Publishing Fund of Tübingen University.
Author details
Paleontological Institute, Shenyang Normal University, 253 North Huanghe
Street, Shenyang, Liaoning 110034, People’s Republic of China. 2Institut für
Geowissenschaften, University of Tübingen, Hölderlinstraße 12, Tübingen
72074, Germany. 3Department of Paleontology & MTA – ELTE Lendület
Dinosaur Research Group, Eötvös Loránd University, Budapest, Hungary.
Department of Geosciences, University of Fribourg, Fribourg 1700,
Received: 21 January 2014 Accepted: 24 March 2014
Published: 5 April 2014
1. Endo R, Shikama R: Mesozoic reptilian fauna in the Jehol Mountainland,
Manchoukuo. Bull Centr Nat Mus Manchoukuo 1942, 3:1–20.
2. Ji S-A: Reptiles. In Fauna and Stratigraphy of Jurassic-Cretaceous in Beijing
and the Adjacent Areas. Edited by Ren D, Lu L-W, Guo Z-G, Ji S-A. Beijing:
Seismic Press; 1995:140–146.
3. Tong H, Ji S-A, Ji Q: Ordosemys (Testudines: Cryptodira) from the Yixian
Formation of Liaoning Province, northeastern China: new specimens and
systematic revision. Am Mus Novit 2004, 3438:1–20.
4. Zhou C-F: A new eucryptodiran turtle from the Early Cretaceous Jiufotang
Formation of western Liaoning, China. Zootaxa 2010, 2676:45–56.
5. Zhou C-F: A second specimen of Manchurochelys manchoukuoensis
Endo & Shikama, 1942 (Testudines: Eucryptodira) from the Early
Cretaceous Yixian Formation of western Liaoning, China. Zootaxa
2010, 2534:57–66.
6. Sukhanov VB, Narmandakh P: A new Early Cretaceous turtle from the
continental deposits of the Northern Gobi (in Russian). Mesozoic and
Cenozoic Faunas and Biostratigraphy of Mongolia. Trans Joint Sov
Mongolian Paleontol Expedition 1974, 1:192–220.
7. Nessov LA: Data on late Mesozoic turtles from the USSR. Studia
Geologica Salmaticensia. Stud Palaeocheloniol 1984, 1:215–223.
8. Gaffney ES, Ye X-K: Dracochelys, a new cryptodiran turtle from the Early
Cretaceous of China. Am Mus Novit 1992, 3048:1–13.
9. Brinkman DB, Peng J-H: New material of Sinemys (Testudines, Sinemydidae)
from the Early Cretaceous of China. Can J Earth Sci 1993, 30:2139–2152.
10. Brinkman DB, Peng J-H: Ordosemys leios, n. gen., n. sp., a new turtle from
the Early Cretaceous of the Ordos Basin, Inner Mongolia. Can J Earth Sci
1993, 30:2128–2138.
11. Gaffney ES: The postcranial morphology of Meiolania platyceps and a
review of the Meiolaniidae. Bull Am Mus Nat Hist 1996, 229:1–165.
12. Brinkman DB, Wu X-X: The skull of Ordosemys, an Early Cretaceous
turtle from Inner Mongolia, People’s Republic of China, and the
interrelationships of Eucryptodira (Chelonia, Cryptodira). Paludicola
1999, 2:134–147.
13. Sukhanov VB: Mesozoic turtles of Middle and Central Asia. In The Age of
Dinosaurs in Russia and Mongolia. Edited by Benton MJ, Shishkin MA, Unwin
DM, Kurochkin EN. Cambridge: Cambridge University Press; 2000:309–367.
14. Parham JF, Hutchison JH: A new eucryptodiran turtle from the Late
Cretaceous of North America (Dinosaur Provincial Park, Alberta, Canada).
J Vertebr Paleontol 2003, 23:783–798.
15. Danilov IG, Averianov AO, Skutchas PP, Rezvyi AS: Kirgizemys (Testudines,
Macrobaenidae): new material from the Lower Cretaceous of Buryatia
(Russia) and taxonomic revision. Fossil Turtle Res 2006, 1:46–62.
16. Sukhanov VB, Narmandakh P: New taxa of Mesozoic turtles from
Mongolia. Fossil Turtle Res 2006, 1:119–127.
17. Gaffney ES, Rich TH, Vickers-Rich P, Constantine A, Vacca P, Kool L: Chubutemys,
a new eucryptodiran turtle from the Early Cretaceous of Argentina, and the
relationships of the Meiolaniidae. Am Mus Novit 2007, 3599:1–35.
18. Joyce WG: Phylogenetic relationships of Mesozoic turtles. Bull Peabody
Mus Nat Hist 2007, 48:3–102.
19. Rabi M, Joyce WG, Wings O: A review of the Mesozoic turtles of the
Junggar Basin (Xinjiang, Northwest China) and the paleobiogeography
of Jurassic to early cretaceous Asian testudinates. Palaeobio Palaeoenv
2010, 90:259–273.
Page 15 of 16
20. Sterli J, de la Fuente MS: New evidence from the Palaeocene of Patagonia
(Argentina) on the evolution and palaeobiogeography of meiolaniid-like
turtles (Testudinata). J Syst Paleontol 2013, 11:835–852.
21. Ye X: Fossil turtles of China. Palaeontol Sin 1963, 150:1–112.
22. Sukhanov VB: Subclass Testudinata, Testudinates (In Russian). In
Fundamentals of Palaeontology Amphibians, Reptiles and Birds. Edited by
Orlov JA. Moscow: Nauka; 1964:354–438.
23. Nessov LA, Khosatzky LI: Early Cretaceous turtles from southeastern Fergana
(in Russian). In Problems in herpetology: Proc 3rd All-union Herpetological Conf.
Leningrad: Zoological Institute of the Academy of Sciences USSR;
24. Chkhikvadze VM: Fossil turtles of the family Sinemydidae (In Russian).
Izvestiya AN Gruzinskoy SSR. Seriya Biologicheskaya 1977, 3:265–270.
25. Khosatzky LI, Nessov LA: Large turtles of the Late Cretaceous of Middle
Asia (in Russian). Trudy Zoologicheskogo Instituta AN SSSR 1979, 89:98–108.
26. Gaffney ES, Meylan PA: A phylogeny of turtles. In The phylogeny and
classification of the tetrapods, Volume 35A, Amphibians, Reptiles, Birds,
Systematics Association Special Volume. 1st edition. Edited by Benton MJ.
Oxford: Clarendon Press; 1988:157–219.
27. Rabi M, Sukhanov VB, Egorova VN, Danilov I, Joyce WG: Osteology,
relationships, and ecology of Annemys (Testudines, Eucryptodira) from
the Late Jurassic of Shar Teg, Mongolia and phylogenetic definitions for
Xinjiangchelyidae, Sinemydidae, and Macrobaenidae. J Vertebr Paleontol;
2014, 34:327-352.
28. Danilov IG, Parham JF: A redescription of ‘Plesiochelys tatsuensis’ from the
Late Jurassic of China, with comments on the antiquity of the crown
clade Cryptodira. J Vertebr Paleontol 2006, 26:573–580.
29. Danilov IG, Parham JF: A reassessment of some poorly known turtles
from the Middle Jurassic of China, with comments on the antiquity of
extant turtles. J Vertebr Paleontol 2008, 28:306–318.
30. Sterli J: A new, nearly complete stem turtle from the Jurassic of South
America with implications for turtle evolution. Biol Lett 2008,
31. Sterli J: Phylogenetic relationships among extinct and extant turtles: the
position of Pleurodira and the effects of the fossils on rooting
crown-group turtles. Contrib Zool 2010, 79:93–106.
32. Vandermark D, Tarduno JA, Brinkman DB, Cottrell RD, Mason S: New Late
Cretaceous macrobaenid turtle with Asian affinities from the High
Canadian Arctic: dispersal via ice-free polar routes. Geology 2009,
33. Sterli J, de la Fuente MS: A new turtle from the La Colonia Formation
(Campanian – Maastrichtian), Patagonia, Argentina, with remarks on the
evolution of the vertebral column in turtles. Paleontology 2011, 54:63–78.
34. Anquetin J: Reassessment of the phylogenetic interrelationships of basal
turtles (Testudinata). J Syst Palaeontol 2012, 10:3–45.
35. Brinkman DB, Yuan C-X, Ji Q, Li D-Q, You H-L: A new turtle from the
Xiagou Formation (Early Cretaceous) of Changma Basin, Gansu Province,
P. R. China. Palaeobio Palaeoenv 2013, 93:367–382.
36. Rabi M, Zhou C-F, Wings O, Sun G, Joyce WG: A new xinjiangchelyid turtle
from the Middle Jurassic of Xinjiang. China and the evolution of the
basipterygoid process in Mesozoic turtles. BMC Evol Biol 2013, 13:203.
37. Tong H, Brinkman D: A new species of Sinemys (Testudines: Cryptodira:
Sinemydidae) from the Early Cretaceous of Inner Mongolia, China.
Palaeobio Palaeoenv 2013, 93:355–366.
38. Wiman C: Fossile Schildkröten aus China. Paleontol Sin C 1930, 6:1–56.
39. Goloboff PA, Mattoni CI, Quinteros AS: TNT, a free program for
phylogenetic analysis. Cladistics 2008, 24:774–786.
40. Goloboff PA, Farris J, Nixon K: TNT: tree search using new technology, vers. 1.1,
Willy Hennig Society Edition; 2008. Program and documentation available at
41. Krenz JG, Naylor GJP, Shaffer HB, Janzen FJ: Molecular phylogenetics and
evolution of turtles. Mol Phylogenet Evol 2005, 37:178–191.
42. Klein IT: Klassification und kurze Geschichte der vierfüßigen Thiere (translated
by F. D. Behn). Lübeck: Jonas Schmidt; 1760.
43. Batsch AJGC: Versuch einer Anleitung, zur Kenntniß und Geschichte der Thiere
und Mineralien. Jena: Akademische Buchhandlung; 1788:528.
44. Joyce WG, Parham JF, Gauthier JA: Developing a protocol for the
conversion of rank -based taxon names to phylogenetically defined
clade names, as exemplified by turtles. J Paleontol 2004, 78:989–1013.
45. Chang S-C, Zhang H, Renne PR, Fang Y: High-precision 40Ar/39Ar age for
the Jehol Biota. Palaeogeogr Palaeoclimatol Palaeoecol 2009, 280:94–104.
Zhou et al. BMC Evolutionary Biology 2014, 14:77
Page 16 of 16
46. Meylan PA: Skeletal morphology and relationships of the Early
Cretaceous side-necked turtle, Araripemys barretoi (Testudines:
Pelomedusoides: Araripemydidae), from the Santana Formation of Brazil.
J Vertebr Paleontol 1996, 16:20–33.
47. Peng J-H, Brinkman DB: New material of Xinjiangchelys (Reptilia:
Testudines) from the Late Jurassic Qigu Formation (Shishugou Group)
of the Pingfengshan locality, Junggar Basin, Xinjiang. Can J Earth Sci
1993, 30:2013–2026.
48. Danilov IG, Sukhanov VB: A basal eucryptodiran turtle “Sinemys” efremovi
(= Wuguia efremovi) from the Early Cretaceous of China. Acta Paleontol
Pol 2006, 51:105–110.
Cite this article as: Zhou et al.: A new specimen of Manchurochelys
manchoukuoensis from the Early Cretaceous Jehol Biota of Chifeng,
Inner Mongolia, China and the phylogeny of Cretaceous basal
eucryptodiran turtles. BMC Evolutionary Biology 2014 14:77.
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