ArticlePDF Available

The ontogenetic growth of Anhangueridae (Pterosauria, Pterodactyloidea) premaxillary crests as revealed by a crestless Anhanguera specimen


Abstract and Figures

The Anhangueridae are a clade of toothed pterodactyloid pterosaurs, known from their characteristicanteriorly expanded premaxillae and conspicuous rostral sagittal premaxillary and dentary crests. Most knownanhanguerids come from the Lower Cretaceous Romualdo Formation within the Araripe Basin of northeast Brazil. Withfour currently valid genera and several specimens referred to the clade, anhanguerids are the most abundant and diversetetrapod group in the Romualdo Formation. However, some studies suggest this diversity may be overestimated, as manytaxa have been diagnosed based on subtle differences in their premaxillary crests, a structure argued to be eitherontogenetically variable or sexually dimorphic. Here we describe an anterior fragment of a gracile pterosaur rostrum thatpossesses the single diagnostic feature of Anhanguera (fifth and sixth pairs of dental alveoli smaller than the fourth andseventh), but lacks a sagittal crest. The affinities of the new fossil among other toothed pterosaurs were tested throughboth cladistic and geometric morphometric approaches, which allow referral of the new specimen to Anhanguera. Theabsence of a crest in the new specimen of Anhanguera suggests that this structure varies in terms of ontogeny and/or sex, and that perhaps it was influenced by sexual selection.
Content may be subject to copyright.
Full Terms & Conditions of access and use can be found at
Journal of Vertebrate Paleontology
ISSN: (Print) (Online) Journal homepage:
The ontogenetic growth of Anhangueridae
(Pterosauria, Pterodactyloidea) premaxillary crests
as revealed by a crestless Anhanguera specimen
Rudah Ruano C. Duque, Felipe L. Pinheiro & Alcina Magnólia Franca Barreto
To cite this article: Rudah Ruano C. Duque, Felipe L. Pinheiro & Alcina Magnólia Franca Barreto
(2022): The ontogenetic growth of Anhangueridae (Pterosauria, Pterodactyloidea) premaxillary
crests as revealed by a crestless Anhanguera specimen, Journal of Vertebrate Paleontology, DOI:
To link to this article:
View supplementary material
Published online: 11 Oct 2022.
Submit your article to this journal
View related articles
View Crossmark data
Laboratório de Paleontologia, Universidade Federal de Pernambuco (UFPE), Centro de Tecnologia e Geociências, Departamento
de Geologia, Av. Acadêmico Hélio Ramos s/n, Cidade Universitária, Recife, Pernambuco, 50740-530, Brazil,;;
Laboratório de Paleobiologia, Universidade Federal do Pampa, Rua Aluízio Barros Macedo, s/n. BR 290 - km 423, São Gabriel, Rio
Grande do Sul, 97307-020, Brazil,
ABSTRACTThe Anhangueridae are a clade of toothed pterodactyloid pterosaurs, known from their characteristic
anteriorly expanded premaxillae and conspicuous rostral sagittal premaxillary and dentary crests. Most known
anhanguerids come from the Lower Cretaceous Romualdo Formation within the Araripe Basin of northeast Brazil. With
four currently valid genera and several specimens referred to the clade, anhanguerids are the most abundant and diverse
tetrapod group in the Romualdo Formation. However, some studies suggest this diversity may be overestimated, as many
taxa have been diagnosed based on subtle differences in their premaxillary crests, a structure argued to be either
ontogenetically variable or sexually dimorphic. Here we describe an anterior fragment of a gracile pterosaur rostrum that
possesses the single diagnostic feature of Anhanguera (fth and sixth pairs of dental alveoli smaller than the fourth and
seventh), but lacks a sagittal crest. The afnities of the new fossil among other toothed pterosaurs were tested through
both cladistic and geometric morphometric approaches, which allow referral of the new specimen to Anhanguera.The
absence of a crest in the new specimen of Anhanguera suggests that this structure varies in terms of ontogeny and/or sex,
and that perhaps it was inuenced by sexual selection.
SUPPLEMENTAL DATASupplemental materials are available for this article for free at
Citation for this article: Duque, R. R. C., F. L. Pinheiro, and A. M. F. Barreto. 2022. The ontogenetic growth of Anhangueridae
(Pterosauria , Pterodactyloidea) premaxillary crests as revealed by a crestless Anhanguera specimen. Journal of Vertebrate
Paleontology. DOI: 10.1080/10.1080/02724634.2022.2116984
The clade Anhangueridae was proposed by Campos and
Kellner (1985) and, since then, its taxonomy has prompted contro-
versy, with several revaluations and propositions of synonymia,
nomina dubia and introduction of new genera (Kellner, 1990;
Kellner and Tomida, 2000; Fastnacht, 2001; Unwin, 2001;Rodri-
gues and Kellner, 2013;Andresetal.,2014; Pinheiro and Rodri-
gues, 2017; Longrich et al., 2018; Pêgas et al, 2019; Holgado and
Pêgas, 2020). Although published taxonomic works may disagree
in several aspects of anhanguerid denition and nomenclature,
they demonstrate that the group reached a considerable diversity
and geographic distribution during the Cretaceous. According to
the most recent propositions, the Anhangueridae consist of 18
species, divided into the taxa Tropeognathinae, Coloborhynchi-
nae, and Anhanguerinae, with specimens found in the U.S.A.,
Brazil, Morocco, England, China, and Australia (Holgado et al.,
2019; Holgado and Pêgas, 2020).
The Anhanguerinae is the Anhangueridae subclade in which
most of the Brazilian representatives are classied, all of them
coming from the Araripe Basin: Ludodactylus,Cearadactylus,
Maaradactylus, and Anhanguera. Among those, Ludodactylus
is the only genus thus far described for the Crato Formation,
and all the remaining were recovered from the Romualdo For-
mation. After the description of Anhanguera blittersdorf
(Campos and Kellner, 1985), tens of anhanguerid skulls have
been collected and reported, being kept in scientic collections
around the world. As a rule, individual anhanguerid species
were described mostly based in subtle morphological discrepan-
cies in their premaxillary crests and overall skull proportions (see
Pinheiro and Rodrigues, 2017). However, albeit still not being a
consensus, it has been suggested by many authors (Bennett, 1992,
1994; Carpenter et al., 2003; Frey et al., 2003; Unwin, 2005;Lu
et al., 2011; Wang et al., 2014; Pinheiro and Rodrigues, 2017)
that the premaxillary crest in pterosaurs is a sexually selected,
dimorphic feature, being subject to ontogenetic variation and
not suitable as a diagnostic feature.
In a review of the genus Anhanguera, Pinheiro and Rodrigues
(2017) reanalyzed supposedly diagnostic features of
A. blittersdorf,A. araripensis,”“A. santanae,”“A. robustus,
A. piscator, and A. spielbergi, revealing that most features pre-
viously used to dene these species were problematic, as they
mainly referred to crest morphology and position, characters
proved to fall within the range of intraspecic variation. Accord-
ing to these authors, after the exclusion of sagittal crest charac-
ters from Anhanguera denition, the single feature kept for
diagnosing the genus was the fth and sixth pairs of teeth
being smaller than the fourth and seventh ones. Pinheiro
and Rodrigues(2017) reappraisal considered only three
species as potentially valid: A. blittersdorf,A. piscator, and
A. spielbergi.
* Corresponding author
Color versions of one or more of the gures in the article can be found
online at
Journal of Vertebrate Paleontology e2116984 (10 pages)
© by the Society of Vertebrate Paleontology
DOI: 10.1080/02724634.2022.2116984
Published online 11 Oct 2022
Here we present a new pterosaur specimen from the
Romualdo Formation, which comprises the anterior portion of
a long rostrum that, albeit lacking a sagittal premaxillary crest,
is consistent with its identication as Anhanguera. Phylogenetic
and geometric morphometric analyses were run in order to
recover the afnities of the new material, as well as to test the
validity of rostral dental alveoli size and distribution in the taxon-
omy of anhanguerids and similar taxa.
The Araripe Basin is arguably the most complex interior sedi-
mentary basin of northeastern Brazil, having its origins and evol-
ution related to the splitting of the African and South American
continents (Assine, 1992). It is limited to the north by the Patos
Lineament and to the south by the Farias Brito Fault, being
inserted over the Precambrian Borborema Province. Its area
covers the southern of Ceará, eastern of Piauí, and western of
Pernambuco states (Fig. 1A), with a 38°3040°55W longitude
and 7°057°50S latitude (Viana and Neumann, 2002).
The Santana Group is composed by three sedimentary units,
from bottom to top: the Crato, Ipubi, and Romualdo formations
(Assine, 1992; Neumann and Cabrera, 1999). Among those, the
Crato and Romualdo Formations are the best known, as much
for their faciological complexity, as for their abundant and excep-
tionally preserved fossils. The Romualdo Formation, which had
its deposition between the Neoaptian and the Eoalbian, is
characterized by a sequence of claystone and dark gray/black
marine shales, with presence of several levels where limestone
concretions are abundant, most of them preserving fossils
within. The Romualdo Formation has produced the largest diver-
sity of pterosaurs of the Santana Group. Above the concretion-
bearing levels, the Romualdo Formation displays slim layers of
coquinas and cochinoid limestone (Assine et al., 2014).
The studied specimen comes from the southern region of the
Araripe Basin, in a locality known as Sítio Gomes,
located in the homonymous district, Exu County (Fig. 1A),
western Pernambuco state. It was exposed on the surface,
within a shale layer over the cochinoid limestone beds
(Fig. 1B), uppermost portion of the Romualdo Formation. The
Sítio Gomes has yielded a great fossil diversity, mainly
composed by shes, identied as Vinctifer,Tharrhias,Rhacolepis,
Neoproscinetes,Notelops,Brannerion,Cladocyclus, and Axelro-
dichthys. A specimen of the testudine Araripemys barretoi was
FIGURE 1. A, map of the Araripe Basin, northeastern Brazil, highlighting the Exu County, Pernambuco, and the location of Sítio Gomes (7°3116
S, 39°3418′′W); B, stratigraphic chart of Sítio Gomes, displaying the level from where DGEO-CTG-UFPE 8283 was collected. Modied from
Duque and Barreto (2018:gs. 12).
Duque et al. Ontogenetic growth of Anhanguera premaxillary crest (e2116984-2)
also recovered, as well as a previously described anhanguerid
pterosaur (Duque and Barreto, 2018).
Institutional AbbreviationsAMNH, American Museum of
Natural History, New York, NY, U.S.A.; BSP, Bayerischen Staats-
sammlung für Paläontologie und Historische Geologie, Munich,
Germany; CAMSM, Sedgwick Museum, Cambridge University,
Cambridge, U.K.; CSRL, Centro Studi e Ricerche Ligabue,
Venice, Italy; DGEO-CTG-UFPE, Departamento de Geologia,
Centro de Tecnologia and Geociências, Universidade Federal de
Pernambuco, Recife, Brazil; IVPP, Institute of Vertebrate Paleon-
tology and Paleoanthropology, Chinese Academy of Sciences,
Beijing, China; IWCMS, Isle of Wight County Museum Service
at Dinosaur Isle, Sandown, Isle of Wight, U.K.; LINHM,Long
Island Natural History Museum, New York, NY, U.S.A.; MN,
Museu Nacional, Rio de Janeiro, Brazil; MPSC, Museu de Paleon-
tologia em Santana do Cariri, Santana do Cariri, Brazil; NHM,
The Natural History Museum, London, U.K.; NSM, National
Museum of Nature and Science, Tokyo, Japan; RGM,Nationaal
Ntuurhistorisch Museum, Leiden, Holland, the Netherlands;
SAO, Sammlung Oberli, St. Gallen, Switzerland; SMNK,Staa-
tliches Museum für Naturkunde, Karlsruhe, Germany; SMU,
Southern Methodist University, Dallas, TX, U.S.A.
Materials, Preparation, and Measurements
The specimen DGEO-CTG-UFPE 8283 consists of the
anterior portion of a slim and long pterosaur rostrum, deposited
in the scientic collection of the Geology Department, Center of
Technology and Geosciences of the Federal University of Per-
nambuco, Recife, Brazil.
The specimen was isolated from a typical Romualdo For-
mation limestone concretion using standard mechanical prep-
aration protocols (Santos, 1985; May et al., 1994). Measures
were taken with a digital universal stainless steel caliper 150
mm/6". Photographs were taken with a Canon EOS Rebel
Camera and edited with the software Adobe Photoshop® CC
and CorelDRA 2019.
Geometric Morphometrics
Two-dimensional geometric morphometrics was applied to test
the relevance of size and position of rostral dental alveoli in the
characterization and diagnosis of anhanguerids and closely
related taxa. In this framework, the analysis was also employed
to test morphological congruence between DGEO-CTG-UFPE
8283 and other specimens that compose the morphometric
dataset we assembled.
A total of 21 specimens were used in the analysis, these being:
the cimoliopterids Camposipterus nasutus (CAMSM B 54556),
Cimoliopterus dunni (SMU 76892), and Cimoliopterus cuvieri
(MHN 39409); two specimens of the hamipterid Hamipterus tian-
shanensis (IVPP V 18935 1 and MN 7536); the tropeognathines
Siroccopteryx moroccensis (LINHM 016) and Tropeognathus
mesembrinus (BSP 1987 I 46); the coloborhynchines Colobor-
hynchus clavirostris (NHM R 1822) and Uktenadactylus wadleighi
(SMU 73058); and the anhanguerines Caulkicephalus trimicrodon
(IWCMS 2002.189.1), Cearadactylus atrox (MN 7019-V), Ceara-
dactylusligabuei (CSRL 12692/12713), Maaradactylus kellneri
(MPSC R 2357), Anhanguera sp. (AMNH 22555), Anhanguera
sp. (SMNK PAL 3895), Anhanguera sp. (NHM R 11978), Anhan-
guera sp. (SAO 16494), Anhanguera sp. (SMNK PAL 2302),
Anhanguera blittersdorf(MN 4805-V), Anhanguera spielbergi
(RGM 401 880), and DGEO-CTG-UFPE 8283.
We used photographs of specimens in ventral view, based on
which 14 landmarks were plotted for each specimen. Landmarks
were taken from the anteriormost and posteriormost limits of
each of the seven rst tooth alveoli. As such, landmarks reect
the size, position, and orientation of alveoli, as well as their rela-
tive distribution throughout the alveolar margin. When alveoli
are anteriorly directed and cannot be seen in ventral view, their
correspondent landmarks were superimposed. The landmarks
were digitalized using the software TPSDig (Rohlf, 2010),
while all analyses were carried out using the MorphoJ software
package, version 1.06a (Klingenberg, 2011). After the Procrustes
superimposition, a Principal Component Analysis (PCA) was
used to investigate morphometric variation within the chosen
sample. As Coloborhynchus clavirostris (NHM R 1822) only pre-
serves its six anteriormost alveoli, missing landmarks were esti-
mated for this specimen by the use of the TPS method
(function estimate.missing) of the Geomorph package (R
environment) (Adams and Otárola-Castillo, 2013).
Phylogenetic Analysis
We assessed the relationships of DGEO-CTG-UFPE 8283
within the phylogenetic framework of Holgado et al. (2019), as
modied by Cerqueira et al. (2021). Scoring of DGEO-CTG-
UFPE 8283 in Cerqueira et al. (2021) data matrix (see the Sup-
plemental Data) resulted in a dataset composed by 61 oper-
ational taxonomic units (OTUs) and 146 characters. All
characters are non-additive and have the same weight. The
analysis was conducted by a heuristic search, using the tree bisec-
tion reconnection algorithm of TNT version 1.5 (Goloboff and
Catalano, 2016), with random seed and 100 replications (100
trees held by replicate). Bremer support values were later calcu-
lated, also using TNT 1.5.
ANHANGUERIA Rodrigues and Kellner, 2013
ANHANGUERIDAE Campos and Kellner, 1985
ANHANGUERINAE Holgado, Pêgas, Canudo, Fortuny,
Rodrigues, Company, and Kellner, 2019
ANHANGUERA Campos and Kellner, 1985
(Fig. 2)
MaterialAnterior fragment of a pterosaur rostrum, DGEO-
CTG-UFPE 8283.
Locality and HorizonRomualdo Formation, Lower Cretac-
eous (Aptian/Albian), Santana Group, Araripe Basin, Exu muni-
cipality, Gomes district (7°3116′′S, 39°3418′′W),
Pernambuco state, Brazil.
PreservationAt the time of the eld prospection, DGEO-
CTG-UFPE 8283 had its largest portion still covered by lime-
stone matrix, forming a long carbonate concretion. At the
exposed portion, a large cavity lled with calcite crystals could
be observed, and a fragmented tooth was also evident at the
surface. After mechanical preparation, the specimen revealed
to be preserved in three dimensions, with no evidence of distor-
tion or attening. Almost the whole left surface of the rostrum
was, however, eroded off prior to collection.
DescriptionAs preserved, the specimen measures 143 mm in
its largest (longitudinal) extension, being 28.6 mm deep in its pos-
terior region. The outer bone wall was, as reported, largely
eroded off prior to collection, being extremely thin (about 0.3
mm thick) in its preserved portions. The specimen is triangular
in transverse section (Fig. 2) and, in lateral view, the rostrum
widens posteriorly, while tapering anteriorly. As a premaxillary
crest is absent, the tip of the rostrum is dorsoventrally at,
being larger than deep in an anterior view.
Duque et al. Ontogenetic growth of Anhanguera premaxillary crest (e2116984-3)
The dorsal surface of the fused premaxillae is anteriorly round,
sharpening posteriorly to form a keel. The suture between the
right premaxilla and the maxilla is visible as a faint line close
to the posterior limit of the specimen, fading at a region near
the seventh tooth position.
As mentioned above, the right side of the specimen is
better preserved, and 12 tooth alveoli are clearly visible com-
posing the right alveolar margin. The specimen bears a con-
spicuous palatal keel, deeper in its posterior end but fading
anteriorly, where the palatal surface becomes convex. The
rst alveolus is anteriorly faced, and the rostrum shows an
anterior expansion that extends until the fth alveolus. Pos-
terior to that, there is a subtly narrower area, where the
sixth and seventh alveoli are located. The right side of the
specimen is completely eroded, but there remains a fragmen-
ted tooth, still articulated to its socket, probably correspond-
ing to the second left element. The erosion made the tooth
root visible, its preserved part being straight, 22 mm long
and 5.4 mm wide, with a circular transverse section. Portions
of the posterior two teeth are also visible, anteroventrally
oriented but broken at their bases.
The fth, sixth, and seventh alveoli are smaller than the
second, third, fourth, and eighth ones. From the rst to the
eighth, the alveoli are mainly circular, the following four being
small and elliptical. The alveoli are increasingly spaced poster-
iorly (Table 1). The sagittal palatal crest begins right after the
seventh alveolus. The crest is well dened posteriorly, rivalling
the alveolar margin in deepness. Anteriorly, it fades to form
the convex anterior palatal surface.
ComparisonSpecimen DGEO-CTG-UFPE 8283 can be
readily assigned to the Anhangueria (Rodrigues and Kellner,
2013) due to the presence of an anterior expansion of the pre-
maxillae and for having its larger teeth placed in the tip of the
rostrum (a feature that can be inferred by measuring alveolar
sizes). The Anhangueria includes Hamipterus,Iberodactylus
and the clade Anhangueridae.
FIGURE 2. DGEO-CTG-UFPE 8283 (Anhanguera sp.) in A, right lateral view; B, left lateral view; C, palatal view; D, dorsal view; E, posterior view; F,
rostral view. Scale bar equals 50 mm.
Duque et al. Ontogenetic growth of Anhanguera premaxillary crest (e2116984-4)
Kellner (1996,2003) considered as synapomorphies of the
Anhangueridae: (1) Premaxillary sagittal crest conned to
anterior portion of skull; (2) Tip of premaxilla slightly expanded;
(3) Short, blade-like dentary sagittal crest. Specimen DGEO-
CTG-UFPE 8283, albeit displaying expanded premaxillae,
lacks a premaxillary crest, supposedly characteristic of the
Anhangueridae. In spite of that, DGEO-CTG-UFPE 8283
shows some diagnostic features of the Anhanguerinae, such as
an enlarged fourth premaxillary tooth, which is larger than the
fth and sixth teeth and as large as (or larger) than the third
tooth (Holgado et al., 2019). In addition, the new specimen dis-
plays a feature considered to be synapomorphic to the genus
Anhanguera: the fth and sixth alveolar pairs are smaller than
the fourth and seventh ones (Kellner, 2003; Pinheiro and Rodri-
gues, 2017). The taxonomic revision of Pinheiro and Rodrigues
(2017), also backgrounded by an extensive morphometric analy-
sis, considered only three Anhanguera species as valid, those
being: Anhanguera blittersdorf,Anhanguera spielbergi, and
Anhanguera piscator.
Anhanguera blittersdorfCampos and Kellner 1985, the type
species of Anhanguera genus, has its holotype (MN 4805-V) con-
sisting of an isolated skull (lacking the lower jaw) with a large
number of alveoli in the upper jaws (26 pairs) and a well-devel-
oped sagittal crest. Based on the fusion degree of cranial bones,
this specimen was referred as a mature individual (Kellner and
Tomida, 2000). As it seems, MN 4805-V and DGEO-CTG-
UFPE 8283 belong in the same genus, as both share the single
Anhanguera synapomorphy (see above). Actually, the most strik-
ing differences between the two specimens are related to the
presence of a premaxillary crest in MN 4805-V and the extension
of the palatal crest, which extends from the fth to the ninth
alveoli in A. blittersdorf.
A second Anhanguera species, Anhanguera spielbergi, is only
known by its holotype (RGM 401 880), which consists of a
large skull displaying an exceptionally deep, blade-like premaxil-
lary crest that begins in the rostral end of the skull and is better
developed than the one of Anhanguera blittersdorfholotype
(MN 4805-V). The palatal keel of RGM 401 880 is as subtle as
the one of DGEO-CTG-UFPE 8283, extending from the fth
to the ninth tooth pairs. Is also noteworthy that the skull of
AMNH 22555 (formerly assigned to Anhanguera santanaeby
Wellnhofer, 1991) apparently lacks a prominent sagittal crest,
even though the dorsal margin of the premaxillae was eroded
off in this particular specimen (Pinheiro and Rodrigues, 2017).
The nine rostral-most tooth alveoli are preserved in AMNH
22555, their distribution throughout the upper jaws being very
similar to what is seen in DGEO-CTG-UFPE 8283. Also, its
palatal crest gently rises starting from the fth pair of
alveoli, in a similar condition to what is displayed by
A. blittersdorf.
In the holotype of Anhanguera piscator (NSM-PV 19892), the
extension of the sutures between the premaxillae and maxillae
cannot be discerned, in a similar condition to what is displayed
by DGEO-CTG-UFPE 8283. In spite of that, the A. piscator
holotype was most likely a juvenile at the time of death, as
demonstrated by the lack of fusion between several bones con-
sidered as ontogenetic proxies. According to Pinheiro and Rodri-
gues (2017), this would explain the low premaxillary crest in this
particular specimen. The fusion between maxillae and premaxil-
lae occurred early in pterosaur ontogeny, thus being a poor
choice as a proxy for ontogenetic development. The size of the
A. piscator premaxillary crest was proposed as diagnostic of
this species by Kellner and Tomida (2000), later disregarded by
Pinheiro and Rodrigues (2017). The holotype of A. piscator
still has its lower jaws in occlusion, preventing from viewing its
palatal morphology.
The specimen SAO 16494, formerly referred to Colobor-
hynchus araripensis by Veldmeijer et al. (2006) was later assigned
to Anhanguera sp. (Pinheiro and Rodrigues, 2017), and has a
well-developed premaxillary crest. SAO 16494 is similar to
DGEO-CTG-UFPE 8283 in having a palatal ridge starting pos-
terior to the seventh tooth pair. This condition differs from
several known Anhanguera skulls. As an example, specimen
NHM R 11978, which also has a well-developed premaxillary
crest, has a palatal crest that rises posterior to the eighth tooth
The Anhanguerinae Cearadactylus atrox (MN 7019-V) differs
from DGEO-CTG-UFPE 8283 for having its four most rostral
tooth pairs larger than the following ones. In addition, its
palatal ridge rises level with the fth tooth pair, and the specimen
probably had a small sagittal premaxillary crest (Vila Nova et al.,
2014). An allegedly second Cearadactylus species, Cearadacty-
lusligabuei, was probably based on a composite, and was inva-
lidated by Vila Nova et al. (2014).
Among the largest anhanguerid skulls known thus far stands
the holotype of Maaradactylus kellneri (MPSC R 2357). In this
species, alveolar pairs fth, sixth and seventh are smaller than
the fourth and eighth, differing, thus, from Anhanguera.The
palate displays a low longitudinal ridge starting close to the
fth tooth pair, and fading level with the 13th. Maaradactylus
kellneri bears a long and deep premaxillary crest (Bantim
et al., 2014). Tropeognathus mesembrinus, also known by large
skull material, has an exceptionally large premaxillary crest,
which extends until the anteriormost limit of the rostrum (Well-
nhofer, 1987). Similar to A. blittersdorf, AMNH 22555, and
Maaradactylus kellneri, the palatal ridge of T. mesembrinus holo-
type (BSP 1987 I 46) begins level with the fth tooth pair (Well-
nhofer, 1987).
Another specimen worth noting is BSP 1991 I 27, described by
Veldmeijer et al. (2009). BSP 1991 I 27 is a fragmentary skull
lacking the tip of the rostrum, as well as several postcranial
elements. BSP 1991 I 27 also comes from the Romualdo For-
mation, and is similar to DGEO-CTG-UFPE 8283 in several
aspects: both are slim, crestless, with a transversal triangular
section and a dorsally expanded and attened anterior portion.
Also, the distance between consecutive alveoli increases in pos-
terior direction (Fig. S2). Differences between both specimens
include the fact that (1) BSP 1991 I 27 would have, if complete,
an about 22% larger rostrum; (2) its last three alveoli are more
rounded than ellipsoid; and (3) the alveoli demonstrate to be
overall larger than the condition observed in DGEO-CTG-
UFPE 8283. In addition, the palatal crest of BSP 1991 I 27
begins more posteriorly when compared with the specimen we
BSP 1991 I 27 was attributed by Veldmeijer et al. (2009)to
Brasileodactylus sp., mainly because of the absence of a
TABLE 1. DGEOCTGUFPE 8283 (Anhanguera sp.), measures of
the dentition in mm.
Alveolus Diastema
Quantity Diameter Quantity Diameter
1 5.14 12 1.97
2 6.3 23 3.38
3 6.37 34 3.17
46 45 3.59
55 56 5.68
6 4.5 677
7 5.34 78 8.8
8 5.8 89 9.4
9 5.85 910 12
10 5.3 1011 12.78
11 5.3 1112 14.8
12 5.2
Duque et al. Ontogenetic growth of Anhanguera premaxillary crest (e2116984-5)
premaxillary crest, which we believe to be a weak diagnostic
feature. Comparisons between BSP 1991 I 27 and Brasileodacty-
lus holotype (MN-4804-V) are limited because the latter only
preserves a mandibular symphysis, which is absent in BSP 1991
I 27. However, BSP 1991 I 27 also appears to present the single
Anhanguera synapomorphy, the fourth and seventh alveoli
being larger than the fth and the sixth ones. As such, BSP
1991 I 27 may also represent a crestless Anhanguera. Unfortu-
nately, the fact that this specimen lacks its anterior rostral end
prevented its inclusion in our morphometric dataset.
Geometric Morphometrics
The Principal Component Analysis results (Fig. 3) are consist-
ent with current phylogenetic and taxonomic propositions for the
relationships of the Anhangueridae and closely related taxa (e.g.,
Holgado and Pêgas, 2020). All the specimens that are
unambiguously assignable to Anhanguera (A.blittersdorf(MN
4805-V), A.spielbergi (RGM 401 880), Anhanguera sp.
(AMNH 22555; SMNK PAL 3895; NHM R 11978 and SAO
16494)) are clustered together in the two-dimensional PCA
Cimoliopterids (Cimoliopterus dunni,C. cuvieri, and Campo-
sipterus) are also clustered together, but the occupied morpho-
space that denes the taxon in our analysis also includes
Siroccopteryx. Interestingly, Maaradactylus stands close to
Caulkicephalus in the horizontal axis (rst principal component),
while Tropeognathus remains alone in the opposite extremity of
this same principal component.
Relevant to our study, specimen DGEO-CTG-UFPE 8283
falls inside the morphospace occupied by unambiguous Anhan-
guera specimens. As such, at least concerning the morphology
of the alveolar margin, the new specimen is indistinguishable
from Anhanguera.
FIGURE 3. Principal Component Analysis of morphometric data collected from 21 analyzed specimens. Landmarks 1 and 14 are depicted in a line
drawing of DGEO-CTG-UFPE 8283. Remaining landmarks (not numbered) should be considered sequentially, in an anterior-posterior direction.
Duque et al. Ontogenetic growth of Anhanguera premaxillary crest (e2116984-6)
Phylogenetic Analysis
Our phylogenetic assessment of DGEO-CTG-UFPE 8283
resulted in 15 equally parsimonious trees of 350 steps each (CI
= 0.65, RI = 0.86). The strict (= Nielsen) consensus (Figs. 4, S1)
recovers DGEO-CTG-UFPE 8283 within a clade together with
Anhanguera piscator, AMNH 22555, and Anhanguera blitters-
dorf. As demonstrated by the consensus topology, all recovered
trees depict DGEO-CTG-UFPE 8283 in a sister-OTU relation-
ship with A. blittersdorf, whereas the relationships of the
clade composed by these two and the remaining Anhanguera
remain unresolved. The clade (DGEO-CTG-UFPE 8283 +
AMNH 22555 + A. piscator +A. blittersdorf) lies in a polytomy
together with Liaoningopterus gui and (Maaradactylus kellneri +
Cearadactylus atrox). As such, our phylogenetic results are in
perfect agreement with the identication of DGEO-CTG-
UFPE 8283 as an additional Anhanguera specimen. Calculated
Bremer support values (Fig. 4) are mainly low, as is usual for pter-
osaur phylogenetic assessments.
As mentioned above, our morphometric analysis of premaxil-
lary and maxillary dental alveoli is consistent with the most
recent taxonomic proposals (Holgado et al., 2019), and demon-
strated to be a useful tool in identifying fragmentary specimens.
Results of our analysis may also shed light on other issues besides
the attribution of DGEO-CTG-UFPE 8283, such as the validity
of the recently erected taxon Cimoliopteridae (Camposipterus
and Cimoliopterus).
When described, the rst Santana Group anhanguerids were
diagnosed by characters that, after further discoveries, were
demonstrated to be either well distributed within the clade
or ontogenetically variable. As such, several Anhanguera
species were recently invalidated, such as A. cuvieri,
A. ttoni,”“A. araripensis,”“A. santanae,and A. robustus
(Pinheiro and Rodrigues, 2017). The geometric morpho-
metric-based allometric regressions of Pinheiro and Rodrigues
(2017) demonstrated a strong positive allometric growth in the
sampled anhanguerid skulls, especially with respect to their
sagittal crests. It was, then, concluded that crest size and pos-
ition are strongly ontogenetically controlled in Anhanguera
(Fig. 5), being poor choices for the diagnosis of nominal
taxa. We should note that, in our PCA results, the specimens
recovered in the closest position to DGEO-CTG-UFPE 8283
were AMNH 22555 and SMNK PAL 3895. Curiously, both rep-
resent the Anhanguera specimens with the smallest sagittal
crests. The rst (AMNH 22555) features a short rostrum and
an apparently better-developed crest, while the latter (SMNK
PAL 3895) presents a comparatively long rostrum and a very
subtle crest.
It has already been discussed (e.g., Bennett, 1992,1994,2006;
Carpenter et al., 2003; Frey et al., 2003; Unwin, 2005) that ptero-
saur premaxillary crests are potentially sexually dimorphic and
subject to ontogenetic variation, being of limited use as diagnos-
tic features. In 2014, two unexpected discoveries added to this
discussion, shedding light over interesting aspects of pterosaur
biology. One assemblage with at least 47 individuals of different
growth stages showed that the ontogenetic variation in Caiuajara
dobruskii is reected mainly by the size and inclination of its pre-
maxillary crest, with this structure becoming bigger and steeper
in the course of the development, in a characteristic positive allo-
metric growth (Manzig et al., 2014). The second study reports the
discovery of a 40-individual bonebed containing males and
females of Hamipterus tianshanensis, as well as several eggs.
Wang et al. (2014) demonstrated that the rostral anterior expan-
sion is an ontogenetic feature in Hamipterus and that the pre-
maxillary crests size and shape are sexually dimorphic within
the species.Three years before, sexual dimorphism in pterosaurs
was already reported for Chinese specimens, when et al.
FIGURE 4. Simplied strict consensus of the most parsimonious trees recovered in the preferred cladistic analysis. Values correspond to Bremer
support. Silhouettes by the author, not to scale.
Duque et al. Ontogenetic growth of Anhanguera premaxillary crest (e2116984-7)
(2011) described a Darwinopterus specimen associated with two
eggs, which was later attributed to Kunpengopterus (Wang et al.,
2015; Zhou et al., 2021). That nding, together with the assess-
ment of several other similar specimens, showed that the darwi-
nopteran males had relatively small pelvises and large cranial
crests, while females had larger pelvises and lacked cranial
crests. Variations on pelvis morphology and crest shape were
also observed in Pteranodon, while, in this genus, both males
and females present crests, those of the males being larger than
the ones of the assumed females (Bennett, 1992,1994). This
mutual sexual selection (where both males and females are orna-
mented and both select mates) is also a reality in extant animals,
and thus cannot be ignored as a possibility for some pterosaurs
(Hone et al., 2012).
The holotype of Brasileodactylus araripensis (MN 4804-V)
consists of a crestless fragmented mandibular symphysis
(Kellner, 1984). While analyzing the ontogeny of the four speci-
mens attributed to Brasileodactylus at that time, Bennett (2018)
highlighted several similarities between Brasileodactylus and
Anhanguera. Both AMNH 24444 and BSP 1991 I 27 show signs
of size-independent skeletal immaturity (Bennett, 2018). When
rst described by Veldmeijer (2003), AMNH 24444 was still
embedded within its original carbonaceous concretion, with the
exposed portions of its right premaxilla and dentary considerably
eroded, which prevents the recognition of the diagnostic charac-
ters of Anhanguera and Brasileodactylus. The attribution of
AMNH 24444 to Brasileodactylus is, thus, debatable and, as far
as the Brasileodactylus record goes, the relationship between
this genus and Anhanguera is still elusive, and more complete
specimens of the former are needed in order to enlighten this
All the proposed Anhanguera species were traditionally
diagnosed by the presence of a premaxillary sagittal crest con-
ned to the rostral end of the skull, subtle variations of this
structure being the main distinguishing features between
nominal taxa (Campos and Kellner, 1985; Kellner and
Tomida, 2000). Comprehensive assessments of Anhanguera
ontogeny (e.g., Pinheiro and Rodrigues, 2017) are recent, and
demonstrate that the strong allometric growth of premaxillary
crests makes those structures ill-suited for taxonomic purposes
(Fig. 5). We presented, here, strong anatomical, morphometric,
and phylogenetic support for the attribution of DGEO-CTG-
UFPE 8283 to Anhanguera sp., this being the rst crestless
Anhanguera recognized as such. The existence of crestless
Anhanguera individuals is in perfect agreement with the onto-
genetic growth of pterosaur headcrests, as well as with the pro-
posed use of the crests as display ornaments. While the
ontogenetic growth of Anhanguera premaxillary crests was
FIGURE 5. Artistic reconstruction based on specimen DGEO-CTG-UFPE 8283. A, skull of a young individual; B, reconstructed skull of an onto-
genetically advanced individual. Scale bar equals 100 mm. Digital painting by Matheus Fernandes Gadelha.
Duque et al. Ontogenetic growth of Anhanguera premaxillary crest (e2116984-8)
already well-established, we should also consider the possibility
that this structure was sexually dimorphic within the genus, an
issue that will probably be solved by future discoveries and
comprehensive analyses of recovered samples.
Geometric morphometrics applied to dental alveoli has
proved to be a useful tool in investigating the relationships of
toothed pterosaurs taxa, especially with regard to fragmentary
specimens. Morphometrics, thus, appears to be a more efcient
tool than the use of sagittal crests as diagnostic features, a prac-
tice that resulted in an overestimated diversity of Romualdo For-
mation pterosaurs (Pinheiro and Rodrigues, 2017).
All the methodological approaches we used (anatomy, mor-
phometrics, and phylogenetics) are in agreement with the identi-
cation of DGEO-CTG-UFPE 8283 as a further Anhanguera
specimen. The lack of a premaxillary crest in the new specimen
is consistent with intrageneric variation, probably reecting the
fact that Anhanguera premaxillary crests were strongly con-
trolled by ontogeny, sexual dimorphism also not being discarded.
RRCD and AMFB: We thank the city hall of Exu and FUN-
DARPE for supporting this research; G. Cordeiro and
C. Marcelino for their valuable eld assistance. FLP: M. Norell
and C. Mehling (AMNH); R. Bantim (MPSC); O. Rauhut and
M. Moser (SNSB-BSPG); A. Kellner and H. Silva (MN);
E. Frey (SMNK); R. Schoch (SMNS); S. Chapman and L. Steel
(NHMUK); D. Pemberton and M. Riley (CAMSM). We thank
J. Bubadué (UENF) for insights on the morphometrics method-
ology. The manuscript was greatly improved by insightful com-
ments from referees C. Bennett and R. Pêgas. This study was
nanced by grants from the Conselho Nacional de Desenvolvi-
mento Cientíco e Tecnológico (CNPq 303071/2014-1 to
RRCD; CNPq 407969/2016-0; 305758/2017-9 to FLP) and Fun-
cultura Independente Project (0756/2014 to RRCD).
Rudah Ruano C. Duque
Felipe L. Pinheiro
Alcina Magnólia Franca Barreto
Adams, D. C., and E. Otárola-Castillo. 2013. Geomorph: an R package
for the collection and analysis of geometric morphometric shape
data.Methods in Ecology and Evolution 4:393399.
Andres, B., J. Clarck, and X. Xu. 2014. The earliest pterodactyloid and the
origin of the group. Current Biology 24:10111016.
Assine, M. L. 1992. Análise Estratigráca da Bacia do Araripe, Nordeste
do Brasil. Revista Brasileira de Geociências 22:289300.
Assine, M. L., J. A. Periotto, M. A. Custódio, V. H. Neumann, F. G.
Varejão, and P. C. Mescolotti. 2014. Sequências deposicionais do
Andar Alagoas da Bacia do Araripe, Nordeste do Brasil. Boletim
de Geociências da Petrobrás, Rio de Janeiro 22:328.
Bantim, R. A. M., A. A. F. Saraiva, J. M. Sayão. 2014. A new toothed pter-
osaur (Pterodactyloidea: Anhangueridae) from the Early
Cretaceous Romualdo Formation, NE Brazil. Zootaxa 3869:201
Bennett, S. C. 1992. Sexual dimorphism of Pteranodon and other ptero-
saurs, with comments on cranial crests. Journal of Vertebrate
Paleontology 12:422434.
Bennett, S. C. 1994. Taxonomy and systematics of the Late Cretaceous
pterosaur Pteranodon (Pterosauria, Pterodactyloidea). Natural
History Museum, University of Kansas Occasional Papers 169:170.
Bennett, S. C. 2006. Juvenile specimens of the pterosaur
Germanodactylus cristatus, with a review of the genus. Journal of
Vertebrate Paleontology 26: 872878.
Bennett, S. C. 2018. New smallest specimen of the pterosaur Pteranodon
and ontogenetic niches in pterosaurs. Journal of Paleontology
Campos, D. A., and A. W. A. Kellner. 1985. Panorama of the ying rep-
tiles study in South America. Anais da Academia Brasileira de
Ciências 57:453466.
Carpenter, K., D. M., Unwin, K. Cloward, C. Miles, and C. Miles. 2003.A
new scaphognathine pterosaur from the Upper Jurassic Morrison
Formation of Wyoming, USA; pp217:4554 in E. Buffetaut; J. M.
Mazrn (eds) Evolution and Palaeobiology of Pterosaurs.
Wyoming. Geological Society of London, Special Publications.
Cerqueira, G. M., M. A. Santos, M. F. Marks, J. M. Sayão, and F. L.
Pinheiro. 2021. A new azhdarchoid pterosaur from the Lower
Cretaceous of Brazil and the paleobiogeography of the
Tapejaridae. Acta Palaeontologica Polonica 66:555570.
Duque, R. R. C., and A. M. F. Barreto. 2018. Novos sítios fossilíferos da
Formação Romualdo, Cretáceo Inferior, Bacia do Araripe, Exu,
Pernambuco, Nordeste do Brasil. Anuário do Instituto de
Geociências 41:514.
Fastnacht, M. 2001. First record of Coloborhynchus (Pterosauria) from
the Santana Formation (Lower Cretaceous) of the Chapada do
Araripe, Brazil. Paläontologische Zeitschrift 75:23.
Frey, E., D. M. Martill, and M. C. Buchy. 2003. A new rested ornitho-
cheirid from the lower Cretaceous of northeastern Brazil and the
unusual death of an unusual pterosaur; pp. 217:5563 in E.
Buffettaut and J. M. Mazin (eds.) Evolution and Palaeobiology of
Pterosaurs, Geological Society Special Publications.
Goloboff, P. A., and S. A. Catalano. 2016. TNT version 1.5, including a
full implementation of phylogenetic morphometrics. Cladistics
Holgado, B., and R. V. Pêgas. 2020. A taxonomic and phylogenetic review
of the anhanguerid pterosaur group Coloborhynchinae and the
new clade Tropeognathinae. Acta Palaeontologica Polonica
Holgado, B., R. V. Pêgas, J. I. Canudo, J. Fortuny, T. Rodrigues, J.
Company, and A. W. A. Kellner. 2019. On a new crested pterodac-
tyloid from the Early Cretaceous of the Iberian Penisula and the
radiation of the clade Anhangueria. Scientic Reports 9:110.
Hone, D. W., Naish, D. and Cuthill, I. C. 2012. Does mutual sexual selec-
tion explain the evolution of head crests in pterosaurs and dino-
saurs? Lethaia 45(2):139156.
Kaup, J. J. 1834. Versuch einer Eintheilung der Saugethiere in 6 Stämme
und der Amphibien in 6 Ordnungen. Isis 3:311315.
Kellner, A. W. A. 1984. Ocorrência de uma mandíbula de Pterosauria
(Brasileodactylus araripensis, nov. gen.; nov. sp.) na Formação
Santana, Cretáceo da Chapada do Araripe, Ceará Brasil. Anais
do Congresso Brasileiro de Geologia, 33:578590.
Kellner, A. W. A. 1990. Os répteis voadores do Cretáceo brasileiro.
Anuário do Instituto de Geociências 12:86106.
Kellner, A. W. A. 1996. Description of new material of Tapejaridae and
Anhangueridae (Pterosauria, Pterodactyloidea) and discussion of
pterosaur phylogeny. Ph.D. dissertation, Columbia University,
New York, 347 pp.
Kellner, A. W. A. 2003. Pterosaur phylogeny and comments on the evol-
utionary history of the group; pp: 217:105137 in E. Buffetaut; J. M.
Mazin (eds.). Evolution and Paleobiology of Pterosaurs. Geological
Society, London, Special Publications.
Kellner, A. W. A., and Y. Tomida. 2000. Description of a new species of
Anhangueridae (Pterodactyloidea) with comments on the ptero-
saur fauna from the Santana Formation (Aptian-Albian), northeast-
ern Brazil. National Science Museum Monographs 17:1135
Klingenberg, C. P. 2011. MorphoJ: an integrated sohtware package for
geometric morphometrics. Molecular Ecology Resources 11:353
Longrich, N. R., D. M. Martill, and B. Andres. 2018. Late Maastrichtian
pterosaurs from North Africa and mass extinction of Pterosauria
at the Cretaceous-Paleogene boundary. Plos Biology 16: e2001663
Lü, J.; D. M. Unwin, D. C. Deeming, X. Jin, Y. Liu, and Q. Ji. 2011.An
egg-adult association, gender, and reproduction in pterosaurs.
Science 331:3211324.
Manzig, P. C., A. W. A. Kellner, L. C. Weinschütz, C. E. Fragoso, C. S.
Vega, G. B. Guimarães, L. C. Godoy, A. Liccardo, J. H. C. Ricetti,
Duque et al. Ontogenetic growth of Anhanguera premaxillary crest (e2116984-9)
and C. C. Moura. 2014. Discovery of a rare pterosaur bone bed in a
Cretaceous Desert with insights on ontogeny and behavior of ying
reptiles. Plos One 9(8): e100005.
May, P., P. Reser, and P. Leiggi. 1994. Macrovertebrates preparation; pp.
113128 in P. Leiggi; P. May. (eds) Vertebrates Paleontological
Techniques, volume I. Cambridge University Press.
Neumann, V. H., and L. Cabrera. 1999. Uma nueva propuesta
estratigráca para la tectonocuencia post-rifte de la Cuenca de
Araripe, nordeste de Brasil. In: Simpósio sobre o Cretáceo do
Brasil, 5. 1963, Rio Claro, Boletim. Rio Claro: UNESP. 279285.
Pêgas, R. V., B. Holgado, and M. E. C. Leal. 2019.OnTargaryendraco wie-
denrothi gen. nov. (Pterodactyloidea, Pteranodontoidea,
Lanceodontia) and recognition of a new cosmopolitan lineage of
Cretaceous toothed pterodactyloids. Historical Biology 33:12661280.
Pinheiro, F. L., and T. Rodrigues. 2017.Anhanguera taxonomy revisited:
is our understanding of Santana Group pterosaur diversity biased
by poor biological and stratigraphic control? PeerJ 5.3285:129.
Plieninger, F. 1901. Beiträge zur Kenntnis der Flugsaurier.
Palaeontographica 48:6590.
Rodrigues, T., and A. W. A. Kellner. 2013. Taxonomic review of the
Ornithocheirus complex (Pterosauria) from the Cretaceous of
England. ZooKeys 308:1112
Rohlf, F. J. 2010. TpsDig, version 216. Departamento of Ecology and
Evolution, State University of New York at Stony Brook.
Available at
Santos, O. S. 1985. Técnicas de Preparação de Fósseis; pp. 26:101127 in
D. A., Campos; R. C. G., Armestro, (eds.), Série Geológica, Seção
Paleontologia e Estratigraa.
Unwin, D. M. 2001. An overview of the pterosaur assemblage from the
Cambridge Greensand (Cretaceous) of Eastern England.
Mitteilungen aus dem Museum für Naturkunde in Berlin,
Geowissenschaliche Reihe 4:189221.
Unwin, D. M. 2005. The Pterosaurs: from deep time. New Yorkm, Pi
Press, 246 pp.
Veldmeijer, A. J. 2003. Preliminary description of a skull and wing of a
Brazilian Cretaceous (Santana Formation; Aptian-Albian) ptero-
saur (Pterodactyloidea) in the collection of the AMNH. PalArchs
Journal of Vertebrate Palaeontology 0:114.
Veldmeijer, A. J., H. J. Meijer, and M. Signore. 2006.Coloborhynchus
from the Lower Cretaceous Santana Formation, Brazil
(Pterosauria, Pterodactyloidea, Anhangueridae); an update.
PalArchs Journal of Vertebrate Palaeontology, 3:1529.
Veldmeijer, A. J., H. J. Meijer, and M. Signore. 2009. Description of
Pterosaurian (Pterodactyloidea: Anhangueridae,
Brasileodactylus) remains from the Lower Cretaceous of Brazil.
Deinsea 13:940.
Viana, M. S. S., and V. H. L. Neumann. 2002. Membro Crato da Formação
Santana, Chapada do Araripe, CE: Riquíssimo registro de fauna e
ora do Cretáceo; pp. 113120 in Schobbenhaus, C., Campos, D.
A., Queiroz, E. T., Winge, M., and Berbert-Born, M. (orgs.). Sítios
Geológicos e Paleontológicos do Brasil, Brasília, DNPM/CPRM/
Vila Nova, B. C., J. M. Sayão, V. H. M. L. Neumann, and Kellner, A.W.A.
2014. Redescription of Cearadactylus atrox (Pterosauria,
Pterodactyloidea) from the Early Cretaceous Romualdo
Formation (Santana Group) of the Araripe Basin, Brazil. Journal
of Vertebrate Paleontology 34:126134.
Wang, X., A. W. A. Kellner, S. Juang, Q. Wang, Y. Ma, Y. Paidoula, X.
Cheng, T. Rodrigues, X. Meng, J. Zhang, N. Li, and Z. Zhou.
2014. Sexually dimorphic tridimensionally preserves pterosaurs
and their eggs from China. Current Biology 24:13231330.
Wang, X., A. W. A. Kellner, X. Cheng, S. Jiang, Q. Wang, J. M. Sayão, T.
Rodrigues, F. Costa, N. Li, X. Meng and Z. Zhou. 2015. Eggshell and
histology provide insight on the life history of a pterosaur with two
functional ovaries. Anais da Academis Brasileira de Ciências 87:
Wellnhofer, P. 1987. New crested pterosaurs from the Lower Cretaceous
of Brazil. Mitteilungen der Bayerischen Staatssammlung für
Paläontologie und Historische Geologie 27: 175186.
Wellnhofer, P. 1991. Weitere Pterosaurierfunde aus der Santana-
Formation (Apt) der Chapada do Araripe, Brasilien.
Palaeontographica A 215:43101.
Zhou, X., Pêgas, R. V., Ma, W., Han, G., Jin, X., Leal, M. E., Bonde, N.,
Kobayashi, Y., Lautenschlager, S., Wei, X., Shen, C. and Ji, S.. 2021.
A new darwinopteran reveals arborealism and an opposed thumb.
Current Biology 31(11): 24292436.
Submitted October 19, 2021; revisions received January 3, 2022;
accepted August 18, 2022.
Handling Editor: Elizabeth Martin-Silverstone.
Duque et al. Ontogenetic growth of Anhanguera premaxillary crest (e2116984-10)
... Other recent cranial material designated Anhanguera sp. includes the anterior portion of a rostrum (DGEO-CTG-UFPE 8283; Duque et al., 2022) lacking premaxillary crest. Referral of DGEO-CTG-UFPE 8283 to the genus Anhanguera is supported by the 5th and 6th pairs alveoli being smaller than the 4th and 7th (Duque et al., 2022). ...
... includes the anterior portion of a rostrum (DGEO-CTG-UFPE 8283; Duque et al., 2022) lacking premaxillary crest. Referral of DGEO-CTG-UFPE 8283 to the genus Anhanguera is supported by the 5th and 6th pairs alveoli being smaller than the 4th and 7th (Duque et al., 2022). ...
The Gondwanan pterosaur record is scarce when compared with that of Laurasia and is reviewed here. The majority of Gondwanan pterosaur remains are derived from South America; however, the relative richness of the South American record compared with other Gondwanan continents is largely a result of the ‘Lagerstätten’ effect. Nevertheless, the South American pterosaur assemblage represents the most speciose and diverse known from Gondwana, with several lineages represented, including the Raeticodactylidae, Rhamphorhynchoidea, Darwinoptera, Ctenochasmatidae, Gnathosaurinae, Nyctosauridae, Ornithocheiridae, Tapejaridae, Thalassodromidae, Dsungaripteridae, Chaoyangopteridae and Azhdarchidae. Gondwanan pterosauromorphs are known only from South America. From Africa rhamphorhynchids, archaeopterodactyloids, pteranodontians, nyctosaurids, ornithocheirids, tapejarids, dsungaripteroids, chaoyangopterids, and azhdarchids have been reported. The Arabian Peninsula has produced nyctosaurids, an istiodactyliform, ornithocheirids and azhdarchids. Non-pterodactyloid pterosaurs have been reported from India. A possible azhdarchid has been reported from Madagascar and rhamphorhynchids are known from isolated teeth. The Antarctic pterosaur assemblage also comprises isolated remains of indeterminate pterodactyloids, and a possible indeterminate rhamphorhynchoid. The pterosaur record from East Gondwana comprises ornithocheirids, azhdarchids and a possible ctenochasmatoid from Australia, as well as azhdarchids from New Zealand. Although our understanding of Gondwanan pterosaurs has greatly improved within the last three decades, the discovery and description of more specimens, particularly from Antarctica and East Gondwana, will enhance our understanding of pterosaurian biodiversity and palaeobiogeography.
Full-text available
The Tapejaridae were an apparently worldwide distributed clade of edentulous pterosaurs, being a major component of several Lower Cretaceous terrestrial faunas. Despite their distribution across Gondwana and Laurasia, the oldest tapejarid remains were found in Barremian units from Europe, what led to the assumption that the clade originated in Eurasia and later dispersed southwards. Here we present a new tapejarid pterosaur species (Kariridraco dianae gen. et sp. nov.) from the Lower Cretaceous Romualdo Formation of Brazil. The holotype (MPSC R 1056) comprises an incomplete, three dimensionally preserved skull, lower jaw, and cervical vertebrae. It shows a unique combination of features such as unusually tall and comparatively short nasoantorbital fenestrae, as well as a premaxillary crest forming an angle of about 45° with respect to main skull axis. Phylogenetic analyses recover the new taxon as a Tupuxuara-related Thalassodrominae, a clade of early-diverging tapejarids that were apparently indigenous to central Gondwana. The inclusion of the new taxon in current phylogenetic frameworks, in addition to similarity cluster analyses of Early Cretaceous tapejarid-bearing pterosaur faunas, indicate Gondwana as the most parsimonious origin center for Tapejaridae, and show that pterosaur communities were affected by large scale tectonic-driven vicariant events.
Full-text available
Pterosaurs, which lived during the Mesozoic, were the first known vertebrates to evolve powered flight.¹,² Arboreal locomotion has been proposed for some taxa,³,⁴ and even considered to have played a role in the origin of pterosaur flight.⁵,⁶ Even so, there is still need for comprehensive quantitative ecomorphological analyses.³,⁴ Furthermore, skeletal adaptations correlated to specialized lifestyles are often difficult to recognize and interpret in fossils. Here we report on a new darwinopteran pterosaur that inhabited a unique forest ecosystem from the Jurassic of China. The new species exhibits the oldest record of palmar (or true) opposition of the pollex, which is unprecedented for pterosaurs and represents a sophisticated adaptation related to arboreal locomotion. Principal-coordinate analyses suggest an arboreal lifestyle for the new species but not for other closely related species from the same locality, implying a possible case of ecological niche partitioning. The discovery adds to the known array of pterosaur adaptations and the history of arborealism in vertebrates. It also adds to the impressive early bloom of arboreal communities in the Jurassic of China, shedding light on the history of forest environments.
Full-text available
Anhanguerids are a particular group of pterodactyloid pterosaurs, characterized mainly by their rostral sagittal crests, well laterally expanded jaw tips and enlarged anterior teeth. Due to the fragmentary nature of most known specimens, including holotypes, the taxonomy of the group has proved particularly difficult and controversial. Coloborhynchinae is a recently proposed clade within the Anhangueridae, and was defined as the most inclusive clade containing Coloborhynchus clavirostris but not Anhanguera or Ludodactylus. Coloborhynchinae was originally thought to include Coloborhynchus, Uktenadactylus, and Siroccopteryx. Here we present a reassessment of the taxonomy and phylogeny of all proposed members of the Coloborhynchinae and Coloborhynchus complex, with new anatomical comparisons and a novel phylogenetic analysis. Several features allow us to establish that coloborhynchines were much more diverse than previously thought, englobing four genera and seven species: Aerodraco sedgwickii gen. et comb. nov., Coloborhynchus clavirostris, Nicorhynchus capito gen. et comb. nov., Nicorhynchus fluviferox gen. et comb. nov., Uktenadactylus rodriguesae sp. nov., and Uktenadactylus wadleighi. Nicorhynchus and Uktenadactylus are considered sister taxa, being distinct on the basis of several rostral characters. Although with a homoplastic flat rostrum surface, Siroccopteryx was recovered out of the Coloborhynchinae, as sister taxon of Tropeognathus, due to similarities on the palatal ridge (which is broad and deep, and starting at the same level) and the relatively stout teeth compared to other anhanguerids. Tropeognathus and Siroccopteryx are further related to the Australian taxa Ferrodraco and Mythunga, which are all grouped in a new clade: the Tropeognathinae. Our analysis suggests that morphological evolution within anhanguerids was quite more complex than previously thought, with coloborhynchines representing the oldest recorded lineage of Anhangueridae, which achieved a worldwide distribution at least from the Aptian to the Cenomanian.
Full-text available
Ornithocheirus wiedenrothi, from the Hauterivian (Early Cretaceous of Germany), is a taxon represented by three-dimensional remains of the lower jaw and wing elements. Its phylogenetic affinities have for long been elusive, though several works had already pointed out that it probably did not belong within the wastebasket genus Ornithocheirus. In the present contribution, we redescribe this species, assigning it to the new genus Targaryendraco and offering updated morphological comparisons. Subsequently, we present a phylogenetic analysis in which we recover a clade formed by Targaryendraco, Aussiedraco, Barbosania, Aetodactylus, Camposipterus and Cimoliopterus. This newly recognised clade is interesting in being quite cosmopolitan and spanning from the Hauterivian to the Cenomanian, like its sister-group, the Anhangueria. The recognition of this clade helps fill the temporal gap between the Anhangueria and Cimoliopterus, and also demonstrates that the diversity of Cretaceous toothed pterosaurs was higher than previously thought.
Full-text available
The pterosaur record from the Iberian Peninsula is mostly scarce and undefined, but in the last few years some new taxa have been described from different Lower Cretaceous sites of Spain. Here we describe a new genus and species of toothed pterodactyloid pterosaur from the Barremian of the Iberian Peninsula, Iberodactylus andreui gen. et sp. nov., that shows a close and rather unexpected relationship with Hamipterus tianshanensis from China. A review of the phylogenetic relationships of the Anhangueria reveals a new family of pterodactyloid pterosaurs, the Hamipteridae fam. nov. being recovered as sister-group of the Anhangueridae. This latter clade can be in turn divided into the new clades Anhanguerinae and Coloborhynchinae. The close relationships of Iberodactylus and Hamipterus shows an interesting palaeobiogeographical correlation between the Chinese and Iberian pterosaur faunas during the Barremian (Lower Cretaceous). The discovery of Iberodactylus strongly suggests that the clade Anhangueria has clear ancestral ties in eastern Laurasia.
Full-text available
Here are new and old inventory of fossiliferous sites in the Romualdo Formation, Albian of the Araripe Basin, in the municipality of Exu, Pernambuco, Northeast of Brazil, with the survey of its fossiliferous diversity, with emphasis on paleovertebrates. Seven localities were studied, and 16 taxa of paleovertebrates were identified, including fishes: Vinctifer comptoni, Rhacolepis buccalis, Calamopleurus cylindricus, Cladocyclus gardneri, Neoproscinetes penalvai, Paraelops cearenses, Tharrhias araripis, Notelops brama, Araripelepdotes temnurus, Brannerion sp. e Beurlenichthys ouricuriensis; new occurrences of pterosaurs Anhangueridae and; chelonians (Araripemys barretoi). The Romualdo Formation has been studied since 1800 and it is internationally recognized as Fossillagerstätte. However, the Pernambuco region of the Araripe Basin lacks systematic studies when compared to the region of Ceará, which indicates the need to register the occurrence of fossiliferous sites and diversity, contributing to the knowledge of vertebrate paleontology in the southwest portion of the Araripe Basin and expanding the paleontological collections of the state of Pernambuco.
Full-text available
Pterosaurs were the first vertebrates to evolve powered flight and the largest animals to ever take wing. The pterosaurs persisted for over 150 million years before disappearing at the end of the Cretaceous, but the patterns of and processes driving their extinction remain unclear. Only a single family, Azhdarchidae, is definitively known from the late Maastrichtian, suggesting a gradual decline in diversity in the Late Cretaceous, with the Cretaceous–Paleogene (K-Pg) extinction eliminating a few late-surviving species. However, this apparent pattern may simply reflect poor sampling of fossils. Here, we describe a diverse pterosaur assemblage from the late Maastrichtian of Morocco that includes not only Azhdarchidae but the youngest known Pteranodontidae and Nyctosauridae. With 3 families and at least 7 species present, the assemblage represents the most diverse known Late Cretaceous pterosaur assemblage and dramatically increases the diversity of Maastrichtian pterosaurs. At least 3 families—Pteranodontidae, Nyctosauridae, and Azhdarchidae—persisted into the late Maastrichtian. Late Maastrichtian pterosaurs show increased niche occupation relative to earlier, Santonian-Campanian faunas and successfully outcompeted birds at large sizes. These patterns suggest an abrupt mass extinction of pterosaurs at the K-Pg boundary.
Full-text available
Background Anhanguerids comprise an important clade of pterosaurs, mostly known from dozens of three-dimensionally preserved specimens recovered from the Lower Cretaceous Romualdo Formation (northeastern Brazil). They are remarkably diverse in this sedimentary unit, with eight named species, six of them belonging to the genus Anhanguera. However, such diversity is likely overestimated, as these species have been historically diagnosed based on subtle differences, mainly based on the shape and position of the cranial crest. In spite of that, recently discovered pterosaur taxa represented by large numbers of individuals, including juveniles and adults, as well as presumed males and females, have crests of sizes and shapes that are either ontogenetically variable or sexually dimorphic. Methods We describe in detail the skull of one of the most complete specimens referred to Anhanguera, AMNH 22555, and use it as a case study to review the diversity of anhanguerids from the Romualdo Formation. In order to accomplish that, a geometric morphometric analysis was performed to assess size-dependent characters with respect to the premaxillary crest in the 12 most complete skulls bearing crests that are referred in, or related to, this clade, almost all of them analyzed first hand. Results Geometric morphometric regression of shape on centroid size was highly statistically significant (p = 0.0091) and showed that allometry accounts for 25.7% of total shape variation between skulls of different centroid sizes. Premaxillary crests are both taller and anteroposteriorly longer in larger skulls, a feature consistent with ontogenetic growth. A new diagnosis is proposed for Anhanguera, including traits that are nowadays known to be widespread within the genus, as well as ontogenetic changes. AMNH 22555 cannot be referred to “Anhanguera santanae” and, in fact, “Anhanguera santanae”, “Anhanguera araripensis”, and “Anhanguera robustus” are here considered nomina dubia. Discussion Historically, minor differences in crest morphology have been used in the definition of new anhanguerid species. Nowadays, this practice resulted in a considerable difficulty in referring well-preserved skulls into known taxa. When several specimens are analyzed, morphologies previously believed to be disparate are, in fact, separated by a continuum, and are thus better explained as individual or temporal variations. Stratigraphically controlled excavations on the Romualdo Formation have showed evidence for faunal turnover regarding fish communities. It is thus possible that some of the pterosaurs from this unit were not coeval, and might even represent anagenetic morphotypes. Unfortunately, amateur collecting of Romualdo Formation fossils, aimed especially at commerce, resulted in the lack of stratigraphic data of virtually all its pterosaurs and precludes testing of these further hypotheses.
Full-text available
The Cambridge Greensand, a remanié deposit that crops out in Cambridgeshire, eastern England, has yielded numerous, though fragmentary, late Early Cretaceous (Albian) vertebrate fossils including more than 2000 isolated pterosaur bones. So far, 32 species of pterosaur have been proposed in connection with the Cambridge Greensand material, but there has been and continues to be considerable confusion concerning the validity of these taxa, their relationships to each other and to other pterosaurs, and the material upon which they were established. A comprehensive systematic revision identified eleven valid species distributed among three families: the Ornithocheiridae (Ornithocheirus simus and possibly a second, as yet unnamed species of Ornithocheirus, Coloborhynchus capito, Coloborhynchus sedgwickii, Anhanguera cuvieri, and Anhanguera fittoni); the Lonchodectidae (Lonchodectes compressirostris, Lonchodectes machaerorhynchus, Lonchodectes microdon and Lonchodectes platystomus); and a species of edentulous pterosaur (Ornithostoma sedgwicki) that may represent the earliest record for the Pteranodontidae. It is possible that some of the taxa currently recognised represent sexual dimorphs (Coloborhynchus capito and Coloborhynchus sedgwickii, Lonchodectes compressirostris and Lonchodectes machaerorhynchus), or disjunct populations of a single species (Ornithocheirus simus and Ornithocheirus sp., Lonchodectes compressirostris and Lonchodectes microdon) and that there may be as few as seven valid species, but the Cambridge Greensand pterosaurs are too poorly known to demonstrate this at present. The Cambridge Greensand pterosaur assemblage is similar to a slightly younger, but much smaller assemblage from the Lower Chalk of England and shares some elements, such as ornithocheirids, in common with many other late Early and early Late Cretaceous assemblages. It is distinguished by the absence of tapejarids and the presence of Lonchodectes which, so far, is only known from the Cretaceous of England. The disparity in taxonomic composition is possibly related to ecological differentiation, and might also reflect some provincialism in late Early and early Late Cretaceous pterosaur faunas. Der Cambridge Greensand, eine in Ostengland aufgeschlossene Remanié-Ablagerung, hat zahlreiche Wirbeltiere aus der oberen Unterkreide (Alb) geliefert. Darunter fanden sich mehr als 2000 isolierte Pterosaurierknochen. Insgesamt wurden aus dem Greensand bis zu 32 Flugsauriertaxa beschrieben, was zu einer beträchtlichen taxonomischen und nomenklatorischen Verwirrung geführt hat, die bis heute andauert. Eine vollständige Revision erkennt 11 Arten aus drei Familien an: (1) die Ornithocheiridae (Ornithocheirus simus und vielleicht eine zweite, bislang unbenannte Art von Ornithocheirus, sowie Coloborhynchus capito, Coloborhynchus sedgwickii, Anhanguera cuvieri und Anhanguera fittoni); (2) die Lonchodectidae (Lonchodectes compressirostris, Lonchodectes machaerorhynchus, Lonchodectes microdon und Lonchodectes platystomus); und schließlich einen zahnlosen Flugsaurier (Ornithostoma sedgwicki). der zu keiner der vorgenannten Familien gehört und sich als stratigraphisch ältester Nachweis der Pteranodontidae erweisen könnte. Es ist nicht auszuschließen, dass einige der gegenwärtig erkannten Taxa eher einen ausgeprägten Sexualdimorphismus illustrieren denn taxonomisch distinkte Arten darstellen (Coloborhynchus capito und Coloborhynchus sedgwickii, Lonchodectes compressirostris und Lonchodectes machaerorhynchus) oder sogar lediglich Endpunkte einer intraspezifisch variablen Population (Ornithocheirus simus und Ornithocheirus sp., Lonchodectes compressirostris und Lonchodectes microdon). In dieser strengeren Fassung bestünden nur sieben gültige Arten, doch leider sind die Flugsaurier des Cambridge Greensand zu schlecht bekannt, um diese Fragen zu beantworten. Die Flugsaurierfauna des Cambridge Greensand ähnelt jüngeren kreidezeitlichen Faunen aus dem Lower Chalk von England. Weiter-hin enthält sie Faunenelemente, wie etwa Ornithocheiriden. die auch für zahlreiche andere Faunen der hohen Unterkreide und tiefen Oberkreide charakteristisch sind. Das Fehlen von Tapejariden und das Auftreten des anscheinend endemischen Lonchodectes sind weitere Kennzeichen des Cambridge Greensand. Die Zusammensetzung der Pterosaurierfaunen folgte offenbar ökologischen Differenzierungen und illustriert einen gewissen Provinzialismus an der Grenze Unter-Oberkreide. doi:10.1002/mmng.20010040112
A new juvenile specimen of Pteranodon from the Smoky Hill Chalk Member of the Niobrara Formation of western Kansas had an estimated wingspan in life of 1.76 m, ~45% smaller than the smallest previously known specimens, but does not differ in morphology from larger specimens. Its presence indicates that juveniles were capable of flying long distances, so it falsifies the interpretation of Pteranodon as growing rapidly to adult size under parental care before flying. Instead juveniles were precocial, growing more slowly to adult size while flying and feeding independently for several years before going to sea. Because juveniles are otherwise unknown in the Smoky Hill Chalk Member, they must have occupied different environments and ecological niches than adults; thus Pteranodon exhibited ontogenetic niches. Evidence is presented that most other pterosaurs (e.g., Rhamphorhynchus , Pterodactylus , Anhanguera ) also exhibited various ontogenetic niches, which, along with their large body size, suggests that pterosaur taxonomic diversity was rather low, like that of crocodilians.