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Cervical vertebrae of an enigmatic pterosaur from
the Crato Formation (Lower Cretaceous,
Araripe Basin, NE Brazil)
MARIA E. C. LEAL1*, RODRIGO V. PE
ˆGAS2, NIELS BONDE3,4 &
ALEXANDER W. A. KELLNER2
1
Centro de Cie
ˆncias, Departamento de Geologia, Universidade Federal do Ceara
´,
Campus do PICI – BL. 912, CEP. 60455-760, Fortaleza, CE, Brazil
2
Laboratory of Systematics and Taphonomy of Fossil Vertebrates,
Departamento de Geologia e Paleontologia, Universidade Federal do Rio de Janeiro,
Museu Nacional, Quinta da Boa Vista s/n, Sa
˜o Cristo
´va
˜o, CEP. 20940-040,
Rio de Janeiro, RJ, Brazil
3
Biosystematics Section, Zoological Museum (SNM, Copenhagen University),
Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark
4
Fur Museum (Muserum Salling), Nederby 28, DK-7884 Fur, Denmark
*Correspondence: castroleal@gmail.com
Abstract: The Brazilian Crato Formation (Lower Cretaceous, Aptian) is well known for its rich
pterosaur fauna. This paper deals with a new find represented by four articulated mid-cervical ver-
tebrae. The vertebrae show a morphology consistent with that seen in the Chaoyangopteridae, espe-
cially the relative elongation, low neural spines, lack of pneumatic foramina on the lateral face of
the centra and the presence of well-developed postexapophyses. Chaoyangopterids are, so far, rep-
resented with confidence only in Chinese deposits; the only record outside the Jehol Group is the
Crato Formation form Lacusovagus magnificens, a partial skull whose assignment to the Chaoyan-
gopteridae has been disputed. Given this controversy, we review the phylogenetic position of Lacu-
sovagus, and discuss the nesting of our new specimen among theChaoyangopteridae, providing
some comments concerning the composition of the group. We conclude that our new specimen pro-
vides further support for the presence of chaoyangopterids in the Early Cretaceous of Brazil.
Supplementary material: Phylogenetic analysis data are available at: http://doi.org/10.6084/
m9.figshare.c.3873391
The Araripe Basin (Early Cretaceous of Brazil) has
an extremely rich pterosaur fauna, comprising over
30 described species for the Santana Group (e.g.
Kellner et al. 2013), with distinct distributions
between the Crato and Romualdo formations (e.g.
Saya
˜o & Kellner 2006). So far, this diversity is
represented indisputably by only two clades: the
Tapejaridae sensu Kellner & Campos (2007) and
the Pteranodontoidea, represented mostly by the
Anhangueria sensu Rodrigues & Kellner (2013).
Records attributed to other clades are more prob-
lematic. Headden & Campos (2014) have described
a possible dsungaripterid based on a fragmentary
lower jaw from the Romualdo Formation. This spe-
cimen was originally described as a tapejarid by
Veldmeijer et al. (2005), an interpretation followed
recently by Pe
ˆgas et al. (2016). Martill (2011)
assigned a partial rostrum from the Romualdo For-
mation to the Ctenochasmatoidea, although this
has been disputed by Witton (2013). Finally, Lacu-
sovagus magnificens from the Crato Formation
was originally interpreted as the first non-Chinese
chaoyangopterid (Lu
¨et al. 2008; Witton 2008),
which was later challenged (Kellner 2013). Other
chaoyangopterids are, so far, restricted to the Jehol
Group, China (Lu
¨et al. 2008).
Here we describe a new specimen from the
Crato Formation (LP/UFC.CH-721; hereafter cal-
led UFC-721) that was retrieved as a probable Chao-
yangopteridae after a phylogenetic analysis, raising
again the possibility of extending the biogeogra-
phical distribution of this clade outside the Jehol
Group and augmenting the known pterosaur diver-
sity for the Araripe Basin.
From:Hone, D. W. E., Witton,M.P.&Martill, D. M. (eds) New Perspectives on Pterosaur Palaeobiology.
Geological Society, London, Special Publications, 455, https://doi.org/10.1144/SP455.15
#2017 The Author(s). Published by The Geological Society of London. All rights reserved.
For permissions: http://www.geolsoc.org.uk/permissions. Publishing disclaimer: www.geolsoc.org.uk/pub_ethics
Geological setting
The Araripe Basin is an intracratonic basin extend-
ing over an area of approximately 9000 km
2
through
the border of the states of Ceara
´, Pernambuco and
Piauı
´, in NE Brazil. Presently, there is some dis-
cussion regarding the stratigraphic nomenclature
of the deposits comprising the former Santana
Formation (see Martill 2007; Kellner et al. 2013
for details). Here, we follow Neumann & Cabrera
(1999) and Valenc¸a et al. (2003). The Santana
Group sensu Valenc¸a et al. (2003) comprises the
Rio Batateira, Crato, Ipubi, Romualdo and Arajara
formations. The highly fossiliferous Crato and
Romualdo formations (of Aptian and Aptian –
Albian age, respectively) represent two of the most
important Mesozoic fossil Konservat Lagersta
¨tten
on Gondwana (Martill 2007), being well known for
their extensive pterosaur record (e.g. Maisey 1991;
Unwin & Martill 2007).
The Crato Formation is composed of laminated
carbonates interbedded with shales, siltstones and
sandstones packed in an approximately 60 m-thick
heterolithic sequence. This unit is interpreted as a
restricted lacustrine or lagoonal palaeoenvironment,
with both marine and fluvial influences, and with
its marginal and central portions well distinguished
through facies differences. Deposition occurred
under the influence of strong seasonal cycles, as
documented by an alternation of micritic laminated
limestone and calciferous shale laminae, with vari-
able clay content. The shallow waters of this exten-
sive lake were supposed to be stratified: top water
layers brackish and well oxygenated, and bot-
tom layers hypersaline and anoxic (Valenc¸a et al.
2003; Martill & Heimhofer 2007; Heimhofer et al.
2010; Catto et al. 2016).
Materials and methods
The specimen described here is housed in the
Ceara
´Federal University (Universidade Federal do
Ceara
´– UFC) public collection under the accession
number LP/UFC.CH-721 (Fig. 1a). The four verte-
brae are laterally compressed within a slab of lami-
nated limestone from a typical example of the Crato
Formation. According to the collection label, the
specimen was found in a mining quarry in the
municipality of Nova Olinda, having been donated
to the university without any further data. Although,
unfortunately, the exact locality of the specimen is
not known, we are confident about the general
area and stratigraphic unit as the Crato Formation
is mined extensively for limestone slabs used as
paving stones in construction sites all over NE
Brazil, and, as noted by several authors, it is from
these mines where most fossils come (e.g. see Barl-
ing et al. 2015).
Originally, these vertebrae were exposed from
the weathered right side only (Fig. 1a). This side
has been prepared mechanically (Fig. 1b). The lime-
stone slab was then covered by acrylic resin and the
opposite side was prepared in diluted 5–8% acetic
acid (Toombs & Rixon 1959) for approximately
2 weeks, resulting in the almost 3D preserved left
side of the vertebrae being exposed (Fig. 1c). Photo-
graphs were taken before and after acid preparation,
with whitening by magnesium oxide used to high-
light anatomical details (Feldmann 1989).
To perform our phylogenetic analyses, we utili-
zed a modified version of the data matrix by Pe
ˆgas
et al. (2016), derived from the original data matrix
by Kellner (2003), with the inclusion of UFC-721
and the following taxa: Lacusovagus magnificens,
Jidapterus edentus,Pterodaustro guinazui,Cteno-
chasma elegans,Gegepterus changi,Feilongus sp.
and Cycnorhamphus suevicus (see the Supplemen-
tary material). We utilized TNT (Tree analysis
using New Technology) by Goloboff et al. (2003),
under the default New Technology Search (see
the Supplementary material for details), in order to
assess their phylogenetic relationships. Even though
a deeper discussion on the internal phylogenetic
relationships of the Pterosauria as a whole is beyond
the scope of this work, we also included UFC-721
and Lacusovagus magnificens in the data matrix
from the analysis of Andres et al. (2014).
Results
Systematic palaeontology
Pterosauria Kaup 1834
Pterodactyloidea Plieninger 1901
Azhdarchoidea Nessov 1984
?Chaoyangopteridae Lu
¨et al. 2008
Gen. et sp. indet. – LP/UFC.CH-721 (Fig. 1a – d)
Description
The four vertebrae are seen in left lateral view as
exposed from the acid-prepared side (Fig. 1c, d).
The anterior three vertebra are almost equally
long, measuring, respectively, 36, 37 and 36 mm,
while the posterior preserved vertebra is slightly
shorter at 34 mm long (all are measured as the dis-
tance between the ends of the zygapophyses, and
it is estimated that up to 1 mm is missing of the tip
of the anterior left prezygapophysis, which, unfortu-
nately, was lost during acid preparation). The speci-
men is here described mainly based on the left side,
exposed after acid preparation. However, some
important information is also available from the
right side; whenever some feature from the right
side is described, this will be clearly stated in
the text.
M. E. C. LEAL ET AL.
All four vertebrae are slightly crushed, espe-
cially one and three, and the neural arches
are incomplete as seen from the left side (Figs
1c, d, 2a & 3). They seem best preserved on the
two anterior vertebrae, while only a small portion
is visible on the two posterior cervicals. On the ori-
ginally exposed and much worn right side of the
vertebral surfaces (Figs 1a, b & 2b), quite a bit
more can be seen of all the low neural spines of a
somewhat irregular, but low aspect covering almost
the entire centra. These low-shaped neural spines
are not well exposed on the last two vertebrae
on the acid-prepared left side (Fig. 1c, d) but are
clearly seen on the right side after mechanical pre-
paration (Fig. 1b).
With somewhat indistinct dorsal edges of the
neural spines, their original shape is uncertain, but
it appears that the anterior spine at 6 mm is the
highest and it is decreasing posteriorly. The centrum
of the anteriormost vertebra has the posterior end
pointed (the postexapophysis) and clearly visible
(despite being broken), and reaching 6 mm behind
the postzygapophyis, and this is in very nearly
natural contact with the succeeding prezygapo-
physis. The former seems nearly complete, with its
dorsal part reaching a little further back than its ven-
tral part bearing the articular surface. The anterior
end of the first centrum is hidden behind the left
prezygapophysis but, from the right-lateral aspect
seen on the originally exposed and worn surface, it
Fig. 1. Specimen LP/UFC.CH-721. (a) Slab with fossil before preparation, right side. (b) After mechanical
preparation, right side. (c) After acid preparation, left side. (d) After acid preparation, whitened with magnesium
oxide, left side. Scale bars equal 10 mm.
ENIGMATIC PTEROSAUR FROM THE CRATO FORMATION
appears that the centrum only extends a little, per-
haps 3– 4 mm, in front of the anterior end of the
neural spine that is exposed beyond the broken
prezygapophysis.
The height of the vertebra as preserved
(c. 13 mm) is probably slightly exaggerated, as the
centrum is crushed and probably squeezed a little
towards the ventral side, so that the relative height
to length ratio can only be estimated as approxi-
mately 0.35. There is no obvious sign of a pneuma-
tic foramen, although this is difficult to ascertain due
to the crushing of the centrum. However both the
latter and the broken anterior end of the prezyga-
pophysis are clearly hollow, as evidenced by the
exposed interior space.
The second vertebra is the one best exposing the
centrum on the left side, which is largely uncrushed.
Its left-lateral zygapophyseal ridge is nearly per-
fectly preserved, almost horizontal (dipping a little
in front) and narrowing in the middle. There is
only a small crack in the ventral part of the prezyga-
pophysis, which has an articular head, pointed in
front and with a slightly convex articular head fac-
ing upwards (fitting into the concave and postero-
ventrally facing articular surface of the postzyga-
pophysis in front). The postzygapophysis has a
smoothly rounded dorsal point projecting over a
similarly facing concave articular surface still in
contact with the posterior part of the convex surface
of the next prezygapophysis.
The second centrum is better preserved than the
one in front, and has only the posterior half crushed
a little. Its left-lateral postexapophysis is also better
visible and quite pointed, protruding for 9 mm pos-
terior to the postzygapophysis. The lateral face of
the centrum is about equally high as the middle
part of the zygapophyseal ridge, and between the
two there is a smooth sulcus in the whole length,
but fading a little in the middle. The anterior lateral
area of the centrum ventral to the zygapophyseal
ridge, where pneumatic foramina can typically
be seen in other pterodactyloids (e.g. Kellner &
Tomida 2000; Vila Nova et al. 2015), is well pre-
served in this vertebra and clearly lacks pneumatic
Fig. 2. Specimen LP/UFC.CH-721. (a) Drawing with abbreviations, left side. (b) Drawing with abbreviations, right
side. (c) Reconstruction in a left-lateral view. Abbreviations: c, condyle; ns, neural spine; poex, postexapophysis;
poz, postzygapophysis; prz, prezygapophysis. Scale bars equal 10 mm.
M. E. C. LEAL ET AL.
foramina. The neural spine is low, long and thin and
not well preserved. It seems lower in the anterior
end, but this could be an artefact of the matrix
covering, as can be seen on the right side where
the anterior part seems about as high as the rest.
The third vertebra is severely crushed especially
in the middle part and with poor preservation of
the low neural spine (Figs 2c, d & 4). The convex-
upwards facing prezygapophysis has small holes
in the antero-ventral surface showing its hollow
interior. The entire centrum is crushed and frag-
mented, and the crushed zygapophysial ridge is
hollow, while the postzygapophyseal process is
well preserved, and shows its concave articular sur-
face and the dorsal point above it (Figs 2d & 4).
Below this, the incomplete postexapophysis bends
markedly downwards.
The convex prezygapophysis of the last and
slightly shorter vertebra has slid out and downwards
from its articulation with the mentioned postzyga-
pophysis, as seen on the left side (Figs 1c, d & 3),
while the articular contact seems better preserved
on the right side (Fig. 1b). The centrum ends in a
strong postexapophysis reaching well behind the
postzygapophysis, which curves laterally (Figs
2a, c & 3), and of which the articular surface cannot
be seen directly from the left, and the process is
broken on the right side. The lateral sulcus is dis-
appearing in the middle. The neural spine is low
and long, being still partly covered by matrix on
the left and acid-prepared side (Fig. 1c, d). The pos-
terior condyle is exposed below and behind the
postzygapophysis. The height of this vertebra is
approximately 20 mm, being around 0.6 times its
length, markedly higher than the other vertebrae.
All four vertebrae have concave ventral pro-
files, so that all are narrower in the middle than at
each end as seen from the lateral face. The sulcus
between the centrum and the zygapophyseal ridge
is best seen on the second vertebra, but can also be
traced on the third and the first despite their crush-
ing, while it is less prominent on the last vertebra.
Phylogenetic analyses results
The phylogenetic analysis produced a strict consen-
sus tree of four most parsimonious trees (length ¼
252 steps, consistency index (CI) ¼0.643, retention
index (RI) ¼0.828). UFC-721 was recovered as a
member of the clade that unites chaoyangopterids
and azhdarchids, in a polytomy involving the Azh-
darchidae (Azhdarcho lancicollis +Quetzalcoatlus
sp. +Zhejiangopterus linhaiensis), Lacusovagus
magnificens,Jidapterus edentus,Shenzhoupterus
chaoyangensis and Chaoyangopterus zhangi
(Fig. 4). When UFC-721 and Lacusovagus mag-
nificens are excluded from the analysis, Jidap-
terus edentus,Shenzhoupterus chaoyangensis and
Chaoyangopterus zhangi form a chaoyangopterid
clade in a sister-group relationship with the Azh-
darchidae. Chaoyangopterids share, as ambiguous
synapomorphies, a concave dorsal margin of the
skull (also seen in some archaeopterodactyloids
and in Pteranodon), elongate mid-cervical vertebrae
Fig. 3. Specimen LP/UFC.CH-721. Left side in an oblique ventro-lateral view. Scale bar equals 10 mm.
ENIGMATIC PTEROSAUR FROM THE CRATO FORMATION
with low neural spines (also seen in archaeoptero-
dactyloids) and a nasoantorbital fenestra accoun-
ting for over 40% of total skull length (also
present in the Tapejaridae and Istiodactylidae),
and, as an unambiguous synapomorphy, a nasoan-
torbital fenestra extending above the orbit (condi-
tion unknown in Chaoyangopterus zhangi). They
share with the Azhdarchidae, as an ambiguous
synapomorphy, the secondary loss of the pneumatic
foramina that pierce the lateral face of the mid-
cervical vertebrae centra. UFC-721 shares with the
Chaoyangopteridae, elongate mid-cervical verte-
brae with low neural spines lacking lateral pneu-
matic foramina on the centra, while Lacusovagus
exhibits a nasoantorbital fenestra accounting for
over 40% of total skull length.
We have also added the new specimen and Lacu-
sovagus to the data matrix of Andres et al. (2014),
although a discussion about conflicting pterosaur
phylogenetic hypotheses is beyond the scope of
the present contribution. The results regarding
the position of UFC-721 and Lacusovagus did not
Fig. 4. Strict consensus tree (of four most parsimonious trees) recovered from the phylogenetic analysis (length ¼
252 steps, CI ¼0.643, RI ¼0.828). Nodes: A, Pterosauria; B, Pterodactyloidea; C, Archaeopterodactyloidea;
D, Azhdarchoidea. Chaoyangopterids, UFC-721 and Lacusovagus magnificens are shown in a red box. Numbers
indicate Bremer support values.
M. E. C. LEAL ET AL.
change: they fell in a polytomy with Chinese
chaoyangopterids and the Azhdarchidae, in a strict
consensus tree of six most parsimonious trees
(CI ¼0.358, RI ¼0.794).
Discussion
Position of UFC-721 cervical vertebrae
within the cervical column
As general for azhdarchoids, mid-cervicals are dis-
tinctively more elongate than cervicals I – II and
VIII–IX (e.g. Cai & Wei 1994; Zhou 2010; Vila
Nova et al. 2015). Furthermore, cervicals VIII and
IX exhibit a dorsalized morphology in many ptero-
dactyloids (e.g. Kellner & Tomida 2000; Bennett
2001), including azhdarchoids (e.g. Cai & Wei
1994; Aires et al. 2014; Vila Nova et al. 2015). It
is thus most likely that the four preserved verte-
brae represent four of the mid-cervicals III – VII.
For tapejarids, the cervical length formula can
be generalized as I +II ,III ,IV ¼V.VI .
VII .VIII .IX (Vila Nova et al. 2015), whereas
for azhdarchids it can be regarded as I +II ,III ,
IV ,V.VI .VII .VIII .IX (Cai & Wei
1994; Steel et al. 1997; Averianov 2010, 2013).
In tapejarids, concerning the comparative
lengths within the cervical series, cervicals IV – VI
are very similar in length and are somewhat longer
than cervical VII (achieving 1.33–1.50 times the
length of VII) but they contrast sharply with the
dorsalized cervicals VIII– IX (over two times
the length of cervical VII: Vila Nova et al. 2015).
In Azhdarcho lancicollis, on the other hand, cervi-
cals IV– VI are much longer than cervicals VII –
VIII (each of them achieving 1.55 – 2.90 times the
individual lengths of VII–VIII), which in turn are
also similar to each other and longer than the dorsal-
ized cervical IX (achieving over 2.85 times the
length of IX, while cervical V achieves over 8
times that of IX: Averianov 2010, 2013).
The pattern for chaoyangopterids remains un-
clear. The cervical series of Shenzhoupterus
has not been described in detail (Lu
¨et al. 2008).
AChaoyangopterus specimen figured by Zhou
(2010) was reported to exhibit an axis and five
other elongate cervical vertebrae. Its purported
first dorsal vertebra was described as ‘cervicalized’
and lacks a preserved rib, while the following ver-
tebra exhibits a rib that bends slightly forward
unlike the following dorsal vertebrae, but shaped
much like in the cervical IX of tapejarids (Vila
Nova et al. 2015). We therefore propose that the
first two purported dorsal vertebrae of the Chao-
yangopterus specimen figured by Zhou (2010)
represent, in fact, the last two cervicals VIII – IX
(Fig. 5). In this case, similar to tapejarids, cervicals
IV–VI would be rather similar in length (with V
being the longest), but longer than cervical VII
(1.25–1.30 times its length) and much longer than
cervicals VIII– IX (c. 2.5 – 3 times of their lengths).
Because (1) the second preserved vertebra of
UFC-721 is the longest of all, (2) is nonetheless
very similar to the first and the third, and (3) these
three are only slightly longer than the fourth
preserved vertebrae, we tentatively interpret the cer-
vical series described herein as representing cervi-
cals IV–VII.
The phylogenetic position of UFC-721
The Chaoyangopteridae were formally named by Lu
¨
et al. (2008) to assemble Shenzhoupterus,Chaoyan-
gopterus,Jidapterus,Eoazhdarcho and Eopterano-
don, all from the Jehol Group, Lower Cretaceous
of China. Their monophyly has been corroborated
(Andres & Ji 2008; Witton 2008, 2013; Pinheiro
et al. 2011; Vullo et al. 2012; Wang et al. 2012;
Andres & Myers 2013; Headden & Campos 2014).
In total, six species have been referred to the
clade: Chaoyangopterus zhangi (Wang & Zhou
2003a), Shenzhoupterus chaoyangensis (Lu
¨et al.
2008), Jidapterus edentus (Dong et al. 2003) and
Eoazhdarcho liaoxiensis (Lu
¨& Ji 2005), all from
the Aptian Jiufotang Formation; Eopteranodon lii
(Lu
¨& Zhang 2005) from the Barremian Yixian
Formation; and the only non-Chinese pterosaur
material assigned to the Chaoyangopteridae, namely
the geographically isolated Lacusovagus magni-
ficens (Witton 2008) from the Brazilian Crato For-
mation. The group has a controversial taxonomic
and systematic history, with Chaoyangopterus
zhangi having been originally regarded as a nycto-
saurid (Wang & Zhou 2003a) and later as an
azhdarchid (Frey et al. 2006); Jidapterus edentus
originally interpreted as an indeterminate pterodac-
tyloid (Dong et al. 2003); Eopteranodon as a ptera-
nodontid (Lu
¨& Zhang 2005); and Eoazhdarcho
as an azhdarchid (Lu
¨& Ji 2005). Subsequent to
the erection of the family Chaoyangopteridae and
referral of all the aforementioned species to the
group (Lu
¨et al. 2008), Eopteranodon has been
reassigned to the Tapejarinae (Andres & Ji 2008;
Vullo et al. 2012; Wang et al. 2012; Andres &
Myers 2013); and Lacusovagus magnificens was
proposed to be a possible thalassodromine tapejarid
(Kellner 2013; Aires et al. 2014). The Chaoyan-
gopteridae were thus, so far, confirmed with cer-
tainty exclusively for the Jiufotang Formation of
the Jehol Group.
The present phylogenetic analyses indicate
that both Lacusovagus magnificens and UFC-721
fall within the clade that unites azhdarchids and
chaoyangopterids, with ambiguous affinities. None-
theless, further discussion on their features might
ENIGMATIC PTEROSAUR FROM THE CRATO FORMATION
shed some light concerning their most probable
relationships.
One of the most interesting features exhibited by
UFC-721 is the lack of pneumatic foramina piercing
the lateral faces of the centra of the mid-cervical
vertebrae. Such foramina are found in a wide range
of pterosaurs, including rhamphorhynchids (e.g.
Bonde & Christiansen 2003), some archaeoptero-
dactyloids (e.g. Wang et al. 2007; Andres & Ji
2008), pteranodontoids (e.g. Kellner & Tomida
2000), dsungaripterids (e.g. Andres & Ji 2008) and
tapejarids (e.g. Vila Nova et al. 2015 contra Eck
et al. 2011). The well-preserved cervical vertebrae
of the Romualdo Formation tapejarids demonstrate
the existence of one, two or three lateral pneuma-
tic foramina on the centrum of the mid-cervicals
of these forms (Vila Nova et al. 2015 – three may
be primitive as seen in Rhamphorhynchus: Bonde
& Christiansen 2003), while the pattern of the Chi-
nese tapejarids is still uncertain due to their crushed
nature (e.g. Wang & Zhou 2003b; Liu et al. 2014;
Vila Nova et al. 2015). At least one pneumatic
Fig. 5. Comparison of the cervical series in different azhdarchoid groups, in a left-lateral view. (a) AMNH 22568
(Tapejaridae: Thalassodrominae), mirrored after Vila Nova et al. (2015). (b)Azhdarcho lancicollis (Azhdarchidae),
after Averianov (2013). (c)Chaoyangopterus zhangi (Chaoyangopteridae), after Zhou (2010). (d) UFC-721
(?Chaoyangopteridae). Roman numerals indicate vertebrae numbers. All scale bars equal 50 mm.
M. E. C. LEAL ET AL.
foramen has been found to pierce the lateral surface
of the centrum of a mid-cervical vertebra in the
Chinese tapejarine Sinopterus dongii (Vila Nova
et al. 2015). Eopteranodon and Eoazhdarcho were
reported to also lack these lateral foramina (Zhou
2010), but these taxa do not exhibit laterally pre-
served cervical vertebrae (Lu
¨& Ji 2005; Lu
¨&
Zhang 2005; Lu
¨et al. 2006a) and therefore the pres-
ence of such foramina cannot be verified.
The secondary loss of these lateral pneumatic
foramina represents a synapomorphy of both the
clades Chaoyangopteridae +Azhdarchidae (Vullo
et al. 2012; Wang et al. 2012) and Archaeoptero-
dactyloidea (e.g. Kellner 2003; Andres & Myers
2013). However, the cervical vertebrae of azhdarch-
ids or chaoyangopterids can be distinguished from
those of archaeopterodactyloids due to the presence
of postexapophyses – a synapomorphy of the
Dsungaripteroidea sensu Kellner, 2003 (e.g. Kellner
2003; Wang et al. 2012; Andres & Myers 2013).
Postexapophyses are found in all dsungaripteroids,
including azhdarchids (e.g. Averianov 2010) and
chaoyangopterids (e.g. Lu
¨et al. 2008; Zhou 2010).
Even those archaeopterodactyloids lacking lateral
pneumatic foramina on the lateral surface of the
mid-cervicals do not exhibit postexapophyses,
such as Pterodactylus antiquus,Pterodaustro
guinazui,Ctenochasma elegans and Feilongus sp.
(e.g. Kellner 2003; Wang et al. 2014). As a nota-
ble exception, the unusual archaeopterodactyloid
Gegepterus changi (Yixian Formation, Early Creta-
ceous of China) is the only non-dsungaripteroid
exhibiting postexapophyses (Wang et al. 2007).
However, the mid-cervical vertebrae of this form
can be distinguished from those of chaoyangop-
terids and azhdarchids due to the presence of pneu-
matic foramina on the lateral surface of the centrum
(Wang et al. 2007).
The lack of such lateral pneumatic foramina in
cervical vertebrae does not imply the lack of pneu-
matization of the cervical vertebrae. Indeed, azh-
darchids such as Azhdarcho lancicollis exhibit
anterior and posterior pneumatic foramina piercing
the centrum of the mid-cervical vertebrae, lateral
to the neural canal (Averianov 2010). These foram-
ina are still unknown for the Chaoyangopteridae
and are not observable on UFC-721. Nonetheless,
UFC-721 seems to be pneumatized as indicated by
slight damage, as well as crushing, that show the
hollow interior of the vertebrae (Figs 2 – 4).
The mid-cervical vertebrae of azhdarchids
are characterized by only very weakly developed
neural spines (e.g. Averianov 2010), in contrast
to UFC-721 and chaoyangopterids (e.g. Zhou
2010). Concerning mid-cervical vertebrae length,
UFC-721 does not exhibit the extreme anteroposte-
rior elongation characteristic of azhdarchids (e.g.
Howse 1986; Cai & Wei 1994; Kellner & Langston
1996; Averianov 2010), including the robust necked
azhdarchid from Romania (Vremir et al. 2015). It
is, however, longer than the cervical vertebrae of
tapejarids (e.g. Vila Nova et al. 2015) and similar
to chaoyangopterids (e.g. Zhou 2010) (see Table 1).
Indeed, we find the cervical vertebrae of UFC-
722 to fall within the interval that corresponds to
known chaoyangopterid cervical vertebrae length/
height ratios, distinct from other azhdarchoids
(Table 1). Although some archaeopterodactyloids
also display elongate mid-cervical vertebrae with
low neural spines, these lack postexapophyses (e.g.
Kellner 2003), with the exception of Gegepterus
changi (Wang et al. 2007), as discussed above.
The cervical vertebrae of the tapejarine Sinopterus
dongii have also been described as elongate (Wang
& Zhou 2003b), although their condition do
not match that seen for the Chaoyangopteridae
(Table 1). The specimen M 4895 (cast MN
4737-V) from the Romualdo Formation, originally
attributed to the pteranodontoid ‘Santanadactylus’
spixi by Buisonje
´(1980) and later reinterpreted as
a Tapejaridae indet. by Kellner (1995, 2004), also
exhibits elongated mid-cervical vertebrae with low
neural spines, although this form displays pneu-
matic foramina piercing the centrum. While tapejar-
ids are known to achieve a maximum length/height
ratio of the mid-cervical vertebrae of approxima-
tely 2, chaoyangopterids surpass 2.5 and even 3,
while azhdarchids surpass 4 (Table 1). UFC-721
exhibits other similarities to the cervical vertebrae
of Chaoyangopterus zanghi, namely long prezy-
gapophyses, well-pronounced postexapophyses and
large postzygapophyses (Zhou 2010; Vila Nova
et al. 2015).
Morphological comparisons thus indicate a pro-
bable close relationship between UFC-721 and the
Chaoyangopteridae, given the combination of the
following features: elongated mid-cervical verte-
brae, low neural spines, and pneumatic foramina
piercing the centrum laterally absent and post-
exapophyses present. The phylogenetic analyses
indicate it to most likely nest within this clade
indeed, although the possibility exists of it nesting
elsewhere within the clade that unites chaoyan-
gopterids and azhdarchids remains, or else as the
sister-group to such clade. We therefore classify it
as ?Chaoyangopteridae indet.
Phylogenetic position of Lacusovagus
magnificens
Lacusovagus magnificens, known from a single
incomplete skull, was described as the first chaoyan-
gopterid from the Crato Formation and the first from
outside of China (Witton 2008). Its large nasoan-
torbital fenestra, together with its edentulous jaws,
ENIGMATIC PTEROSAUR FROM THE CRATO FORMATION
suggests affinities to the Azhdarchoidea rather than
with the also toothless Pteranodontidae or Nycto-
sauridae (Witton 2008). The long and straight
rostrum most certainly demonstrates it to be a non-
tapejarine azhdarchoid, while the absence of a pre-
maxillary crest was interpreted as evidence of a
non-thalassodromine nature too (Witton 2008). It
was also argued not to represent either an azh-
darchid, and to share, with chaoyangopterids, a
slender posterodorsal margin of the nasoantorbi-
tal fenestra and a low skull profile (Witton 2008).
Unfortunately, the specimen is severely crushed
dorsoventrally and only a tentative reconstruction
of its posterodorsal margin of the nasoantorbital
fenestra and skull profile was possible (Witton
2008). The original height and thickness of this cra-
nial region in Lacusovagus thus cannot be assessed
with confidence.
Lacusovagus was also considered a non-azhdar-
chid azhdarchoid due to its relatively short rostrum.
Indeed, azhdarchids in general exhibit long rostra
(e.g. Cai & Wei 1994; Kellner & Langston 1996;
Ibrahim et al. 2010). Still, it should be noticed
that a possible unusually short-snouted azhdar-
chid is known. Dubbed the ‘Javelina azhdarchid’
(Witton 2013), TMM 42489-2 exhibits a relatively
short snout, comparable to that of thalassodromines
(Table 2), and this is partially why it has, in the past,
Table 1. Comparison of length/height ratio of selected azhdarchoid and archaeopterodactyloid taxa
Clade Taxon or
specimen
Length/height
range of
preserved
mid-cervicals
References
Thalassodrominae AMNH 22568 0.9–1.88 Vila Nova et al. (2015)
Thalassodrominae MN 4728-V 1.00–1.90 Vila Nova et al. (2015)
Tapejarinae PMOL-AP00030 1.5 Liu et al. (2014)
Tapejarinae AMNH 24445 2.00–2.06 Vila Nova et al. (2015)
Tapejarinae Sinopterus dongii 1.36–2.18 Wang & Zhou (2003b)
Tapejarinae ‘Huaxiapterus’corollatus 1.47– 1.92 Lu
¨et al. (2006b)
Chaoyangopteridae Chaoyangopterus zhangi 2.05–3.29 Wang & Zhou (2003a)
Chaoyangopteridae Shenzhoupterus chaoyangensis 2.5– 3.33 Lu
¨et al. (2008)
Chaoyangopteridae Jidapterus edentus 1.9–2.69 Dong et al. (2003)
?Chaoyangopteridae UFC-721 2.1–2.86 This work
Azhdarchidae MB.R. 2832 4.73 Costa et al. (2015)
Azhdarchidae Zhejiangopterus linhaiensis 4.0–4.75 Cai & Wei (1994)
Azhdarchidae Azhdarcho lancicollis 3.6–4.12 Averianov (2010)
Azhdarchidae Phosphatodraco mauritanicus c. 4 Pereda Suberbiola et al. (2003)
Azhdarchidae Eurazhdarcho langendorfensis c. 6 Vremir et al. (2013)
Azhdarchidae R.2395 4.9 Vremir et al. (2015)
Archaeopterodactyloidea Pterodactylus antiquus 2.96 Howse (1986)
Archaeopterodactyloidea Huanhepterus quingyangensis 1.76–6.1 Dong (1982)
Archaeopterodactyloidea Pterodaustro guinazui 3.6– 4.37 Witton (2013)
Archaeopterodactyloidea Ctenochasma elegans 3.2 – 3.8 Witton (2013)
Archaeopterodactyloidea Gegepterus changi 4.8 Wang et al. (2007)
Archaeopterodactyloidea Feilongus sp. 3.18–6.9 Wang et al. (2014)
Table 2. Comparison of the rostral values (after Kellner 2010) of selected azhdarchoid taxa
Clade Taxon or specimen Rostral value References
Tapejarinae Tapejara wellnhoferi 3.2 Wellnhofer & Kellner (1991)
Thalassodrominae Tupuxuara leonardii 7.9 Kellner (2004)
Azhdarchoidea indet. Lacusovagus magnificens (?)–c. 12 Witton (2008)
Chaoyangopteridae Chayoangopterus zhangi 10.54 Wang & Zhou (2003a)
Chaoyangopteridae Shenzhoupterus dongii 7.24 Lu
¨et al. (2008)
Chaoyangopteridae Jidapterus edentus 11.34 Dong et al. (2003)
?Azhdarchidae TMM 42489-2 7.06 Kellner (2004)
Azhdarchidae Quetzalcoatlus sp. c. 18.5 Kellner & Langston (1996)
Azhdarchidae Zhejiangopterus linhaiensis 13.3 Cai & Wei (1994)
M. E. C. LEAL ET AL.
been considered to be a thalassodromine (Kellner
2004; Martill & Naish 2006). However, the cervical
vertebrae of TMM 42489-2 have been reported
to display the unique and unusual features of azh-
darchids while still pending detailed description
(Andres & Myers 2013). If this specimen really rep-
resents an azhdarchid, it is therefore possible that it
is a basal azhdarchid or, perhaps, even a secondarily
short-snouted azhdarchid, raising the possibility that
the same could apply to Lacusovagus. We also
notice that the rostral value (calculated as the rostral
length divided by the height of the anteriormost
point of the margin of the nasoantorbital fenestra,
after Kellner 2010) of Lacusovagus magnificens,
after the reconstruction of its skull by Witton (2008),
would actually be very close to that of the azh-
darchid Zhejiangopterus linhaiensis (Cai & Wei
1994) (Table 2). Once again, this cannot be verified
due to the material’s incompleteness. No cervical
vertebrae or any other postcranial materials are
known for Lacusovagus.
We therefore suggest that, while the known mor-
phology of Lacusovagus is sufficient to set it apart
from the Tapejaridae, only more complete material
could determine with more certainty if it, indeed,
falls within chaoyangopterids or, alternatively, clo-
ser to azhdarchids. We therefore recommend that
it should be regarded as a ?Chaoyangopteridae, as
well as UFC-721. Even though it is noticeable that
the holotype of Lacusovagus magnificens presents
less diagnostic features than UFC-721 concerning
its probable chaoyangopterid nature, it remains
possible that both specimens represent the same
species.
We therefore restrict the Chaoyangopteridae to
the Chinese forms and consider UFC-721 and
Lacusovagus magnificens as the only other known
possible members of the group.
Conclusions
The morphology of UFC-721 matches the Chaoyan-
gopteridae. The presence of postexapophyses, com-
bined with the lack of pneumatic foramina piercing
the lateral surface of the centra, indicate that it falls
within the clade that unites chaoyangopterids and
azhdarchids, as corroborated by the phylogenetic
analysis results. The elongate aspect, as well as
the low neural spine and the well-pronounced post-
exapophyses, also match the morphology seen in
chaoyangopterids (e.g. Zhou 2010; Vila Nova
et al. 2015). The lack of extreme elongation of the
mid-cervicals, a synapomorphy of the Azhdarchi-
dae, indicates it to fall outside of this clade.
Although the exact relationship between these
two clades and UFC-721 could only be ascertained
with more complete material, our results indicate
that the specimen represents a chaoyangopterid.
The holotype specimen of Lacusovagus magnif-
icens is here also considered as a possible chaoyan-
gopterid. Thus, the possibility that both specimens
represent the same species also remains open.
We therefore restrict the Chaoyangopteridae to
the Chinese forms. We highlight the plausibility of
the existence of the Chaoyangopteridae in Brazil,
first proposed by Witton (2008) and now reinforced
and more supported by the discovery of UFC-721.
We would like to thank the organizing committee of the
Flugsaurier 2015 meeting in Portsmouth for putting this
volume together and inviting us to contribute. We thank
Francisco Figueiredo (UERJ) for technical assistance in
photography. MECL and NB thank Eberhard (Dino)
Frey, Christiane Birnbaum and Wolfgang Munk (SMNK)
for access to the holotype of Lacusovagus magnificens.
We thank the Willi Hennig Society for making TNT
freely available. MECL thanks CNPq/FUNCAP for her
DCR grant (CNPq/FUNCAP-DCR/305426/2014-1 and
DCR-0024-01186.01.00/14). NB thanks the Zoological
Museum (SNM) for the facilities and room put at his
disposal during this work, and the Fur Museum for financ-
ing part of his tour to European collections. RVP thanks
FAPERJ (grant 213265) and CNPq (#131186/2017-5) for
funding. AWAK thanks CNPq (grant 304780/2013-8) and
FAPERJ (grant E-26/102.737/2012) for funding. The
authors thank Ma
´rcio Mendes (Colec¸a
˜o Paleontolo
´gica –
UFC) for access to UFC-721. We all thank the editors
for their patience for missed deadlines and two anonymous
reviewers for their valuable comments.
References
Aires, A.S.S., Kellner, A.W.A., Mu
¨ller, R.T., da
Silva, L.R., Pacheco, C.P. & Dias-Da-Silva,S.
2014. New postcranial elements of the Thalasso-
drominae (Pterodactyloidea, Tapejaridae) from the
Romualdo Formation (Aptian– Albian), Santana
Group, Araripe Basin, Brazil. Palaeontology,57,
343–355.
Andres,B.&Ji, Q. 2008. A new pterosaur from the Liao-
ning Province of China, the phylogeny of the Ptero-
dactyloidea, and the convergence in their cervical
vertebrae. Palaeontology,51, 453– 469.
Andres,B.&Myers, T.S. 2013. Lone star pterosaurs.
Earth and Environmental Sciences Transactions of
the Royal Society of Edinburgh,1, 383– 398, https://
doi.org/10.1017/S1755691013000303
Andres, B., Clark, J.M. & Xu, X. 2014. The earliest
pterodactyloid and the origin of the group. Current
Biology,24, 1011– 1016.
Averianov, A.O. 2010. The osteology of Azhdarcho lan-
cicollis Nessov, 1984 (Pterosauria, Azhdarchidae)
from the Late Cretaceous of Uzbekistan. Proceedings
of the Zoological Institute of the Russian Academy of
Sciences,314, 264– 317.
Averianov, A.O. 2013. Reconstruction of the neck of
Azhdarcho lancicollis and lifestyle of azhdarchids
(Pterosauria, Azhdarchidae). Paleontological Jour-
nal,47, 203– 209, https:// doi.org/10.1134/S00310
30113020020
ENIGMATIC PTEROSAUR FROM THE CRATO FORMATION
Barling, N., Martill, D.M., Heads, S.W. & Gallien,
F. 2015. High fidelity preservation of fossil insects
from the Crato Formation (Lower Cretaceous) of
Brazil. Cretaceous Research,52, 605– 622.
Bennett, C.S. 2001. The osteology and functional mor-
phology of the Late Cretaceous pterosaur Pteranodon.
Palaeontographica Abteilung A,260, 1– 153.
Bonde,N.&Christiansen, P. 2003. The detailed anat-
omy of Rhamphorhynchus: axial pneumaticity and its
implications. In:Buffetaut,E.&Mazin, J.M.
(eds) Evolution and Palaeobiology of Pterosaurs.
Geological Society, London, Special Publications,
217, 217–232, https://doi.org/10.1144/GSL.SP.2003.
217.01.13
Buisonje
´, P.H. 1980. Santanadactylus brasilensis nov.
gen., nov. sp., a long-necked, large pterosaurier from
the Aptian of Brazil. Proceedings of the Koninklijke
Nederlandse Akademie Van Wetenschappen, Series
B,83, 145– 172.
Cai,Z.&Wei, F. 1994. On a new pterosaur (Zhejiangop-
terus linhaiensis gen. et sp. nov.) from Upper
Cretaceous in Linhai, Zhejiang, China. Vertebrata
Palasiatica,32, 181– 194.
Catto, B., Jahnert, R.J., Warren, L.V., Vareja
˜o, F.G.
&Assine, M.L. 2016. The microbial nature of
laminated limestones: Lessons from the Upper
Aptian, Araripe Basin, Brazil. Sedimentary Geology,
341, 304– 315, https://doi.org/10.1016/j.sedgeo.2016.
05.007
Costa, F.R., Saya
˜o, J.M. & Kellner, A.W.A. 2015.
New pterosaur material from the Upper Jurassic of
Tendaguru (Tanzania), Africa. Historical Biology,
27, 646– 655.
Dong, Z. 1982. A new pterosaur (Huanhepterus quingyan-
gensis gen. et sp. nov.) from Ordos, China. Vertebrata
Palasiatica,20, 115– 121.
Dong, Z.-M., Sun, Y.-W. & Wu, S.-Y. 2003. On a new
pterosaur from the Lower Cretaceous of Chaoyang
Basin, Western Liaoning, China. Global Geology,22,
1–7.
Eck, K., Elgin, R.A. & Frey, E. 2011. On the osteology
of Tapejara wellnhoferi Kellner 1989 and the first
occurrence of a multiple specimen assemblage from
the Santana Formation, Araripe Basin, NE-Brazil.
Swiss Journal of Palaeontology,130, 277– 296.
Feldmann, R.M. 1989. Whitening fossils for photo-
graphic purposes. In:Feldmann, R.M., Chapman,
R.E. & Hannibal, J.T. (eds) Paleotechniques.
Paleontological Society, Special Publications, 4,
342–346.
Frey, E., Buchy, M.C., Stinnesbeck, W., Gonza
´lez,
A.G. & Stefano, A. 2006. Muzquizopteryx coa-
huilensis, n. g., n. sp., a nyctosaurid pterosaur with
soft tissue preservation from the Coniacian (Late
Cretaceous) of northeast Mexico (Coahuila). Oryctos,
6, 19–40.
Goloboff, P.A., Farris, J.S. & Nixon, K. 2003. TNT:
Tree analysis using New Technology. Version 1.1. Pro-
gram and documentation, http://www.zmuc.dk/pub
lic/phylogeny/TNT/
Headden, J.A. & Campos, H.B.N. 2014. An unusual
edentulous pterosaur from the Early Cretaceous
Romualdo Formation of Brazil. Historical Bio-
logy: An International Journal of Paleobiology,27,
815–826, https:// doi.org/10.1080/08912963.2014.
904302
Heimhofer, U., Ariztegui, D., Lenniger, M., Hes-
selbo, S.P., Martill, D.M. & Rios-Netto, A.M.
2010. Deciphering the depositional environment of
the laminated Crato fossil beds (Early Cretaceous,
Araripe Basin, North-eastern Brazil). Sedimentology,
57, 677– 694.
Howse, S.C.B. 1986. On the cervical vertebrae of the
Pterodactyloidea (Reptilia: Archosauria). Zoological
Journal of the Linnean Society,88, 307–328.
Ibrahim, N., Unwin, D.M., Martill, D.M., Baidder,L.
&Zouhri, S. 2010. A new pterosaur (Pterodactyloi-
dea: Azhdarchidae) from the Upper Cretaceous of
Morocco. PLoS ONE,5, e10875, https://doi.org/10.
1371/journal.pone.0010875
Kaup, S.S. 1834. Versuch einer Eintheilung der Sauge-
thiere in 6 Sta
¨mme und der Amphibien in 6 Ordnung.
Isis von Oken,1834, 311–324.
Kellner, A.W.A. 1995. The relationships of the Tapejar-
idae (Pterodactyloidea) with comments on pterosaur
phylogeny. In:Sun,A.&Wang, Y. (eds) Sixth Sym-
posium on Mesozoic Terrestrial Ecosystems and
Biota, Short Papers. China Ocean Press, Beijing,
73–77.
Kellner, A.W.A. 2003. Pterosaur phylogeny and com-
ments on the evolutionary history of the group.
In:Buffetaut,E.&Mazin, J.M. (eds) Evolution
and Palaeobiology of Pterosaurs. Geological Society,
London, Special Publications, 217, 105–137, https://
doi.org/10.1144/GSL.SP.2003.217.01.10
Kellner, A.W.A. 2004. New information on the Tapejar-
idae (Pterosauria, Pterodactyloidea) and discussion
of the relationships of this clade. Ameghiniana,41,
521–534.
Kellner, A.W.A. 2010. Comments on the Pterano-
dontidae (Pterosauria, Pterodactyloidea) with the
description of two new species. Anais da Academia
Brasileira de Cie
ˆncias,82, 1063– 1084, https:// doi.
org/10.1590/S0001-37652010000400025
Kellner, A.W.A. 2013. A new unusual tapejarid (Ptero-
sauria, Pterodactyloidea) from the Early Cretaceous
Romualdo Formation, Araripe Basin, Brazil. Earth
and Environmental Sciences Transactions of the
Royal Society of Edinburgh,103, 1–14.
Kellner, A.W.A. & Campos, D.A. 2007. Short note on
the ingroup relationships of the Tapejaridae (Pterosau-
ria, Pterodactyloidea). Boletim do Museu Nacional –
Geologia,75, 1– 14.
Kellner, A.W.A. & Langston,W.J
R. 1996. Cranial
remains of Quetzalcoatlus (Pterosauria, Azhdarchidae)
from Late Cretaceous sediments of Big Bend Natio-
nal Park. Journal of Vertebrate Paleontology,16,
222–231.
Kellner, A.W.A. & Tomida, Y. 2000. Description of
a New Species of Anhangueridae (Pterodactyloidea)
with Comments on the Pterosaur Fauna from the San-
tana Formation (Aptian –Albian), Northeastern Brazil.
National Science Museum, Tokyo, Monographs, 17.
Kellner, A.W.A., Campos, D.A.
et al
. 2013. The largest
flying reptile from Gondwana: a new specimen of
Tropeognathus cf. T. mesembrinus Wellnhofer, 1987
(Pterodactyloidea, Anhangueridae) and other large
pterosaurs from the Romualdo Formation, Lower
M. E. C. LEAL ET AL.
Cretaceous, Brazil. Anais da Academia Brasileira de
Cie
ˆncias,85, 113– 135, https:// doi.org/10.1590/
S0001-37652013000100009
Liu, D.-X., Zhou, C.-F., Wang, J.-Q., Li, W.-G. & Wei,
Q.-W. 2014. New data on the cervical morphology of
the Chinese tapejarine. Historical Biology: An Interna-
tional Journal of Paleobiology,27, 638– 645, https://
doi.org/10.1080/08912963.2014.885962
Lu
¨,J.&Ji, Q. 2005. New azhdarchid pterosaur from the
Early Cretaceous of Western Liaoning. Acta Geologica
Sinica,79, 301– 307.
Lu
¨,J.&Zhang, B.K. 2005. New pterodactyloid pterosaur
from the Yixian Formation of western Liaoning. Geo-
logical Review,51, 458– 462.
Lu
¨, J., Gao, C., Liu, J., Meng,Q.&Ji, Q. 2006a.
New material of the pterosaur Eopteranodon from
the Early Cretaceous Yixian Formation, western
Liaoning, China. Geological Bulletin of China,25,
555–571.
Lu
¨, J., Gao, Y., Xing, L., Li,Z.&Ji, Q. 2006b. A new spe-
cies of Huaxiapterus (Pterosauria: Tapejaridae) from
the Early Cretaceous of western Liaoning, China.
Acta Geologica Sinica,81, 683– 687.
Lu
¨, J., Unwin, D.M., Xu,L.&Zhang, X. 2008. A
new azhdarchoid pterosaur from the Lower Creta-
ceous of China and its implications for pterosaur phy-
logeny and evolution. Naturwissenschaften,95,
891–897.
Maisey, J.G. 1991. Santana Fossils: an Illustrated Atlas.
Neptune, TFH Publications Inc.
Martill, D.M. 2007. The age of the Cretaceous Santana
Formation fossil Konservat Lagersta
¨tte of north-east
Brazil: a historical review and an appraisal of the bio-
chronostratigraphic utility of its palaeobiota. Creta-
ceous Research,28, 895– 920.
Martill, D.M. 2011. A new pterodactyloid pterosaur
from the Santana Formation (Cretaceous) of Brazil.
Cretaceous Research,32, 236– 243.
Martill, D.M. & Heimhofer, U. 2007. Stratigraphy of
the Crato Formation. In:Martill, D.M., Bechly,G.
&Loveridge, R.F. (eds) The Crato Fossil Beds of
Brazil: Window into an Ancient World. Cambridge
University Press, Cambridge, 25– 43.
Martill, D.M. & Naish, D. 2006. Cranial crest develop-
ment in the azhdarchoid pterosaur Tupuxuara, with a
review of the genus and tapejarid monophyly. Palae-
ontology,49, 925– 941.
Nessov, L.A. 1984. Pterosaurs and birds of the Late Creta-
ceous of Central Asia. Pala
¨ontologische Zeitschrift,1,
47– 57.
Neumann, V.H. & Cabrera, L. 1999. Una nueva
propuesta estratigrafica para la tectonosecuencia
post-rifte de la cuenca de Araripe, Noreste de Brasil.
In:Boletim do 58Simpo
´sio Sobre o Creta
´ceo do Brasil
e18Simpo
´sio Sobre el Creta
´cico de Ame
´rica del Sur
Serra Negra-SP. UNESP, Rio Claro, Brazil, 279–285.
Pe
ˆgas, R.V., Leal, M.E.C. & Kellner, A.W.A. 2016. A
Basal Tapejarine (Pterosauria; Pterodactyloidea; Tape-
jaridae)from the Crato Formation, Early Cretaceous of
Brazil. PLoS ONE,11, e0162692.
Pereda Suberbiola, X., Bardet, N., Jouve, S., Iaro-
che
´ne, M., Bouya,B.&Amaghzaz, M. 2003. A
new azhdarchid pterosaur from the Late Cretaceous
phosphates of Morocco. In:Buffetaut,E.&
Mazin, J.M. (eds) Evolution and Palaeobiology of
Pterosaurs. Geological Society, London, Special Pub-
lications, 217, 79–90, https:// doi.org/10.1144/GSL.
SP.2003.217.01.08
Pinheiro, F.L., Fortier, D.C., Schultz, C.L., Andrade,
J.A.F.G. & Bantim, R.A.M. 2011. New information
of the pterosaur Tupandactylus imperator, with com-
ments on the relationships of Tapejaridae. Acta Palae-
ontologica Polonica,56, 567– 580.
Plieninger, F. 1901. Beitra
¨ge zur Kenntnis der Flugsau-
rier. Palaeontographica,48, 65– 90.
Rodrigues,T.&Kellner, A.W.A. 2013. Taxonomic
review of the Ornithocheirus complex (Pterosauria)
from the Cretaceous of England. ZooKeys,308, 1 –112.
Saya
˜o, J.M. & Kellner, A.W.A. 2006. Novo esqueleto
parcial de pterossauro (Pterodactyloidea, Tapejaridae)
do Membro Crato (Aptiano), Formac¸a
˜o Santana, Bacia
do Araripe, nordeste do Brasil. Estudos Geolo
´gicos,
16, 16–40.
Steel, L., Martill, D.M., Kirk, J.R.J., Anders, A.,
Loveridge, R.F., Frey,E.&Martin, J.G. 1997. Ara-
mbourgiania philadelphiae: giant wings in small halls.
Geological Curator,6, 305– 313.
Toombs, H.A. & Rixon, A.E. 1959. The use of acids in the
preparation of vertebrate fossils. Curator: The Museum
Journal,2, 304– 312.
Unwin, D.M. & Martill, D.M. 2007. Pterosaurs from the
Crato Formation. In:Martill, D.M., Bechly,G.&
Loveridge, R.F. (eds) The Crato Fossil Beds of Brazil:
Window into an Ancient World. Cambridge University
Press, Cambridge, 475– 524.
Valenc¸a, L.M.M., Neumann, V.H. & Mabesone, J.M.
2003. An overview on Callovian–Cenomanian intra-
cratonic basins of northeast Brazil: onshore strati-
graphic record of the opening of the southern
Atlantic. Geologica Acta,1, 261– 275.
Veldmeijer, A.J., Signore,M.&Meijer, H.J.M. 2005.
Description of two pterosaur (Pterodactyloidea) man-
dibles from the Lower Cretaceous Santana Formation,
Brazil. Deinsea,11, 67– 86.
Vila Nova, B.C., Saya
˜o, J.M., Lange, M.C. & Kellner,
A.W.A. 2015. Comments on the cervical vertebrae of
the Tapejaridae (Pterosauria, Pterodactyloidea) with
description of new specimens. Historical Biology: An
International Journal of Paleobiology,27, 770– 780,
https://doi.org/10.1080/08912963.2015.1007049
Vremir, M., Kellner, A.W.A., Naish,D.&Dyke, G.J.
2013. A new Azhdarchid pterosaur from the Late Cre-
taceous of the Transylvanian Basin, Romania: implica-
tions for Azhdarchid diversity and distribution. PLoS
ONE,8, e54268, https://doi.org/10.1371/journal.
pone.0054268
Vremir, M., Witton, M., Naish, D., Dyke, G., Bru-
satte, S.L., Norell,M.&Totoianu, R. 2015. A
medium-sized robust-necked azhdarchid pterosaur
(Pterodactyloidea: Azhdarchidae) from the Maas-
trichtian of Pui (Hat¸eg Basin, Transylvania, Roma-
nia). American Museum Novitates,3827, 1– 16.
Vullo, R., Maruga
´n-Lobo
´n,J.
et al
. 2012. A new
crested pterosaur from the Early Cretaceous of Spain:
the first European tapejarid (Pterodactyloidea: Azh-
darchoidea). PLoS ONE,7, e38900.
Wang,X.&Zhou, Z. 2003a. Two new pterodactyloid
pterosaurs from the Early Cretaceous Jiufotang
ENIGMATIC PTEROSAUR FROM THE CRATO FORMATION
Formation of Western Liaoning, China. Vertebrate
Palasiatica,41, 34– 41.
Wang,X.&Zhou, Z. 2003b. A new pterosaur (Pterodac-
tyloidea, Tapejaridae) from the Early Cretaceous
Jiufotang Formation of western Liaoning, China and
its implications for biostratigraphy. Chinese Science
Bulletin,48, 16– 23.
Wang, X., Kellner, A.W.A., Zhou,Z.&Campos, D.A.
2007. A new pterosaur (Ctenochasmatidae, Archaeop-
terodactyloidea) from the Lower Cretaceous Yixian
Formation of China. Cretaceous Research,28,
245–260.
Wang, X., Kellner, A.W.A., Jiang,S.&Cheng,X.
2012. New toothed flying reptile from Asia: Close
similarities between early Cretaceous pterosaur faunas
from China and Brazil. Naturwissenschaften,99,
249–257.
Wang, X., Shen, C., Gao,C.&Jin, K. 2014. New
material of Feilongus (Reptilia: Pterosauria) from the
Lower Cretaceous Jiufotang Formation of Western
Liaoning. Acta Geologica Sinica,88, 13–17.
Wellnhofer,P.&Kellner, A.W.A. 1991. The skull of
Tapejara wellnhoferi Kellner (Reptilia, Pterosauria)
from the Lower Cretaceous Santana Formation of the
Araripe Basin, Northeastern Brazil. Mitteilungen der
Bayerischen Staatssammlung fu
¨r Pala
¨ontologie und
Historische Geologie,31, 89– 106.
Witton, M.P. 2008. A new azhdarchoid pterosaur from
the Crato Formation (Lower Cretaceous, Aptian?) of
Brazil. Palaeontology,51, 1289– 1300.
Witton, M.P. 2013. Pterosaurs: Natural History, Evolution,
Anatomy. Princeton University Press, Princeton, NJ.
Zhou, C.-F. 2010. New material of Chaoyangopterus
(Pterosauria: Pterodactyloidea) from the Early Creta-
ceous Jiufotang Formation of western Liaoning,
China. Neues Jahrbuch fu
¨r Geologie und Pala
¨ontolo-
gie, Abhandlungen,257, 341– 350, https:// doi.org/
10.1127/0077-7749/2010/0081
M. E. C. LEAL ET AL.
