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An Acad Bras Cienc (2021) 93(Suppl. 2): e20201568 DOI 10.1590/0001-3765202120201568
Anais da Academia Brasileira de Ciências | Annals of the Brazilian Academy of Sciences
Printed ISSN 0001-3765 I Online ISSN 1678-2690
www.scielo.br/aabc | www.fb.com/aabcjournal
An Acad Bras Cienc (2021) 93(Suppl. 2)
Running title: Pterosaur taxonomy
and diversity
Academy Section:
PALEONTOLOGY
e20201568
93
(Suppl. 2)
93(Suppl. 2)
DOI
10.1590/0001-3765202120201568
PALEONTOLOGY
A taxonomic approach on diagnostic
characters used to defi ne new pterosaur taxa
and an estimation of pterosaur diversity
DENIS LUIZ FERNANDES, IVAN NUNES & FABIANA R. COSTA
Abstract: Diagnostic characters from 227 pterosaur species were listed, separated
into cranial or post-cranial elements and counted. From 21 post-cranial and 23 cranial
elements, most diagnostic characters were related to phalanges (15%) and rostrum.
Post-cranial characters comprise 44.23%, and cranial characters 55.77% of all characters
used in pterosaur diagnoses. The highest correlation between diagnostic features
occurs between the coracoid and the scapula. 25.11% and 28.63% of sampled taxa were
diagnosed with 3-4 and 5-6 characters, respectively. The mean number of 6.79 characters
was found in specimens with both cranial and post-cranial elements, and 4.86 and 4.17 in
those with just cranial or post-cranial elements, respectively. 31 from 227 species (13.7%)
were erected based on single elements, which are most frequently complete or partial
mandibles (n=18). We estimate that 23.4% of the total pterosaur genera are currently
known, with 90% of this diversity to be unveiled up to 2145. As the requirements of broad
and cautious revision of genus/group must be undertaken, and some deposits will
provide mostly fragmented and incomplete material, the assignment of fairly incomplete
specimens to the most inclusive taxonomic level is feasible. Tracing this scenario can
guide future works on the description of new pterosaur taxa.
Key words: Morphology-based species, Pterosauria, Systematic Biology, Taxonomy
INTRODUCTION
Delineating species and their taxonomy has
been traditionally a matter of recognizing
morphological characters (Schwentner et al.
2011) as structural attributes of organisms that
are primarily recognized as different from any
other. For centuries, Morphology has been the
primary or sole source of data for delimiting
species (Cook et al. 2010). Under the requirement
of a species being unique and identifiable
following a specifi c code, each name has to be
linked to a type specimen, and this identifi cation
is associated to a species concept (Cook et al.
2010). That of Mayr’s (1996) defining species
as “a morphological kind that is different
from other such kinds” particularly restricts
data to morphological characters (Cook et al.
2010). Despite data defi ning morphology-based
species have been currently complemented by
other data source such as DNA sequence data,
which has fomented plenty of debate on the
suffi ciency of morphological data alone to defi ne
species (e.g., Ebach & Carvalho 2005a, b, Packer
et al. 2009), this cannot be applied to some
areas that usually can count solely on structure
(Morphology), such as the case of Paleontology.
Indeed, recognition of paleontological species
relies almost exclusively on their morphological
differences, which is hampered by the often
fragmentary and isolated nature of fossils
(Forey et al. 2004). This explains the differences
DENIS LUIZ FERNANDES, IVAN NUNES & FABIANA R. COSTA PTEROSAUR TAXONOMY AND DIVERSITY
An Acad Bras Cienc (2021) 93(Suppl. 2) e20201568 2 | 20
between the nature of elements that are used
to define new taxa, ranging from cranial to post-
cranial elements or both, and from complete to
fairly incomplete material.
When it comes to pterosaurs the
number of characters raised as diagnostic
to define a new species varies from one
(e.g., Azhdarcho lancicollis Nessov, 1984,
Bennettazhia oregonensis (Gilmore, 1928),
Domeykodactylus ceciliae Martill, Frey, Diaz &
Bell, 2000, Gnathosaurus subulatus Meyer, 1833,
“Huaxiapterus” corollatus Lü, Jin, Unwin, Zhao,
Azuma & Ji, 2006, Nyctosaurus lamegoi Price,
1953, Rhamphorhynchus etchesi O’Sullivan
& Martill, 2015 and Tupuxuara longicristatus
Kellner & Campos, 1988) to up to 29 features
(Eudimorphodon ranzii Zambelli, 1973), which
could be related to the completeness degree
of material (the more complete the specimen,
the higher number of osteological features
to be eventually pointed as diagnostic).
When it comes to the type of characters (i.e.,
autapomorphic or synapomorphic), there is
also a noticeable variation in this number
of diagnostic features that could be assigned
to methodological bias whether in complete
specimens or not. For instance, Mythunga
camara Molnar & Thulborn, 2007 is an Early
Cretaceous pterodactyloid pterosaur described
based on 10 original features of an incomplete
snout and mandible, but only two of them were
identified as autapomorphic. On the other hand,
the abovementioned and much more complete
Chinese tapejarid “Huaxiapterus” corollatus, a
partial skeleton and skull, is defined by a single
supposed autapomorphy (a distinctive hatched-
shaped process on the cranial crest). There are
also taxa (e.g., species of the genus Anhanguera
Campos & Kellner, 1985, Pinheiro & Rodrigues
2017) largely diagnosed by subtle differences
in cranial anatomy based particularly on the
morphology and position of structures as crests,
which may presumably be sexual dimorphisms
or ontogenetic variations (Bennett 1992, Manzig
et al. 2014). However, neither dimorphic or
ontogenetic aspects, nor the type of characters
termed as diagnostic are here considered, and
such discussion is beyond the scope of this paper.
The systematic biology, as it is known,
is based on the description of an organism
that supports taxonomic recognition, and the
diagnosis of new or revised taxa has long been
considered part of systematic accounts (Cifelli
& Kielan-Jaworowska 2005). The International
Code of Zoological Nomenclature (ICZN)
provides definitions and a set of rules on how
to name newly described organisms, assuring
the stability of the zoological nomenclature.
However, it does not set a norm on the amount
(from 1-29 features in pterosaurs) or nature of the
diagnostic characters used to define new taxa,
which is widely variable among researchers and
depends on the nature of studied organisms.
The character-based species, as defined
by Nixon & Wheeler (1990) as “the smallest
aggregation of populations (sexual) or lineages
(asexual) diagnosable by a unique combination
of character states in comparable individuals
(semaphoronts)”, has the number of diagnostic
traits to be considered to define a species as
one of its major practical difficulties (Willmann
& Meier 2000). Thus, as a matter of debate and
also to try to delineate a pattern regarding the
most used structures for diagnosing pterosaur
species, we have delineated three main aims
to this study: to determine (1) the nature of
elements from which the osteological characters
that diagnose new species are defined, (2) the
average number of characters used to diagnose
pterosaur species, and (3) to make a projection
concerning the rate of future pterosaur
discoveries to predict these discoveries as to
guide future works on the description of new
pterosaur species.
DENIS LUIZ FERNANDES, IVAN NUNES & FABIANA R. COSTA PTEROSAUR TAXONOMY AND DIVERSITY
An Acad Bras Cienc (2021) 93(Suppl. 2) e20201568 3 | 20
Institutional abbreviations
IVPP - Institute of Vertebrate Paleontology and
Paleoanthropology, Beijing, China; MN - Museu
Nacional, Rio de Janeiro, Brazil; NHMUK - The
Natural History Museum, London, UK; PIMUZ
- Paläontologisches Institut und Museum,
Universität Zürich, Switzerland; UJA - University
of Jordan, Amman, Jordan.
MATERIALS AND METHODS
Data on diagnostic characters from all
taxonomically diagnosable pterosaur species
ever described up to August 2020 (n = 227) were
compiled from The Paleobiology Database
(PaleoDB: www.paleobiodb.org) and published
literature. Diagnostic characters are here
interpreted as differential character states (i.e.,
uniquely shared by all members of a taxon
but not by non-members) or a unique and
differential combination of characters used to
define a taxon. The former is here termed as
autapomorphic (as a unique apomorphy to a
taxon or a group of organisms), as discriminated
by Dubois (2017). Here we refrain from differing
the type of characters in the sense of separating
autapomorphic from synapomorphic ones (i.e.,
whether unique from a single taxon or shared
with other taxa). All of them are termed as
diagnostic and considered according to their
nature (cranial or post-cranial).
The final dataset comprises (for each
listed species) nature of preserved skeletal
material (cranial, post-cranial or both), the
number of characters used to diagnose each
pterosaur species, completeness degree (i.e.,
complete or partial skeletons, and which parts
are preserved in incomplete material), year of
description, period, locality and country (see the
supplementary DataSet by Fernandes et al. 2021
at doi:10.17632/w7thrrs9dh.1).
As to provide the most updated compilation
of diagnosable pterosaur species so far, we
have checked along for synonyms and nomina
dubia (not considered). Despite the fact that
other pterosaur species compilations have
been provided previously (e.g., Andres 2010,
Butler et al. 2013, Dean et al. 2016), our purpose
differs by focusing on the number and nature
of characters used in the original diagnoses
of pterosaur species, as well as predicting the
rate of future pterosaur discoveries. It is worth
mentioning that once we have considered the
elements that have historically been used as
original diagnostic features, we disregarded
whether the characters are currently valid or
not. Neither aspects of pterosaur diversity nor
the quality of fossil record has been evaluated
or discussed herein.
Once fossil species are mainly diagnosed
on the basis of osteological characters, cranial
and post-cranial elements used to define these
characters in each species were determined.
These elements were then individually counted
regarding the number of times they were used
when diagnosing species that comprised only
cranial and both cranial and post-cranial
material (cranial elements), and only post-
cranial and both cranial and post-cranial
material (post-cranial elements). Osteological
elements were only considered once per
diagnosis (e.g., if a taxon was diagnosed using
two distinct phalangeal features, it was counted
as “phalangeal elements” - 1). Moreover, when
these elements were combined with others to
term a single diagnostic character, they were
counted separately (e.g., if a taxon was diagnosed
by the hypothetical diagnostic character “wing
metacarpal shorter than ulna and first wing
phalanx, with a pronounced posterior curvature”,
it was counted as “phalangeal elements” - 1,
“metacarpal elements”- 1, and “ulnar elements”
- 1). Subsequently the frequency (%) of these
DENIS LUIZ FERNANDES, IVAN NUNES & FABIANA R. COSTA PTEROSAUR TAXONOMY AND DIVERSITY
An Acad Bras Cienc (2021) 93(Suppl. 2) e20201568 4 | 20
(cranial and post-cranial) elements related to
diagnostic characters was determined in order
to indicate which elements would have been
most used in the diagnosis of new species.
Mean, median and mode were calculated
from the number of characters used to diagnose
each pterosaur species. The frequency (%) of
the amount of characters (ranging from the
min-max values of 2 - 31) that diagnosed new
pterosaur species was calculated, as well as
the frequency of each cranial and post-cranial
element used to diagnose these species.
A Principal Component Analysis (PCA)
was applied to analyze similarity patterns of
characters frequency between diagnoses due
to the very large dataset (Jollife & Cadima 2016).
PCA is an orthogonal linear transformation of
the data for a new coordinate system, reducing
the dimensionality of such datasets, increasing
interpretability and minimizing information
loss (Jolliffe 2002). In this analysis, the greatest
variance for any projection of data is along the
first coordinate (Principal Component 1 - PC1)
and the second greatest variance is along the
second coordinate (Principal Component 2 -
PC2), and so on, being the number of principal
components less than or equal to the number of
original variables (Jolliffe 2002). The Hierarchical
Cluster Analysis was performed as a complement
with the linkage criterion of UPGMA (unweighted
pair group method with arithmetic mean) and
applying a correlation similarity index to find out
which any given pair of characters join together
in the tree diagram (Sokal 1958, Krebs 1999,
Nielsen 2016). The goal is to build a tree diagram
where the characters that were more used in the
same diagnosis are placed on branches that are
close together.
To estimate pterosaur diversity and to
make a projection concerning the rate of future
pterosaur discoveries, the number of specimens
assigned to each genus was taken from the
PaleoDB (Alroy 2013) downloaded on August
16th, 2019. From this date up to August 2020 new
genera were sourced from the literature. Here
we applied the Abundance-based Coverage
Estimator (ACE) (Chao & Lee 1992, Chao & Yang
1993) as a statistical method to consider the
incompleteness of the fossil record (following
Wang & Dodson 2006). The ACE model estimates
the number of discoverable genera also
comprising future discoveries, and only takes
into account genera considered scarce (i.e.,
those with ten or less individuals assigned to
a genus), which avoid inaccuracies (e.g., those
motivated by difficulties in estimating the exact
number of material available for abundant
genera, such as Pteranodon, with more than
a thousand individuals known so far (Bennett
2000)). The diversity was estimated with the
following equation:
Estimated Diversity =Dabun +
D
rare
Crare +
f
1
Crare γ2
rare
Where
γ2
rare =max[max(Drare i(i–1)fi
Crare(ifi)2–1,0)(1+ 1–Crare i(i–1)fi
Crare ifi–1),0]
and
Crare =1–f1
nrare
1
Dabun is the number of abundant genera (n>10),
Drare is the number of rare genera (n<10), nrare is
the number of individuals among rare genera,
and fi is the number of individuals known from
exactly i individuals. All calculations were made
using the LibreOffice® Calc software and Past4.3
was used to generate the dendrogram.
It is worth mentioning that specimens not
assigned to a specific genus (e.g., IVPP V 17959,
a wukongopterid; Cheng et al. 2016) were not
considered in the estimation using the ACE
model, neither ichnotaxa nor species without
a valid diagnosis. Here we have accounted for
the “discoverable” and “assignable” pterosaur
genera with current technology and taxonomic
DENIS LUIZ FERNANDES, IVAN NUNES & FABIANA R. COSTA PTEROSAUR TAXONOMY AND DIVERSITY
An Acad Bras Cienc (2021) 93(Suppl. 2) e20201568 5 | 20
methods, and thus provided a lower estimate
of the ever existed diversity (Wang & Dodson
2006) since the original diversity cannot be
recovered.
Other data related to each species, such as
year of the species’ description and the number
of assigned specimens to a species, were also
used to predict future pterosaur discoveries and
to produce statistics for estimating pterosaur
diversity, respectively. The prediction of
future discoveries was performed by fitting a
logistic accumulation curve of the form y=807/
(1+806*e^(-0, 0.026026*t)) to the cumulative
counts of known genera throughout the years
using the estimation of pterosaur diversity as the
point where the curve becomes an asymptote.
RESULTS AND DISCUSSION
Which osteological elements are the most
employed to diagnose new pterosaur species?
From 21 post-cranial elements, most diagnostic
characters were related to phalanges (15%),
followed by humeri (13%) and vertebrae (12.25%)
(Figure 1), and from 23 cranial elements the most
used cranial-related characters regard those of
the rostrum, as follows: teeth (16.20%), mandible
(12.93%) and premaxilla (10.44%) (Figure 2). Post-
cranial characters comprise 44.49%, and cranial
characters 55.51% of all characters used in
pterosaur diagnoses. If species with both cranial
and post-cranial elements are considered, teeth
(9.99%) account for the majority of characters,
followed by mandible (7.64%), phalanges (6.61%)
and humeri (5.43%) (Figure 3).
In PCA analysis, it was found that the first
two components (PC1 and PC2) correspond to
32.28% of all variance. and the other two (PC3
and PC4) to 6.50% and 5.34%, respectively.
The scatterplot of PC1-PC4 scores are shown
in Figure 4 but, as explained before, the
representation of the variance is low in PC3
and PC4. Thus, we have limited our approach
to the first two components. The reduced space
of the first two components (Figure 5) show
that PC1 has a positive correlation especially
with the frequency of cranial elements, while
PC2 mostly has positive correlation with the
Figure 1. Frequency of post-cranial elements diagnosing new pterosaur taxa.
DENIS LUIZ FERNANDES, IVAN NUNES & FABIANA R. COSTA PTEROSAUR TAXONOMY AND DIVERSITY
An Acad Bras Cienc (2021) 93(Suppl. 2) e20201568 6 | 20
frequency of post-cranial elements. The scatter
plot groups in the negative side of both axes the
features that have low frequency in diagnosis
and that are mostly used to diagnose the
most complete specimens with both cranial
and post-cranial elements. Factor loadings are
presented in Figure 6. When considering the
axes alone, it can be seen that taxa diagnosed
with only cranial elements are influencing PC1,
with Austriadactylus cristatus Dalla Vecchia,
Wild, Hopf & Reitner, 2002, Istiodactylus
sinensis Andres & Qiang, 2006, Maaradactylus
spielbergi Veldmeijer, 2003, Haopterus gracilis
Wang & Lü, 2001, and Cearadactylus atrox
Leonardi & Borgomanero, 1985, respectively,
with major descendant contribution. PC2
is being influenced by taxa with only post-
cranial elements, with Ningchengopterus liuae
Lü, 2009, Changchengopterus pani Lü, 2009,
Vesperopterylus lamadongensis Lü, Meng,
Wang, Liu, Shen & Zhang, 2017, Orientognathus
chaoyngensis Lü, Pu, Xu, Wei, Chang & Kundrát,
2015, and Carniadactylus rosenfeldi Dalla Vecchia,
1995, respectively, with major descendant
contribution. Taxa diagnosed with both cranial
and post-cranial elements influence both axes,
depending on how many characters used in the
diagnosis are cranial or post-cranial (Figure 6).
The Hierarchical Cluster Analysis shows a
dendrogram in which osteological elements
are frequently used together to erect new taxa,
which is organized in eight main clusters (Figure
7). Most clusters group features that are often
found together due to being anatomically near
to each other, but it is not always the case
because of the low frequency of some of the
features (e.g., a cluster grouping the ischium
with the occipital bone). The highest correlation
between diagnostic features occurs between the
coracoid and the scapula. Other features often
used together for diagnostic purposes include
both nasoantorbital and orbital fenestrae; fibula
and tarsus; and femur and tibia. Features that
do not often occur with other specific features
are pteroid, lacrimal, and dentary.
How many characters on average are used to
diagnose pterosaur taxa?
Mode and median were 5.0, with mean of 5.6.
There was also a strong negative correlation
between the number of diagnostic features
and the percentage of taxa (-0.77), which
Figure 2. Frequency of cranial elements diagnosing new pterosaur taxa.
DENIS LUIZ FERNANDES, IVAN NUNES & FABIANA R. COSTA PTEROSAUR TAXONOMY AND DIVERSITY
An Acad Bras Cienc (2021) 93(Suppl. 2) e20201568 7 | 20
means that less taxa are diagnosed with more
characters. 25.11% and 28.63% of pterosaur taxa
were diagnosed with 3-4 and 5-6 characters
(Figure 8). Despite this pattern, some taxa are
outstandingly out of the normal curve as quite
complete specimens being diagnosed within the
range of 13-29 characters (e.g., Eudimorphodon
ranzii and Vesperopterylus lamadongensis Lu,
Meng, Wang, Liu, Shen & Zhang, 2017, with 31 and
15 cranial and post-cranial diagnostic characters,
respectively).
There is a quite obvious tendency of having
more diagnostic characters in more complete
specimens, which is numerically substantiated
by a mean of 6.79 characters in specimens with
both cranial and post-cranial elements, and
4.86 and 4.17 in those with just cranial or post-
cranial elements, respectively. Notwithstanding,
there are fairly complete specimens with a
sole diagnostic feature, such as the case of
“Huaxiapterus” corollatus diagnosed by a
hatchet-shaped process on the cranial crest, as
well as “Huaxiapterus” atavismus Lü, Teng, Sun,
Shen, Li, Gao & Liu, 2016 and “Huaxiapterus”
benxiensis Lü, Gao, Xing, Li & Sun, 2007, with only
two diagnostic elements (Lü et al. 2006, 2007,
2016). Caviramus shesaplanensis Frösbisch &
Frösbisch, 2006 (PIMUZ A/III 1225), on the other
hand, consists of an incomplete mandible and
is diagnosed by 10 characters, such as the case
of Cretornis hlavaci Fric, 1881 (an incomplete left
wing) with 14 diagnostic features (Averianov &
Ekrt 2015).
What are the problems in taxonomy of fossil
taxa anyway?
Theoretical and practical problems concerning
the erection of higher taxa are currently
being addressed and hamper the efficiency
and transparency of the taxonomical work
(Komarek & Beutel 2006). If taxonomy of
extant taxa can benefit from molecular studies
Figure 3. Frequency of cranial and post-cranial
elements diagnosing new pterosaur taxa.
DENIS LUIZ FERNANDES, IVAN NUNES & FABIANA R. COSTA PTEROSAUR TAXONOMY AND DIVERSITY
An Acad Bras Cienc (2021) 93(Suppl. 2) e20201568 8 | 20
Figure 4. The six possible PCA scatter plot combinations for PC1 to PC4 of post-cranial (circle) and cranial (triangle)
osteological features.
Figure 5. PCA scatter plot (PC1 and PC2) of the diagnostic signal of post-cranial (circle) and cranial (triangle)
osteological features.
DENIS LUIZ FERNANDES, IVAN NUNES & FABIANA R. COSTA PTEROSAUR TAXONOMY AND DIVERSITY
An Acad Bras Cienc (2021) 93(Suppl. 2) e20201568 9 | 20
using conservative and fast evolving genes for
phylogenetic reconstructions on both high and
lower levels, respectively (Komarek & Beutel
2006), extinct taxa can basically count, as
already mentioned, solely on morphology itself.
This increases the concern about making (good)
choices of suitable characters as a crucial
stage of appropriate taxonomic work (Komarek
& Beutel 2006). Thus, if we mainly deal with
combination of morphological characters to
advocate species recognition (not considering
here the discussion on chronospecies and
stratospecies, which is beyond the scope of this
paper), our selection of characters relies on how
deep is our taxonomic approach. This directs
towards an easily detectable issue as we are
dealing with species recognition based solely
on morphological differences of specimens that
are usually fragmentary and highly incomplete:
the level of taxonomic identification depends on
which parts of the morphology is preserved, and
how complete they are. It is obviously different
to describe individual parts as separate species
or a fairly complete skeleton, and depending
on the amount of parts we have (i.e., a single
element, a bunch of cranial or/and post-cranial
elements), we can turn to even fine details on
the morphological investigation of perceptible
differences (i.e., deepen the taxonomic level of
investigation).
However, how deep we go on this task
is constantly a matter of debate, with some
advocating against (and even strongly refusing
to) the erection of new taxa based on single
elements (specially fragmentary ones) as it
could bring excessive noise to phylogenetic
analysis (e.g., less resolved consensus trees
and increased numbers of EMPTs; Huelsenbeck
1991, Wiens and Reeder 1995, Wiens 2003), or
even create systematic problems to be further
solved on late reassessments of these taxa
when insufficient study of types or taxa have
created synonyms. This can happen when the
authors do not consider reviewing all species
of a group under consideration, which creates
an insufficient background to substantiate the
introduction of a new species, tending to produce
synonyms (Komarek & Beutel 2006). The lack of
Figure 6. PCA factor loadings (PC1 and PC2) of taxa described with only post-cranial (circle), cranial (triangle) and
both cranial and post-cranial (cross) osteological features.
DENIS LUIZ FERNANDES, IVAN NUNES & FABIANA R. COSTA PTEROSAUR TAXONOMY AND DIVERSITY
An Acad Bras Cienc (2021) 93(Suppl. 2) e20201568 10 | 20
this critical approach to erect new taxa without
sufficient comparison with other species and/
or an extensive review may lead to inadequate
taxonomic results. A recent example is the case
of Thalassodromeus oberlii (Headden & Campos
2014), formerly “Banguela” oberlii described as a
new species of dsungaripterid pterosaur based
on an incomplete mandible from the Romualdo
Formation (Santana Group, northeastern Brazil)
(Pêgas et al. 2018). This synonymization has been
proposed as none of the four autapomorphies
erected for “Baguela” oberlii could distinguish it
from Thalassodromeus sethi Kellner & Campos,
2002, and the recognition of a second species
of Thalassodromeus Kellner & Campos, 2002
would in turn reflect the speciose nature of
some pterosaur taxa from this formation (Pêgas
et al. 2018). Nonetheless, if requirements of a
broad revision of genus/group are properly
undertaken, we can walk the path to assign
these fairly incomplete specimens to the most
inclusive taxonomic level.
Another abovementioned topic that can
be debated is that the correct identification of
fragmented fossils has proven to be difficult,
and because of this reaching a more inclusive
taxonomic level to erect a new species can raise
doubts on the validity of this species. The severity
of this issue is directly proportional to the degree
of fragmentation displayed by specimens. A
single piece of element demands a deepened
analysis on its morphological features that can
be potentially diagnostic. This varies depending
on the nature of this element (e.g., a plain bone
diaphysis or a piece of vertebra). The holotype
of the monotypic species Araripedactylus dehmi
Wellnhofer, 1977, for instance, consists of a
single first phalanx embedded in a limestone
concretion that was originally allocated into
the Pterodactyloidea, and lately considered to
belong to the Ornothocheiroidea (sensu Kellner)
based on its provenance by Kellner & Tomida
(2000), who was not able to confirm none of
its autapomorphies (even though seven were
erected).
Indeed, few features can be taken from
pterosaur phalanges themselves, particularly if
their extremities are lacking/damaged (such as
the case of A. dehmi). Notwithstanding, the case
of other elements such as mandible is fairly
different, but it depends on the completeness
Figure 7. Dendrogram showing the co-occurrence of
diagnostic features.
DENIS LUIZ FERNANDES, IVAN NUNES & FABIANA R. COSTA PTEROSAUR TAXONOMY AND DIVERSITY
An Acad Bras Cienc (2021) 93(Suppl. 2) e20201568 11 | 20
level of the specimen that is being described. If we
take as an example the ventral shape (concave)
of the mandibular symphysis that diagnoses
the only element of the dsungaripteroid
Tendaguripterus recki Unwin & Heinrich, 1999,
which is the best known taxon from the Upper
Jurassic Tendaguru Beds of Tanzania (Kellner et
al. 2007), a mapping on the diagnostic characters
of all the analyzed species in this study shows
that the shape of dorsal/ventral margins
of the mandibular symphysis can be found
also diagnosing Argentinadraco barrealensis
Kellner & Calvo, 2017 (mandibular symphysis
with marked concave ventral margin in lateral
view), Aussiedraco molnari Kellner, Rodrigues
& Costa, 2011 (dorsal margin of mandibular
symphysis markedly convex, ventral margin
of the symphysis straight), Aymberedactylus
cearensis Pêgas, Leal & Kellner, 2016 (dorsally
concave mandibular symphysis throughout
entire extent) and Caupedactylus ybaka Kellner,
2013 (posterior half of the ventral margin of the
mandibular symphysis forming a slight convex
surface). It is interesting to notice that all of the
listed taxa, apart from C. ybaka, are only known
from a (complete or partially complete) lower
jaw, such as the case of T. recki. Thus, this level
of analysis regarding the shape of a specific
portion of the lower jaw, or any specific bone
structure from other bones, are more likely to
be identified when the taxonomist can rely on
(very) fragmented specimens. This seems to be
quite obvious since we are “forced” to perceive
the details of more incomplete material to try
to reach the more inclusive taxonomic level as
possible.
Another well-known problem concerning
the erection of new species regards the limited
sample size of fossils, which was recently
addressed by Massare & Lomax (2018) for
Ichthyosaurus. Aquatic reptiles, as pterosaurs,
bear unique morphological characters and
did not have living representatives or suitable
analogs. The authors have evaluated if different
hindfin morphology in Ichthyosaurus was of
taxonomic utility in the sense of erecting new
species, and argued that the sample size has
“implications for identifying unique diagnostic
characters (autapomorphies) based on limited
fossil material”. In the case of Ichthyosaurus,
Figure 8. Frequency of characters used to diagnosis new pterosaur taxa.
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if just fewer specimens would have been
available, variation in hindfin morphology could
have appeared less variable and more distinct.
This shows that the more reduced sample size,
the less variation will be recognized, which
hampers morphotypes identification (Massare
& Lomax 2018). As morphotypes are defined
as different types of individuals that belong
to the same species (morph), recognition of
morphotypes relies upon many quite complete
specimens of a species, otherwise intermediate
morphologies could not be identified. Thus,
unique morphologies can only be stated as such
if numerous specimens can more confidently
show that these are indeed taxonomically
distinct characters and not a grade form within
the variation. Massare & Lomax (2018) also call
the attention for the case of isolated elements
that seem to bear these particular morphologies.
As these elements seem to be slightly different
from other known species, and in the lack of
more elements that could provide a better
comparison to these same elements in different
species, they are usually erected as new species.
Regarding pterosaurs, most species are
erected based on one or few specimens and, as
usual for fossil material, relies primarily upon
morphology (although anatomical information
is frequently missing). A worth mentioning case
is the Pteranodon-complex, which comprises
the best known pterosaurs so far and was a
subject of investigation by many researchers
concerning the identification of different
species. This much-debated complex has been
lately addressed by Kellner (2010) who re-
evaluated the genus Pteranodon and erected
two new species (Geosternbergia maiseyi
Kellner, 2010 and Dawndraco kanzai Kellner,
2010). The author also discussed other problems
besides the reduced number of specimens to
define new species, such as the incompleteness
of fossil material, taphonomy and the absence
of modern representatives or suitable analogs.
However, as abovementioned, the major issue
to be considered for taxonomy in fossils is
morphology, but as form and structure can
vary depending on ontogeny, gender, individual
differences and taphonomy (Kellner 2010), the
lack of a considerable number of specimens
hampers the recognition of variation as a result
of one of these factors or taxonomically distinct
characters. In the case of the Pteranodon-
complex, although different ontogenetic stages
have already been recognized by Bennett (1993)
for Pteranodon, a total of 14 species have been
described, 11 of which referred to Pteranodon
but considered as inflated by some reviewers
(Kellner 2010). Thus, fossil taxonomy can
possibly be failing to reflect the real diversity
and consequently biasing our view over the
paleobiology of extinct taxa.
But what would be the impact in pterosaur
systematics if fairly fragmented fossils are
erected as new taxa?
As morphological information is essential to
taxonomic studies but is constantly incomplete in
fossils, which are subjected to many taphonomic
and diagenetic processes (Lautenschlager
2016), some pterosaur taxonomists refrain
from erecting new taxa from single pieces of
bone elements. However, 31 from 227 species
(13.7%) are erected based on single elements:
1-5 characters are used to diagnose 24 species,
6-9 to 6 species and up to 10 characters to 1
species. From the nature of these elements, they
are mostly complete or partial mandibles (n=18),
and others consist of maxillae (n=4), cervical
vertebrae and snout fragments (n=3 for both),
humeri (n=1), premaxillae (n=1) and phalanx
(n=1). The taxonomic validity of Arambourgiana
philadelphiae Arambourg, 1954 (holotype UJA
VF-1, cervical V lacking its posterior end), one of
these species, has been questioned by Witton
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et al. (2010) who have proposed to synonymize
it with Hatzegopteryx thambema Vremir, 2010.
Indeed the misinterpretation over the mid-
cervical vertebra of Arambourgiana Nessov
& Jarkov, 1989 (originally described as a wing
metacarpal by Arambourg (1954, 1959)) may have
been induced by the difficulties in identifying
a single 620 mm cylindrical cervical vertebra
at the time azhdarchids were not known (and
consequently neither giant pterosaurs that
could have bear such elongated necks) and the
lack of fully developed vertebral processes that
could give an easier clue about its nature. Thus,
it is understandable that a piece of bone with a
circular cross-section could be attributed to a
limb bone diaphysis instead of being considered
an axial element.
As already mentioned, A. dehmi consists of a
single first phalanx and was originally allocated
into the Pterodactyloidea (and lately considered
as an ornothocheiroid sensu Kellner). The
extreme thickness of this phalanx pointed out by
the original description of Wellnhofer (1977) (not
lately confirmed by Kellner & Tomida (2000)),
together with the damaged condition of its distal
end, would have imposed difficulties in the
identification of a plain piece of bone in the late
70’s. Also, Bogolubovia orientallis (Bogolubov
1914) described in the early XX century, was
originally assigned to the genus “Ornithostoma”
Seeley, 1871 and belonging to pteranodontids
before having its own genus erected (Nesov &
Yarkov 1989). The specimen, which consisted of
a fragment of the posterior portion of a cervical
vertebra, was lately regarded as a nomen
dubium by Bakhurina and Unwin (1995), who
have questioned the possibility of identification
of its type material. This potential taxonomical
invalidity was then refuted by Averianov et al.
(2005) based on the species being considerably
different from other known cervical vertebrae
of azhdarchids in which concerns the position
of the spinal canal, the low condyle and well
developed postexapophyses (Averianov et al.
2005).
Taxonomic discordances have also
comprised Brasileodactylus Kellner, 1984
(holotype MN 4804-V, proximal part of a mandible)
firstly assigned to the Ornothocheiridae by
Kellner (1984) before being more contentiously
allocated in the Pterodactyloidea incertae
sedis (Kellner 1991), then to have affinities
to the Anhangueridae (Kellner & Tomida,
2000) and even considered to be a species of
Coloborhynchus Owen, 1874 (Frey et al. 2003).
However, a dentary sagittal groove bearing
small sub-grooves and the extremely elongated
mandibular symphysis when compared with
that of Anhanguera, Criorhynchus Owen, 1974
and Coloborhynchus seem to be apomorphic
features of Brasileodactylus (Veldmeijer et al.
2005). The anterior portion of the rostrum (partial
mandible) of the holotype (NHMUK PV 39409) of
Cimoliopterus cuvieri (Bowerbank, 1851), formerly
Pterodactylus cuvieri, was lately reassigned to
the genus Ornithocheirus and Coloborhynchus
until Rodrigues & Kellner (2013) have placed it in
a new monotypic genus. Also, Coloborhynchus
clavirostris Owen, 1874 (holotype NHMUK PV
R 1822), a fragment of premaxilla and maxilla,
has been synonimized with Ornithocheirus
simus [=Criorhynchus simus] by Hooley (1914),
Kuhn (1967) and Wellnhofer (1978) until being
revalidated by Lee (1994) whose position was
corroborated by Unwin (2001) and Rodrigues &
Kellner (2013). On the contrary, Lonchodectes
compressirostris (formerly attributed to
the genera Pterodactylus Cuvier, 1809 and
Ornithocheirus), a partial maxilla also referred
by Hooley (1914) who re-introducted the genus
Lonchodectes Hooley, 1914 and considered
Lonchodectes compressirostris (Owen, 1851)
one of the nine Lonchodectes species, was
considered a valid species by Unwin (2001) and
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lately a nomen dubium by Rodrigues & Kellner
(2013). Uktenadactylus wadleighi (Lee, 1994),
former Coloborhynchus wadleighi, consists of
a partial snout that was reassigned to a new
genus in 2009 by Kellner & Rodrigues, who had
restricted the genus Coloborhynchus to the single
species C. clavirostris. Another Lonchodectes
species, Lonchodectes sagittirostris (Owen,
1874), consisting of a pair of lower jaws (formerly
allocated to the Ornithocheirus genus), was also
considered a nomen dubium by Rodrigues and
Kellner (2013) and then reassigned to the genus
Serradraco by Rigal et al. (2017). Indeed, the
exceedingly fragmentary nature of the Cambridge
Greensand pterosaurs made their systematic a
constantly disputed taxonomic question over
a decade until Rodrigues and Kellner (2013)
have extensively reviewed the Ornithocheirus
complex and discussed many ornithocheirids in
the light of the revised taxonomy.
Even Siroccopteryx moroccensis Mader &
Kellner, 1999, only known from the front portion
of the mandible, had its genus considered as
a junior synonym of Coloborhynchus by Unwin
(2001) by the resemblance of this genus to a
specimen of Coloborhynchus described by Lee
(1994) and closely related to Anhanguera by
Fastnatch (2001). Rodrigues & Kellner (2009)
have then considered Siroccopteryx a distinct
genus.
As abovementioned, 13.7% of all pterosaur
species were erected based on single elements.
According to Massare & Lomax (2018), isolated or
fragmentary elements lack plentiful information
to justify the erection of new taxon, and in the
absence of several specimens it is not possible
to properly identify whether what appear to be
unique morphologies are indeed taxonomically
distinct characters or intermediate forms within
the variation. Therefore, it is not possible to
know if the erection of these species is justified,
especially in the lack of a more deepened and
detailed taxonomic study, until other studies
challenge these nominations by critically
re-examining these species. This frequently
poses a major problem concerning the discard
of previously accepted taxonomic names by
synonymization or the proposal of nomina
dubia. This current procedure makes an effort
to minimize taxonomic inflation (i.e., inflation
of species names) when individual parts being
described as separate species are shown to be
problematic. As above exemplified, this is also a
major concern when it comes to pterosaurs, with
several species being constantly challenged.
Another problem of increasing species-level
taxa based on limited fossils is the increased
diversity bias. Taxonomic inflation is more
critical when taxa have a fragmentary and sparse
fossil record (Uhen & Pyenson 2007). However, it
is noteworthy that sometimes the description of
new taxa based solely on complete specimens
may also bias diversity, but differently from
what is expected when dealing with incomplete
specimens (Donovan 2001). Thus, if diversity
bias can occur even when complete specimens
are described, this cannot be an argument to
prevent limited specimens to be erected as new
taxa.
Notwithstanding, although numerous
problems are related to naming species based
on incomplete and fragmentary material, many
type specimens are incomplete but diagnostic
in vertebrate paleontology (Uhen & Pyenson
2007). We thus refrain from advocating against
this practice despite these potential problems,
but suggest being particularly cautious when
species-level taxa are erected based on
limited and/or isolated material. In the case
of pterosaurs, as already mentioned, potential
taxonomic problems could be avoided if
diagnostic features are mapped with cautious by
a broad and deep taxonomic study also based
on as many comparisons with other material
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as possible. Along with that, current research
practices can help, such as reproducing high-
resolution photographs in descriptive research
articles and publishing informative figures,
which enables better anatomical comparisons
to be done.
How many pterosaur genera are still unknown?
One of the major substantial challenges in
Paleontology is to quantify the diversity of
animal groups (Alroy et al. 2001), and despite
some punctual efforts on quantifying some of
these groups (e.g., the diversity of dinosaurs;
Dodson 1990, Russell 1995, Wang & Dodson
2006), studies of this kind are still scarce.
The well-known incompleteness of the fossil
record, as well as taxonomic difficulties, indeed
hampers the diversity estimation of fossil groups
(Wang & Dodson 2006). Research on particularly
estimating the pterosaur diversity also follows
this pattern, with few studies having been
performed so far (e.g., Butler et al. 2009, 2012,
2013).
There are 189 valid pterosaur genera up to
now. Although a deep analysis on pterosaur
diversity using different approaches is beyond
the scope of this paper, we have estimated it
by using the ACE model to reach a result for the
generic pterosaur diversity of 807, which means
that 23.4% of the pterosaur genera are currently
known. Because of the small sample sizes from
the Late Triassic to the Mid Jurassic, estimation
for these periods are very unreliable (Table I).
These data allowed us to predict the rate of
future pterosaur discoveries by fitting a logistic
accumulation curve to the cumulative counts of
known genera throughout the years using the
estimation of pterosaur diversity as the point
where the curve becomes an asymptote. This
curve indicates that near 2060 about half of the
pterosaur diversity will be known, and predicts
that 90% of this diversity will have been unveiled
up to 2145 (Figure 9).
From 2000 to 2019, 116 genera were described,
which means that in those two decades on
average 6.11 new genera are described per year.
The prediction that 90% of the generic richness
will be known in 2145 requires 5.5 new genera to
be described per year, or that in a bit more than
a century, 540 new genera need to be described.
The number of 807 genera is especially
low for the entire Mesozoic when compared to
the current diversity of flying vertebrates, and
to the diversity of land vertebrates of the time.
Neornithes, a group that includes all living birds,
is presently the most diverse clade of present-
day vertebrates that is widespread to roughly
all ecological niches (Gill 2007), and bats (order
Chiroptera) account for ~ 20% of mammal diversity,
which make these modern flying vertebrates one
of the largest monophyletic mammalian clades
(Lei & Dong 2016). It is estimated that 88% of
bats that ever existed did not enter the fossil
record (Eiting & Gunnell 2009), and the similarity
of Character Completeness Metric (CCM) records
for pterosaurs, extinct chiropterans and birds
are probably due to similar taphonomic bias
related to their resembling ecologies (Dean et
al. 2016, Brocklehurst et al. 2012, Brown et al.
2019). Thus, a low percentage of the pterosaurs
that ever existed is also expected.
CONCLUSIONS
The level of taxonomic identification relies on
which parts of the morphology are preserved,
and how complete they are. Analyzed data
showed that 31 from 227 pterosaur species
(13.7%) are erected based on single elements
that are mostly complete or partial mandibles
(n=18). Selection of characters relies on how deep
is our taxonomic approach as we mainly deal
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with combination of morphological characters
to advocate species recognition, but the lack
of a critical approach to erect new taxa without
sufficient comparison with other species and/
or an extensive review may lead to inadequate
taxonomic results. The fragmentary nature of
some fossils can also raise doubts on the validity
of the erected species and could be avoided
by a more deepened and detailed taxonomic
study. Finally the limited sample size of fossils
hampers the recognition of morphotypes and
thus intermediate morphologies could not be
identified. Despite all these problems, we refrain
from advocating against the erection of new
taxa based on limited and/or isolated material,
but suggest being particularly cautious when
species-level taxa are erected. Moreover, since
some deposits will provide mostly fragmented
Figure 9. Rate of future pterosaur discoveries using a logistic accumulation curve of the form y=807/(1+806*e^(-0,
0.026026*t)). The dotted line represents the estimated curve, and the solid line corresponds to the known growth.
Table I. Generic diversity (richness) estimated for each Mesozoic periods and the entire Mesozoic. Since some
genera are found in the interface of two epochs, the sum of the richness of these subperiods do not add up to the
richness of the entire Mesozoic.
Period Known diversity Estimated diversity Percentage known
Entire Mesosoic 189 807 23.4%
Late Triassic 13 25 52.0%
Early Jurassic 5 6 89.3%
Mid Jurassic 15 35 42.5%
Late Jurassic 38 141 27.0%
Early Cretaceous 82 396 20.7%
Late Cretaceous 43 196 22.0%
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and incomplete fossil material (as many type
specimens are incomplete but diagnostic
in vertebrate paleontology), as far as the
requirements of a broad and cautious revision
of genus/group are properly undertaken, the
assignment of these fairly incomplete specimens
to the most inclusive taxonomic level is feasible.
We still have much more than half of the
estimated pterosaur genera to discover (more
specifically, 77.9% is yet to be discovered), which
justify the continuous effort of unveiling this
diversity by describing new taxa, even though if
we account for single, very fragmented material
(together with deepening the taxonomic level of
investigation). As this statistical survey regarding
the nature and number of the osteological
structures that use to define new pterosaur
taxa has never been made before, tracing this
scenario has the potential to guide future works
on the description of new pterosaur taxa.
Acknowledgments
FRC want to thank Conselho Nacional de
Desenvolvimento Científico e Tecnológico (CNPq, grant
number 421772/2018-2) for financial support.
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How to cite
FERNANDES DL, NUNES I & COSTA FR. 2021. A taxonomic approach
on diagnostic characters used to define new pterosaur taxa and an
estimation of pterosaur diversity. An Acad Bras Cienc 93: e20201568. DOI
10.1590/0001-3765202120201568.
Manuscript received on October 5, 2020;
accepted for publication on March 23, 2021
DENIS LUIZ FERNANDES1
https://orcid.org/0000-0003-3285-3588
IVAN NUNES2
https://orcid.org/0000-0001-7985-2836
FABIANA R. COSTA3
https://orcid.org/0000-0003-3596-0143
1Universidade de São Paulo, Instituto de Biociências, Rua
do Matão, Tv. 14, Butantã, 05508-090 São Paulo, SP, Brazil
2São Paulo State University Júlio de Mesquita Filho,
Laboratory of Herpetology, Institute of Biosciences,
Campus do Litoral Paulista, Praça Infante D. Henrique,
s/n, Parque Bitaru, 11330-900 São Vicente, SP, Brazil
3Federal University of ABC, Laboratory of Vertebrate
Paleontology and Animal Behavior (LAPC), Center of
Natural and Human Sciences, Campus São Bernardo
do Campo, Rua São Paulo, s/n, Jardim Antares,
09606-070 São Bernardo do Campo, SP, Brazil
Correspondence to: Fabiana Rodrigues Costa
E-mail: fabiana.costa@ufabc.edu.br
Author contributions
FRC and IN conceived and designed the study; DLF collected
all data; FRC, DLF and IN wrote the paper. All authors have
discussed and reviewed the manuscript.