Está en la página 1de 14

Journal of Vertebrate Paleontology

ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/ujvp20

Brazilian Permian Dvinosaurs (Amphibia,


Temnospondyli): Revised Description and
Phylogeny

Claudia Marsicano, Kenneth D. Angielczyk, Juan C. Cisneros, Martha Richter,


Christian F. Kammerer, Jörg Fröbisch & Roger M. H. Smith

To cite this article: Claudia Marsicano, Kenneth D. Angielczyk, Juan C. Cisneros, Martha
Richter, Christian F. Kammerer, Jörg Fröbisch & Roger M. H. Smith (2021): Brazilian Permian
Dvinosaurs (Amphibia, Temnospondyli): Revised Description and Phylogeny, Journal of Vertebrate
Paleontology, DOI: 10.1080/02724634.2021.1893181

To link to this article: https://doi.org/10.1080/02724634.2021.1893181

View supplementary material

Published online: 06 May 2021.

Submit your article to this journal

Article views: 132

View related articles

View Crossmark data

Full Terms & Conditions of access and use can be found at


https://www.tandfonline.com/action/journalInformation?journalCode=ujvp20
Journal of Vertebrate Paleontology e1893181 (13 pages)
© by the Society of Vertebrate Paleontology
DOI: 10.1080/02724634.2021.1893181

ARTICLE

BRAZILIAN PERMIAN DVINOSAURS (AMPHIBIA, TEMNOSPONDYLI): REVISED


DESCRIPTION AND PHYLOGENY

CLAUDIA MARSICANO, *,1,2 KENNETH D. ANGIELCZYK,3 JUAN C. CISNEROS, 4 MARTHA RICHTER, 5


CHRISTIAN F. KAMMERER, 6 JÖRG FRÖBISCH,7,8 and ROGER M. H. SMITH 9,10
1
Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Departamento de Ciencias Geológicas, C1428EHA Ciudad
Autónoma de Buenos Aires, Argentina, claumar@gl.fcen.uba.ar;
2
CONICET-UBA (Consejo Nacional de Investigaciones Científicas y Técnicas-Universidad de Buenos Aires), Instituto de Estudios
Andinos (IDEAN);
3
Negaunee Integrative Research Center, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, Illinois 60605,
U.S.A., kangielczyk@fieldmuseum.org;
4
Museu de Arqueologia e Paleontologia, Universidade Federal do Piauí, 64049-550, Teresina, PI, Brazil, juan.cisneros@ufpi.edu.br;
5
Earth Sciences Department, Natural History Museum, Cromwell Road, London SW7 5BD, U.K., m.richter@nhm.ac.uk;
6
North Carolina Museum of Natural Sciences, Raleigh, North Carolina, U.S.A., christian.kammerer@naturalsciences.org;
7
Museum für Naturkunde, Leibniz−Institut für Evolutions- und Biodiversitätsforschung, Invalidenstr. 43, D−10115 Berlin, Germany,
joerg.froebisch@mfn.berlin;
8
Institut für Biologie, Humboldt-Universität zu Berlin, Invalidenstr. 42, D−10115 Berlin, Germany;
9
Evolutionary Studies Institute, University of the Witwatersrand, Private Bag 3, Wits 2050, Johannesburg, South Africa,
Roger.Smith4@wits.ac.za;
10
Iziko South African Museum, P.O. Box 61, Cape Town 8000, South Africa, rsmith@iziko.org.za

ABSTRACT—Recently collected temnospondyl fossils from the Cisuralian Pedra de Fogo Formation (north-eastern Brazil)
indicate a diverse assemblage of aquatic tetrapods, including the dvinosaurs Timonya anneae and Procuhy nazariensis. Here
we present revised diagnoses for these species and detailed descriptions of their holotypes. Timonya anneae is distinguished
from all other dvinosaurs by several cranial characters including: combined width of both parietals less than interorbital
width; presence of a groove-like internal carotid artery foramen; and presence of an ossified opisthotic. In the mandible,
T. anneae presents two parasymphyseal fossae on each side of the mandibular symphysis to accommodate palatal fangs
and a well-developed postglenoid area. Procuhy nazariensis, mostly preserved as a mold of the skull table and mandible,
is diagnosed by the presence of the anteriormost extension of the squamosal posterior to parietal midlength; pineal
foramen posterior to the midlength of the parietal; supratemporal exposed on the posterior border of the skull table; and
presence of postglenoid process of the surangular separated from the retroarticular process of the articular by the
mandibular sulcus. A new inclusive phylogeny of Temnospondyli indicates that Dvinosauria consists of the
Trimerorhachidae (including Procuhy as the sister-taxon of Trimerorhachis) and the ‘short-snouted’ dvinosaurs, with
Timonya as an early-diverging representative of the latter clade. The Pedra de Fogo dvinosaurs show close relationships
with Cisuralian taxa from the North American southwest, reinforcing close paleogeographic connections between these
regions in the late Paleozoic, but represent endemic taxa, corroborating the pattern suggested by the plant fossil record.

SUPPLEMENTAL DATA—Supplemental materials are available for this article for free at www.tandfonline.com/UJVP

Citation for this article: Marsicano, C., K. D. Angielczyk, J. C. Cisneros, M. Richter, C. F. Kammerer, J. Fröbisch, and R. M. H.
Smith. 2021. Brazilian Permian dvinosaurs (Amphibia, Temnospondyli): revised description and phylogeny. Journal of
Vertebrate Paleontology. DOI: 10.1080/02724634.2021.1893181

INTRODUCTION 2015; Schoch, 2018). Most recent phylogenetic analyses of Tem-


nospondyli place Dvinosauria on the stem of the Stereospondylo-
Dvinosauria (Yates and Warren, 2000) is an extinct clade of
morpha (sensu Yates and Warren, 2000), a clade that includes
mostly small-bodied temnospondyls that were fully adapted to
most of the derived temnospondyls from the Permo–Triassic
an aquatic lifestyle. Members of the clade are characterized by
(e.g., Yates and Warren, 2000; Ruta and Bolt, 2006; Schoch,
well-defined sensory sulci on the adult skull roof, extensive and
2013; although see Pardo et al. [2017] for an alternative topology).
well-ossified gill skeletons, and elongated bodies (28 or more pre-
Dvinosauria was originally named for the genus Dvinosaurus
sacral vertebrae) when they are completely preserved, as in
from the Lopingian (late Permian) of Russia (Bystrow, 1938;
Dvinosaurus and Trimerorhachis (e.g., Bystrow, 1938; Warren,
Shishkin, 1973), but most knowledge of the clade comes from
1999; Yates and Warren, 2000; Witzmann, 2013; Cisneros et al.,
taxa recorded in the Carboniferous and Cisuralian (early
Permian) of North America (Case, 1935; Chase, 1965; Berman,
1973; Sequeira, 1998; Milner and Sequeira, 2011; Englehorn
et al., 2008). Several of these taxa, such as Isodectes,
* Corresponding author Erpetosaurus, Neldasaurus and particularly Trimerorhachis, are
Color versions of one or more of the figures in the article can be found represented by multiple specimens (Sequeira, 1998; Milner and
online at www.tandfonline.com/ujvp.

Published online 06 May 2021


Marsicano et al.—Brazilian Permian dvinosaurs (e1893181-2)

Sequeira, 2011; Milner and Schoch, 2013; Schoch, 2018), with system. The system uses a 10–225 kV microfocus X-ray source
Trimerorhachis being known from especially abundant material and an amorphous silicon flat panel detector with a pixel size of
(Milner and Schoch, 2013). The Laurasian record of the 200 microns by 200 microns and a resolution of 2,048 by 2,048
group extends into the Early Triassic, being represented by pixels. The specimen was scanned at 220 kV, 400 mA, with a
Tupilakosaurus from both Greenland (Nielsen, 1967) and 0.5 mm brass beam filter, obtaining a 0.0635 mm isotropic voxel
Russia (Shishkin 1961, 1973). resolution. The CT data were imported into Amira 5.3.3, where
Dvinosaur fossils are much rarer in the southern hemisphere, the segmentation and the initial three-dimensional (3D) surface
where the clade is represented mainly by Triassic records from model were computed. The extracted 3D surface models were
southern Gondwana. The taxon Thabanchuia oomie occurs in then imported into Geomagic Studio 2012 to repair and edit irre-
strata assigned to the Lystrosaurus declivis Assemblage Zone gularities in the surface mesh geometry. All animations and still
(Early Triassic) of the South African Karoo Basin, and is rep- images of the digital specimen were rendered in Blender 2.60.
resented by multiple well-preserved small specimens including
complete skulls (Warren, 1999; Botha and Smith, 2020). In
SYSTEMATIC PALEONTOLOGY
addition, a putative dvinosaur was reported from the Buena
Vista Formation of the Paraná Basin in northern Uruguay (Mar- TEMNOSPONDYLI Zittel, 1888
sicano et al., 2000; Piñeiro et al., 2003), based on a fragmentary DVINOSAURIA Yates and Warren, 2000
skull. The age of the Uruguayan fossil is uncertain, as its host TIMONYA ANNEAE Cisneros, Marsicano, Angielczyk,
strata have been considered to be either Early Triassic (Marsi- Smith, Richter, Fröbisch, Kammerer and Sadleir, 2015
cano et al., 2000; Dias da Silva et al., 2007; Modesto and (Figs. 1–6)
Botha-Brink, 2010) or Lopingian (late Permian) (Piñeiro et al.,
2003) in age.
The Cisuralian Pedra de Fogo Formation (Parnaíba Basin of Holotype—MAP PV001, skull and partial postcranial
north-eastern Brazil), better known for its rich record of paleo- elements.
flora (e.g., Iannuzzi et al, 2018; Conceição et al., 2020), has also Horizon and Locality—Lower part of the Pedra de Fogo For-
produced temnospondyl remains, notably the large, long- mation (Parnaíba Basin), Cisuralian. Timon municipal area
snouted probable platyoposaurid Prionosuchus plummeri (locality PB028), Maranhão State, Brazil (Cisneros et al., 2015).
(Price, 1948; Cox and Hutchinson, 1991). Recent fieldwork in Revised Diagnosis—Timonya is distinguished from all other
the Pedra de Fogo Formation has recovered the remains of puta- dvinosaurs by the following unique combination of derived char-
tive rhinesuchid temnospondyls and two new dvinosaur taxa acter states: combined width of both parietals less than interorbi-
(Timonya anneae and Procuhy nazariensis), which represent tal width; anteroposterior length of the frontals subequal to the
the first definite dvinosaur records in the Paleozoic of Gondwana parietals; the premaxilla extends posteriorly in the palate so
(Cisneros et al., 2015). that its suture with the vomer is well behind the marginal tooth
The purpose of this work is to provide for the first time a row; prefenestral division of the palate as wide as long; foramen
detailed osteological description of the holotypes of the two for internal carotid artery on the ventral surface of the parasphe-
Pedra de Fogo dvinosaurs, and to present a new inclusive phylo- noid plate is elongated and groove-like; ossified opisthotic; pres-
geny of Temnospondyli in order to test the position of Dvino- ence of well-developed postglenoid area on the mandible longer
sauria within the clade and evaluate the interrelationships of than glenoid; mandible with a very shallow and wide profile,
dvinosaurids. Using this framework, we present a plausible resulting in the coronoids facing completely dorsally; presence
hypothesis on the paleogeographic history of dvinosaurs in the of a pair of parasymphyseal fossae on each side of mandibular
southern hemisphere. symphysis to accommodate the vomerine and palatal fangs.
Institutional Abbreviations—MAP (formerly UFPI), Museu Remarks—The holotype is preserved in a large piece of rock
de Arqueologia e Paleontologia, Universidade Federal do that has broken into several smaller blocks that fit together.
Piauí, Teresina, Brazil; PB, Parnaíba Basin locality (Museu de The three blocks containing the skull and the anteriormost post-
Arqueologia e Paleontologia catalogue); USNM, National cranial elements were found in 2011. In subsequent field trips to
Museum of Natural History (Smithsonian Institution), Washing- the same outcrop, additional blocks of fossil material pertaining
ton D.C., U.S.A. to the same specimen were found, including six additional frag-
Anatomical Abbreviations—Ac, anterior coronoid; An, ments of different size. The additional elements in these blocks
angular; Ar, articular; Arc, arch; Arcg, arcadian groove; Atl + are still unprepared and include part of the vertebral column,
Ax, atlas-axis; Bo, basioccipital; Cb, ceratobranchial; Cg, pectoral girdle (clavicle), and assorted isolated small bones.
carotid groove; Cl, clavicle; D, dentary; Eo, exoccipital; Epi, epip-
terygoid; Ept, ectopterygoid; f, fang; Fad, adductor fossa; Fr,
Skull
frontal; Ic, interclavicle; In, intercentrum; It, intertemporal; Ju,
jugal; La, lacrimal; Mc, middle coronoid; Mx, maxilla; Na, Dermal Ornament—The ornamentation of the dermal bones
nasal; Op, opisthotic; Pa, parietal; Par, prearticular; Pc, posterior of the skull in the holotype resembles that of most other temnos-
coronoid; Pfr, prefrontal; Pal, palatine; Ple, pleurocentrum; Pmx, pondyls. It consists of a coarse, pitted pattern developed at the
premaxilla; Po, postorbital; Pof, postfrontal; Pp, postparietal; ossification center of each dermal bone combined with a ridge-
Pqf, paraquadrate foramen; Psh, parasphenoid; Ps, postsplenial; and-furrow pattern radiating from it. The ornamentation is
Psf, parasymphyseal fossa; Psfn, postsymphyseal fang; Pt, ptery- most prominent on the jugal, postorbital, supratemporal, and
goid; Qj, quadratojugal; s, stapes; Sa, surangular; Sp, splenial; Sq, squamosal.
squamosal; St, supratemporal; Tab, tabular; V, vomer; Ver, ver- Lateral-line System—Traces of the lateral-line sensory sulci
tebral centra. are visible on the left side of the skull in the holotype, where
the dorsal surfaces of the skull table are better preserved. In
general, the sulci are relatively wide but shallow. The supraorbi-
COMPUTED TOMOGRAPHY AND IMAGE
tal sulcus runs close to the orbital margin along the prefrontal,
PROCESSING
the postfrontal, and over part of the postorbital. The infraorbital
X-ray micro-computed tomography (μCT) scan data for the sulcus is positioned along the jugal lateral to the orbit and
holotype of Timonya annae were acquired at Varian Medical extends anteriorly over the dorsolateral exposure of the palatine
Systems with a model BIR-225/500-CT/DR Industrial CT (LEP) and the maxilla. It continues towards the lacrimal, where
Marsicano et al.—Brazilian Permian dvinosaurs (e1893181-3)

the sulcus forms a strong bend (lacrimal flexure). There are also Neldasaurus (Schoch, 2018). Nevertheless, in Dvinosaurus and
indications of large elongated pits, probably related to the Acroplous the postparietals are strongly shortened anteroposter-
lateral-line system (see Witzmann et al., 2010), aligned antero- iorly, a condition not seen in Timonya.
posteriorly on the supratemporal and extending posteriorly The prefrontal is a stout, comma-shaped bone that constitutes
across the tabular-postparietal suture. the anteromedial border of the orbit. In front of the orbit, the
Skull Table Bones—The general outline of the skull is para- prefrontal contacts the LEP laterally and the lacrimal anteriorly.
bolic with an abbreviated preorbital region (Fig. 1A), similar to The prefrontal extends posteriorly around the orbital margin to
that of the North American Cisuralian dvinosaur Acroplous meet the postfrontal at approximately the midlength of the
(Engelhorn et al., 2008). The skull table bones are better orbit. The postfrontal is sub-quadrangular, slightly larger than
preserved on the left side of the skull. Although some bones the prefrontal, and extends posteriorly to meet the supratem-
on the right side are missing or badly crushed anteriorly, traces poral. There is no intertemporal ossification in the skull table,
of the sutures between elements are present on the natural similar to several other dvinosaurs like Dvinosaurus (Bystrow,
rock endocast of the interior surface of the skull roof (Fig. 1A). 1938), Acroplous (Engelhorn et al., 2008), and Triassic tupilako-
In general, the contacts among the bones of the skull table are saurids (see Warren, 1999). The supratemporal is relatively large
strongly interdigitated and in some cases they slightly overlap, and quadrangular, occupying the area between the parietal and
making the sutures difficult to trace. The general shape and squamosal. It is twice as long as wide and bears a pointed anterior
location of the nares can be partially traced on the endocast. process that contacts the postorbital. The squamosal also is large,
The nares were rounded, relatively small, and located anteriorly. rather anteroposteriorly elongated, and is surrounded by the
The orbits are relatively large and located slightly anterior and tabular, the supratemporal, the postorbital, the jugal, and the
lateral to the midline of the table. The interorbital width across quadratojugal. The squamosal forms part of the posterior
the frontals is relatively broad, nearly one and a half times the border of the skull table, which is nearly straight, following the
maximum orbital width. transverse line of the tabular and postparietal. Given this mor-
The premaxilla is partially preserved on both sides of the skull phology, the otic notch is absent. The tabular is small, somewhat
and has a short prenarial extension. The nasals are roughly quadrangular and smoothly tapers laterally. The tabular does not
square and occupy the middle of the preorbital region. The pre- project posterior to the margin of the skull table (i.e., tabular
maxilla-nasal suture is missing on both sides of the skull. Later- horns are absent). The condition of a straight posterior margin
ally, the nasal contacts the lacrimal and posteriorly it forms a of the table stemming from the absence of otic notch and
V-shaped suture between the frontal and the prefrontal. The tabular horns is also present in the Permian Isodectes (Sequeira,
combined width of the nasals is similar to that of the frontals, 1998) and Acroplous (Engelhorn et al., 2008) and in the Triassic
as in the North American Cisuralian divinosaur Isodectes tupilakosaurids (see Warren, 1999).
(Sequeira, 1998). The lacrimal is relatively small, anteroposter- The maxilla is partially visible on both sides of the skull. It
iorly elongated, and is exposed on the margin of the nares. Never- extends anteriorly from its contact with the premaxilla lateral
theless, it is excluded from the orbit margin by the contact to the nares, and it continues posteriorly to contact the quadrato-
between the LEP and the prefrontal. This condition is otherwise jugal at the level of the anterior border of the subtemporal fossa
only present in Isodectes (Sequeira, 1998). on the ventral border of the cheek. The maxilla is a thin strip of
The frontals are narrow, elongated elements that are about as bone that only expands anteriorly, just in front of the LEP, where
long anteroposteriorly as the orbits; they nearly double the it contacts the lacrimal. The presence of an LEP on the margin of
length of the nasals. The naso-frontal suture is slightly anterior the orbit on the skull table has been described previously in
to the anterior margin of the orbit, similar to Trimerorhachis Isodectes (Sequeira, 1998), Acroplous (Engelhorn et al., 2008),
and Neldasaurus (Schoch, 2018). A pointed process is present and Triassic tupilakosaurids (see Warren, 1999).
on the anterior edge of the frontal that invaginates the posterior The jugal forms most of the posterolateral border of the orbit.
margin of the nasal. The frontal is excluded from the orbital It strongly tapers anteriorly to contact the LEP on the lateral
margin by an extended prefrontal-postfrontal contact. The parie- margin of the orbit. Posteriorly it deepens behind the orbit,
tals are also anteroposteriorly elongated, being as long as the where it contacts the postorbital, the squamosal, and the quadra-
frontals and markedly longer than the supratemporals. The com- tojugal. A process of the jugal projects ventrally in front of the
bined width of both parietals is less than the interorbital width, a subtemporal fossa, but the maxilla-quadratojugal suture prevents
condition otherwise only observed in Triassic tupilakosaurids its exposure on the ventral border of the cheek.
(see Warren, 1999). The pineal foramen is located near the mid- The postorbital is relatively slender, much narrower than the
point of the interparietal suture, as in Acroplous (Engelhorn orbital width, and forms the posterior border of the orbit. Poster-
et al., 2008). In other short-snouted dvinosaurs the pineal iorly, it wedges between the squamosals and supratemporals, and
foramen is positioned more anteriorly on the interparietal laterally it contacts the posterior expansion of the jugal behind
suture, as in Dvinosaurus (Bystrow, 1938; Shishkin, 1973), the orbit. In contrast with dvinosaurs such as Erpetosaurus,
Erpetosaurus (Milner and Sequeira, 2011), and Isodectes Dvinosaurus, Thabanchuia, and Tupilakosaurus, where the inter-
(Sequeira, 1998). The similar anteroposterior length of the temporal bone is also absent, the postorbital does not extend
frontals and parietals is a condition only previously observed medially to contact the parietal (see Schoch, 2018). Among dvi-
in the recently described latest Carboniferous dvinosaur nosaurs the absence of a postorbital-parietal contact, as in
Trypanognathus (Schoch and Voig, 2019). The nearly straight Timonya, is otherwise only seen in Acroplous (Engelhorn
frontal-parietal suture is at the level of the posterior orbital et al., 2008). The remaining dvinosaurs (e.g., Trimerorhachis,
margin, as in Triassic tupilakosaurids (see Warren, 1999). Later- Neldasaurus, Isodectes) retain an intertemporal bone that prevents
ally, the parietal contacts the postfrontal and the supratemporal, contact between the postorbital and parietal (see Schoch, 2018).
and posteriorly it has a W-shaped suture with the postparietal. Palate—The right interpterygoid vacuity is better preserved,
The postparietal is approximately quadrangular in shape and although neither of them is complete. The general shape
slightly tapers laterally towards its contact with the tabular, appears to be relatively rounded and narrows posteriorly. The
forming an L-shaped suture with the supratemporal. This type subtemporal fossa also is incomplete but better defined on the
of contact is present in most dvinosaurs where the postparietal right side of the specimen. It is anteroposteriorly elongated,
tapers laterally, such as Dvinosaurus (Bystrow, 1938; Shishkin, and is bordered medially by the pterygoid, and anteriorly by a
1973), Acroplous (Engelhorn et al., 2008), Isodectes (Sequeira, process of the jugal, thus excluding the ectopterygoid from its
1998), Trimerorhachis (Milner and Schoch, 2013), and rim (Figs. 1B, 2).
Marsicano et al.—Brazilian Permian dvinosaurs (e1893181-4)

FIGURE 1. MAP PV001, holotype of Timonya anneae. A, fossil skull in dorsal view (left) and interpretative drawing (right); B, fossil skull and partial
postcranium in ventral view (left) and interpretative drawing (right).
Marsicano et al.—Brazilian Permian dvinosaurs (e1893181-5)

process on the anteromedial border of the interpterygoid vacuity.


The vomer encloses the choana anteriorly, and posteriorly it is
enclosed by the palatine, which excludes the maxilla from the
choanal margin. Just anterior to the choana there is a vomerine
fang (approx. 5 mm length), and its replacement pit, on both
sides of the palate. On the right vomer, there is evidence of a
transverse vomerine tooth row including at least three enlarged
teeth around half the size of the vomerine fang. The palatine is
subtriangular in outline and bears a single massive fang on its
anterior edge behind the choana. This fang is nearly double the
size of the vomerine fang. At least the anterior half of the pala-
tine is exposed on the border of the interpterygoid vacuity. The
rest of the border is badly damaged, so the extent of this
exposure is unknown. The ectopterygoid is anteroposteriorly
elongated and is about as long as the palatine. It bears a longi-
tudinal tooth row of approximately 10 teeth and a fang at the
midlength of the row. The ectopterygoid was apparently
excluded from the margin of the interpterygoid vacuity by the
pterygoid, and from the subtemporal fossa by a process of the
jugal.
The maxilla is partially preserved on both sides of the skull. As
previously mentioned, the maxilla contacts the quadratojugal on
the ventral border of the cheek and it is excluded from the border
of the choana. The marginal tooth row is composed of very small,
closely packed teeth that diminish in size posteriorly. They are
smaller than the corresponding teeth on the dentary marginal
row (Fig. 2).
Occiput—The structure of the occiput in the holotype can be
described from a natural break in the specimen that exposes
the occipital region in anterior view (Fig. 3), as well as from
the 3D rendering of the CT-scan data (Fig. 4). The skull table
and palate have a gently downturned profile mostly due to the
ventral curvature of the squamosals and the quadrate rami of
the pterygoids. As a result, the quadrate condyles are positioned
below the level of the occipital condyle when seen from behind.
The central portion of the occiput is occupied by a crescentic,
concave occipital condyle. Ventrally, the basioccipital constitutes
most of the articulation area and has a median groove for the
notochord. Lateral and dorsal to the notochordal groove lie the
exoccipitals, which also bear a median furrow. The whole struc-
FIGURE 2. MAP PV001, holotype of Timonya anneae. Segmented and ture is located behind the posterior border of the skull table,
colored bones of the palate from the 3D model. such that the occiput is gently inclined anteriorly when viewed
from above. Both exoccipitals are somewhat displaced from
their original position, particularly on the right side of the skull
(Fig. 4). The exoccipital extends anterodorsally into a stout verti-
cal process that meets the descending occipital flange of the post-
The central part of the palate is formed by the parasphenoid. parietal. Lateral to the process, a short paraoccipital process
The corpus is pentagonal and narrows anteriorly into a strip- extends anterolaterally towards the tabular. Between the dorsal
like cultriform process. The ventral surface of the corpus is and paroccipital processes, a small, rounded posttemporal fenes-
smooth, and its borders turn upwards so that the dorsal surface tra is present. Just below the foramen magnum, each exoccipital
of the process is smoothly concave. The parasphenoid corpus expands medially into a triangular laminar submedullar process.
underplates the basioccipital leaving only a thin strip of the On the left side of the skull, an isolated ossification is located
basioccipital visible posteriorly in ventral view (Fig. 1B). Ante- just in front and somewhat lateral to the exoccipital and is under-
riorly the base of the cultriform process is flanked by a groove plated by the parasphenoid. It is aligned with the exoccipital,
leading into the carotid foramen. Laterally, the contact of the slightly expanded anteriorly, and pierced by a small foramen lat-
parasphenoid with the pterygoids is incomplete on both sides erally. We identify this element as part of an ossified opisthotic
of the skull. The pterygoids appear disarticulated from the para- (Fig. 4). Among dvinosaurs, ossified elements of the otic
sphenoid, suggesting the absence of a firm contact between the capsule have only been described previously in Trimerorhachis
pterygoids and the basipterygoid process of the basisphenoid. (Watson, 1956; Schoch, 1999).
On the left side of the skull, the dorsal and lateral surface of Both stapes are preserved in the specimen. The right stapes is
the parasphenoid are partially preserved. A poorly ossified basi- close to its original position and the left is displaced inside of the
sphenoid is present, with a flat basipterygoid process preceded by cranium, lying at the level of the base of the cultriform process of
an anteroposteriorly elongated articular facet, as occurs in the the parasphenoid. The stapes is short and robust with a nearly
Trimerorhachis specimen described by Watson (1956:fig. 20). In square footplate. It is pierced by a stapedial foramen and bears
Timonya, however, both structures face laterally instead of a reduced ventral process. Nevertheless, the shaft is particularly
anterolaterally. short and compressed with an abbreviated vertical process.
The vomer is plate-like and nearly square. Posteriorly, it bears Based on the orientation of its footplate, the right stapes
a medial process that conceals the anterior part of the cultriform appears to be preserved close to its original position, although
Marsicano et al.—Brazilian Permian dvinosaurs (e1893181-6)

FIGURE 3. MAP PV001, holotype of Timonya


anneae. Posterior view. Segmented and colored
bones of the occiput and palate from the 3D
model.

it is rather horizontal. The short stapes with an abbreviated ver- surface of the pterygoid is mostly complete. There, the ascending
tical process resembles the stapes described for Dvinosaurus ramus is a smoothly curved, posteriorly concave lamina that
(Shishkin, 1973), although that of Timonya is even more robust. arises abruptly above the level of the quadrate ramus and ends
The occipital surface of both cheeks is largely missing (Figs. 3, anteromedially at the level of the basipterygoid articulation.
4). On the right side, a tiny quadratojugal is partially preserved The ascending lamina contacts the skull roof below the squamo-
on the ventrolateral corner of the skull and is pierced by a sal and along the supratemporal-squamosal suture towards the
small paraquadrate foramen at its contact with the squamosal. parietal (Fig. 4). In anterior view, at the level of the basipterygoid
The pterygoids are also incomplete, but some details can be articulation, the lamina contacts the epipterygoid anterome-
seen. The quadrate ramus is a wide, strip-like lamina that is dially, which appears to conceal the basipterygoid articulation
downturned towards the quadrate, thus forming the character- anteriorly. The epipterygoid arises from the dorsal surface of
istic vaulted palatal profile seen in other dvinosaurs such as the pterygoid and it is represented by an expanded basal
Acroplous (Engelhorn et al., 2008) and Dvinosaurus (Bystrow, portion facing anteromedially (Fig. 3). Its dorsalmost border is
1938; Shishkin, 1973). On the right side of the skull, the dorsal incomplete, thus no ascending process and/or otic process (such
as in Eryops; Sawin, 1941) are evident. No ossified epipterygoid
has been described in dvinosaurs, apart from in Acroplous in
which it is also seemingly incomplete dorsally (Hotton, 1959;
Coldiron, 1978).
Mandible—Part of the left mandible is exposed on the surface
of the block containing the skull (Fig. 1A), and additional infor-
mation is available from the CT-scan data (Fig. 5). It is difficult to
determine several of the sutures, particularly those on the labial
and ventral surfaces. The mandible has a very shallow and wide
profile, particularly in front of the adductor fossa; thus the coro-
noids face completely dorsally (Fig. 5A). The mandible deepens
slightly posterior to the adductor fossa and extends behind the
glenoid in a postglenoid area (PGA). The adductor fossa is rela-
tively long, and its labial wall is slightly taller than the lingual one.
On the lingual side of the mandible and just behind the glenoid,
there is a chordatympanic foramen on the prearticular. The labial
surface of the mandible preserves a narrow canal from the
sensory system, the oral sulcus. It extends along the ventral
border of the tooth row; dorsal to the sulcus the dentary is not
sculptured. The sulcus extends posteriorly and dorsally following
the dorsal border of the adductor wall on the surangular and con-
tinues onto the PGA to converge with the mandibular canal on
the dorsal border of the PGA.
As preserved on both hemimandibles, the PGA is at least as
long as the glenoid, even though its posteriormost tip is
missing. Labially, the PGA is limited by an extension of the sur-
angular, and ventrally by the angular. The articular area and the
PGA are hollow because part of the articular was cartilaginous
during the animal’s life. From the preserved bones, the articular
formed not only the glenoid but also the dorsal face of the PGA
and the distalmost part of its lingual surface. The surangular is
FIGURE 4. MAP PV001, holotype of Timonya anneae. Skull cross- exposed on the labial wall of the posterior third of the mandible,
section approximately at the level of the base of the cultriform process and also partially contributes to the posterior border of the
of the parasphenoid in A, fossil anterior view and B, interpretative adductor fossa. Dorsally, and just at the level of the
drawing. glenoid, the surangular forms a small, rounded, ornamented
Marsicano et al.—Brazilian Permian dvinosaurs (e1893181-7)

FIGURE 5. MAP PV001, holotype of Timonya


anneae. Segmented and colored bones of the
right hemimandible from the 3D model in A,
occlusal and B, ventral view.

knob (Fig. 5A). The knob is limited ventrally by the mandibular (Bystrow, 1938; Warren, 1999; Milner and Schoch, 2013). As in
sulcus and thus appears to be homologous with the postglenoid Thabanchuia, the proximal ends of the ceratobranchials are
process described by Warren and Black (1985) for some Triassic expanded and seemingly double-headed, probably for articula-
temnospondyls. Behind the process, the retroarticular process is tion with the basibranchial element (see Witzman, 2013).
relatively long, with subparallel borders. However, Timonya has four pairs of ceratobranchials like
A rounded and ornamented postglenoid process on the suran- Dvinosaurus and Trimerorhachis (Witzman, 2013), whereas
gular is also present in Trimerorhachis and Neldasaurus (C. Mar- Thabanchuia only possesses three pairs (Warren, 1999).
sicano, pers. obs.). However, the postglenoid area in Timonya is
relatively longer than in Thabanchuia, Dvinosaurus, and
Tupilakosaurus, where it is also expanded dorsally with a trans-
Postcranial Skeleton
verse trough behind the glenoid (Bystrow, 1938; Shishkin, 1973;
Warren, 1999). In Trimerorhachis, Neldasaurus, and Isodectes Axial Skeleton—Seven mostly articulated vertebrae, including
the PGA is abbreviated. the atlas, are associated with the skull (Fig. 6). Most of the ribs
The dentary tooth row bears densely packed teeth that are are missing from the association although there are some
slightly larger than the maxillary teeth and are markedly elements dispersed in the sediment that can be interpreted as
curved inwards. There are indications of enlarged symphyseal rib fragments. The neural arch bears a short spine nearly directly
teeth but not fangs, although the area is incomplete on both above the transverse process, which has a quadrangular cross-
hemimandibles. Lateral to the symphyseal region on the anterior section. The vertebrae are strongly notochordal, with the inter-
coronoid, there are two parasymphyseal fossae that pierced the centrum and two large pleurocentra forming a nearly complete
entire mandible, such that they exit in the area of the splenial. peripheral rim around the notochordal canal (Fig. 6A). The inter-
These fossae accommodate the vomerine and palatine fangs, as centra and pleurocentra are relatively thin and strip-like. The
is clearly observed on the right side of the skull where the mand- intercentrum is crescentic with the tips nearly touching each
ible is in articulation and the fangs protrude from the ventral other dorsally. The pleurocentra are comma-shaped and in
surface of the mandible (Fig. 5B). some cases in contact ventrally, forming a crescentic structure
Branchial Skeleton—There are remains of four ceratobran- that is open dorsally. The intercentra and pleurocentra are of
chials preserved on the right side of the specimen beneath the equivalent size in lateral view, with the neural arch located dor-
posterior third of the palate and underlaid by the pectoral sally approximately midway between them. The centrum of the
girdle (Figs. 1B, 3, 4). They are well-ossified, relatively large, first vertebrae (the atlas-axis) is formed by two ossifications,
and hollow. The elements are nearly circular in cross-section left and right, leaving a small notochordal canal in between
and gently curve medially, with a slightly expanded anterior (Fig. 6B). The centrum is anteroposteriorly longer than the
end. Each element bears a very shallow longitudinal groove on centra behind it, as it is formed by the co-ossification of the pleur-
its medial surface, which ends before reaching the expanded ocentra and intercentra of the atlas and axis. Its anterior face
anterior end. The presence of the groove indicates a perenni- bears a convex condyle that perfectly fits the concave surface
branchiate condition, where elements of the branchial skeleton of the occipital condyle. The atlantal neural arch is well-ossified,
are present and well-ossified, as has been postulated for other relatively small, and encloses a relatively larger neural canal than
dvinosaurs (e.g., Thabanchuia, Dvinosaurus, Trimerorhachis) the other neural arches in the preserved series.
Marsicano et al.—Brazilian Permian dvinosaurs (e1893181-8)

FIGURE 6. MAP PV001, holotype of Timonya anneae. Segmented and colored bones of the axial skeleton from the 3D model. A, a vertebra, from left
to right, in anterior, lateral, and posterior views. B, the partially articulated seven first thoracic vertebrae, including the atlas-axis in lateral view (left
side of the animal).

Osteoderms—Several elongate, unornamented ossifications likely were all part of the trunk covering that were dispersed
(approximately 5 mm maximum length) are preserved associated after the animal’s death.
with the specimen (Fig. S1 in Supplemental Data). They are pre-
served dispersed beneath the palate and around the postcranial TEMNOSPONDYLI Zittel, 1888
elements, but others are associated in groups. The ones DVINOSAURIA Yates and Warren, 2000
beneath the skull are relatively rhomboidal whereas those PROCUHY NAZARIENSIS Cisneros et al. , 2015
exposed more posteriorly near the postcranial fragments are (Figs. 7, 8)
more spindle-shaped. The presence of dermal scales associated
with the trunk in temnospondyls is widely known, particularly Holotype—MAP PV011, partial skull table and right mandib-
as covering of the ventral surface of the body (see Witzmann, ular ramus associated in the same slab.
2007). In dvinosaurs, such as Trimerorhachis, Neldasaurus, Horizon and Locality—Lower Pedra de Fogo Formation (Par-
Erpetosaurus, and Isodectes, different morphologies of dermal naíba Basin), Cisuralian. Nazária Municipality (locality PB131),
scales have been described (Chase, 1965; Olson, 1979; Milner Piauí State, Brazil (Cisneros et al., 2015).
and Sequeira, 2011). Rectangular and ornamented osteoderms Referred Specimen—MAP PV 770, a partial skull table,
also are present in some dvinosaurs, such as Isodectes and missing the snout, preserved in a slab as part and counterpart
Acroplous, but in this case they are located below the ventral (Fig. 8); collected in 2015 at locality PB178, Nazária municipality,
and medial borders of the mandible (see Milner and Sequeira, Piauí State, Brazil.
2011). This type of osteoderm is absent in Timonya. Therefore, Revised Diagnosis—Procuhy is distinguished from all other
the bony structures found in the specimen beneath the palate members of Dvinosauria by the following unique combination
and associated with the axial skeleton more posteriorly most of derived character states: anteriormost extension of the
Marsicano et al.—Brazilian Permian dvinosaurs (e1893181-9)

FIGURE 7. MAP PV011, holotype of Procuhy nazariensis. A, fossil skull table in ventral view and right hemimandible in lingual view (left) and B,
interpretative drawing (right).

squamosal posterior to parietal midlength; combined width of Skull


both parietals equal to interorbital width; pineal foramen posi-
The holotype consists of a natural mold of the dorsal surface of
tioned posterior to the midlength of the parietal; supratemporal
the skull table, with some fragments of table bones preserved in
exposed on the posterior border of the skull table; length of the
ventral aspect. The mold preserves some of the sutures and orna-
parietal more than three times its width; in the mandible, pres-
mentation, making it possible to produce a composite description
ence of postglenoid process of the surangular separated from
of the skull table.
the retroarticular process of the articular by the mandibular
Dermal Ornament and Lateral-line System—The scattered
sulcus.
areas that preserve ornament do not show any distinctive fea-
tures; the ornament is very similar to that present in most tem-
nospondyls and is dominated by a coarsely pitted pattern. Only
a partial fragment of a relatively wide, shallow lateral-line
canal is preserved on the right lacrimal, which shows a pro-
nounced curvature (lacrimal flexure). This is part of the infraor-
bital canal, which generally runs across the lacrimal lateral to the
orbit. The presence of a lacrimal flexure in front of the orbit has
been described previously in some other dvinosaurs such as
Trimerorhachis and Neldasaurus (Chase, 1965; Milner and
Schoch, 2013).
Skull Table—The skull table is completely missing anterior to
the naso-frontal suture; furthermore, the lateralmost borders of
the table on both sides of the skull are not preserved. Therefore,
the position and shape of the snout, including the external nares,
are unknown. Most of the bone around the orbits is missing, so
their overall shape is uncertain. The orbit outlines shown in
Figure 7 were reconstructed using MAP PV 770 (see Fig. 8).
The best-preserved part of the skull table is the postorbital
region, which is quadrangular and anteroposteriorly elongated.
This shape stems from the marked elongation of the parietals,
postorbitals and postfrontals, a condition also present in some
dvinosaurs such as Isodectes (Sequeira, 1998) and Erpetosaurus
(Milner and Sequeira, 2011), although in Procuhy the parietals
are proportionally longer than in other dvinosaurs.
The postfrontals are partially preserved on both sides of the
FIGURE 8. MAP PV770, referred specimen of Procuhy nazariensis. table and extend behind the orbit to contact the postorbital lat-
Fossil skull table in dorsal view with interpretative drawing. erally, and the intertemporal and parietal posteriorly. The
Marsicano et al.—Brazilian Permian dvinosaurs (e1893181-10)

postfrontal-prefrontal suture is not preserved in the specimen, mandible (PGA) and that the ventral border of the ramus was
and only part of the left prefrontal-frontal suture is preserved. slightly convex (Fig. 7). Anteriorly, at the symphysis, the base
However, it is clear in PV 770 that the frontals were excluded of a relatively large fang is present. The anterior third of the
from the orbital margin (Fig. 8). The frontals are narrow and mandible was bordered ventrally by the splenial, which sur-
elongate, and their sutures with the nasals seem to have been rounded a subcircular parasymphyseal fenestra anterior and
situated beyond the anterior margin of the orbit. The parietals lateral to the symphysis. The posteriormost tip of the mandible
are long, somewhat quadrangular, and constitute the largest bears a short and rounded process that is preserved as a
bones of the postorbital region, being anteroposteriorly longer natural mold. The process projects dorsally and is most probably
than the frontals, the postorbitals, and the supratemporals. Ante- the retroarticular process of the articular. A second process is
riorly, the frontal-parietal suture appears to be located just also preserved as a natural mold in the sediment, and this
behind the posterior border of the orbit, although the contact might represent the postglenoid process of the surangular, separ-
is not well preserved. Anterolaterally, the parietal contacts the ated from the retroarticular process by the mandibular sulcus
postfrontal, laterally the intertemporal and the supratemporal, (see Warren and Black, 1985). A similar structure of the PGA,
and posteriorly it joins the postparietal. The pineal foramen is with two blunt processes projecting posteriorly from the articular
located well behind the midpoint of the mid-parietal suture. and surangular, is also present in Acroplous (based on USNM
The postparietals are well-developed and roughly square; later- 22528, CAM pers. observ.) but in that taxon there is a third
ally they contact the tabular and the supratemporal. As pre- process of the surangular labially, a condition that cannot be cor-
served, the posterior border of the skull table between the roborated in Procuhy because of the holotype’s preservation
postparietals is concave anteriorly. The tabulars are nearly as mostly as a natural mold. In Trimerorhachis, the postglenoid
large as the postparietals and they are also somewhat square in area also bears posterior projections of the articular and surangu-
profile. They form a short, blunt projection (tabular horn) on lar, which Milner and Schoch (2013) identified as the retroarticu-
the posterior border of the table, as can be observed on the left lar and arcadian processes, respectively. However, the exact
side of the holotype and PV 770. Short and rounded tabular morphology of the processes varies among the different
horns only have been described previously in Carboniferous– Trimerorhachis species (Olson, 1955; Milner and Schoch, 2013).
Permian trimerorhachids, such as Trimerorhachis and Neldasaurus
(see Schoch, 2018).
The supratemporals are relatively large and wider than the PHYLOGENETIC ANALYSIS
parietals but not as elongated. Anteriorly, the supratemporal Methods
tapers and wedges between the intertemporal and postorbital
at about the midlength of the parietal. On the left side of the We constructed a new phylogenetic dataset by combining
table, a nearly straight suture separates the supratemporal from characters from several previous comprehensive analyses on
the preserved fragment of squamosal. Posteriorly, the supratem- temnospondyls and particularly on dvinosaurs (Holmes et al.,
poral contacts the postparietal and tabular, and extends laterally 1998; Yates and Warren, 2000; Ruta and Bolt, 2006; Engelhorn
to contribute to the posterior margin of the table. Among dvino- et al., 2008; Schoch, 2013; Cisneros et al., 2015; Marsicano et al.,
saurs, this condition was only reported in the Carboniferous 2017). During the description of the Brazilian dvinosaur
taxon Eugyrinus (Milner, 1980). Only a fragment of the left squa- material we added new characters and modified and re-coded
mosal is present in the specimen, and it is too poorly preserved to several others (details in Supplemental Data). Our final
trace the shape of the otic embayment. However, the short, blunt dataset includes 40 temnospondyl taxa (OTUs) and 178 discrete
tabular horn suggests that a shallow embayment was present. characters, all treated as unordered and weighted equally. The
Although poorly preserved, this is also evident in MAP PV data-matrix was compiled in Mesquite 3.2 (Maddison and Mad-
770. On the left side of the skull, a natural mold of part of a dison, 2018) and the phylogenetic analysis was performed using
rod-like bone is positioned at the level of the putative otic TNT version 1.5 (Goloboff and Catalano, 2016). We used the
embayment. Its identity is uncertain, but it could represent the traditional search (heuristic) option of tree bisection reconnec-
distal part of the left stapes. The intertemporal is clearly visible tion (TBR) set to collapsing ambiguously supported branches
on both sides of the table. It is a prominent oblong bone, posi- (“collapsing rule 1”) and saving 10 replicates per tree. The heur-
tioned in the middle of the temporal area and surrounded by istic search produced 10 MPTs (tree length = 1029 steps, Con-
the postorbital, supratemporal, parietal, and postfrontal. An sistency Index = 0.22, Retention Index = 0.44, Rescaled
intertemporal ossification is present in some other dvinosaurs, Consistency Index = 0.1). The strict consensus tree and the
such as Eugyrinus (Milner, 1980), Trimerorhachis (Milner and majority rule consensus, which is identical to tree number 1,
Schoch, 2013), Isodectes (Sequeira, 1998), and Neldasaurus are included in the Supplemental Data as Figs. S2 and S3,
(Chase, 1965), and has long been considered a plesiomorphic respectively. We used symmetric resampling to measure
character state for temnospondyls (see Yates and Warren, branch support, using the topology of tree number 1 and 5000
2000). The postorbital is relatively large (about as long as the resampling replicates.
supratemporal), anteroposteriorly elongated, and tapers poster-
iorly between the squamosal and supratemporal. As noted
Results
above, the area surrounding both orbits is extensively
damaged. Nevertheless, a suture between the postorbital and The new phylogenetic analysis is much more inclusive than our
the lacrimal is apparent on the posterolateral border of the previous investigation of the relationships of Procuhy and
right orbit. As a result, the lacrimal forms the majority of the Timonya (Cisneros et al., 2015), but our results for Dvinosauria
lateral side of the orbit, excluding the jugal from its rim. as a whole, and Timonya and Procuhy specifically, are consistent
Among dvinosaurs, this condition is only present in Trimerorhachis (see Fig. S2 in Supplemental Data). The clade Dvinosauria
(Milner and Schoch, 2013). (Fig. 9) consists of two sister-groups, Trimerorhachidae (includ-
Mandible—The right hemimandible is partially preserved in ing Erpetosaurus, Neldasaurus, Trypanognathus, Trimerorhachis,
the same fashion as the skull table, partially as a natural mold and Procuhy) and the “short-snouted” dvinosaurs (Dvinosauroi-
but with some bones still present. The bones preserved are dea sensu Yates and Warren, 2000) Dvinosaurus, Timonya,
mostly visible in internal aspect, and they are flattened against Isodectes, and Acroplous as successive sister taxa of
each other (Fig. 7). From the general profile of the ramus, it is Tupilakosauridae (Thabanchuia + Tupilakosaurus). Previous cla-
evident that there was an abbreviated postglenoid area in the distic analyses of dvinosaurs (Engelhorn et al., 2008; Schoch,
Marsicano et al.—Brazilian Permian dvinosaurs (e1893181-11)

FIGURE 9. Calibrated cladogram of Dvino-


sauria obtained in the present study with the
Brazilian dvinosaurs in bold. 1, Trimerorhachi-
dae; 2, Dvinosauroidea; 3, Tupilakosauridae.
Ages from http://www.stratigraphy.org/
ICSchart/ChronostratChart2020-03.pdf.
Abbreviations: Artinsk, Artinskian; Ass, Asse-
lian; C, Carboniferous; Cap, Capitanian; Ch,
Changhsingian; Giz, Gzelian; Ind, Induan; Kas,
Kasimovian; Kung, Kungurian; Mosc, Moscov-
ian; Ole, Olenekian; Roa, Roadian; Sak, Sak-
marian; Tr, Triassic; Wor, Wordian; Wu,
Wuchiapingian.

2018; Schoch and Voigt, 2019) yielded basically the same results palatoquadrate fissure (66:0), and the absence of a basicranial
although they varied in taxon sampling (e.g., Engelhorn et al., suture between the pterygoids and the parasphenoid plate
2008 did not include Procuhy or Timonya because they had not (97:0), among others. The position of the Brazilian trimerorha-
yet been discovered). Schoch and Voigt (2019), who used the chid Procuhy as the sister taxon of Trimerorhachis from North
same set of characters as Engelhorn et al. (2008) but with a America is supported by the presence of a large, anteroposter-
larger sample of divinosaur taxa including the Brazilian ones, iorly extended lacrimal that contacts the postorbital posteriorly,
also obtained the clade Trimerorhachidae, although it was restricted excluding the jugal from the orbital margin (20:3).
to the North American taxa Neldasaurus + Trimerorhachis. This
clade is the sister-group of a clade that includes most dvinosaurs
as successive sister-taxa of Tupilakosauridae (Dvinosauroidea). DISCUSSION
In this tree, the Brazilian Procuhy appears as the basalmost dvi- At a broad scale, our analysis places Dvinosauria at the base of
nosaur (Schoch and Voigt, 2019), in contrast to its position as the Temnospondyli, as the sister group of the remainder of the clade
sister-taxon of Trimerorhachis recovered here. (see Fig. S3 in Supplemental Data). Among the non-dvinosaur-
The new topology obtained here (Fig. 9) depicts a more ian temnospondyls, edopoids and “dendrerpetids” group
inclusive Carboniferous–Permian clade Trimerorhachidae together in a clade that is in turn the sister group of higher Ster-
(Erpetosaurus + ((Neldasaurus + Trypanognathus) + (Trimerorhachis ospondylomorpha. Other datasets that include a significant
+ Procuhy))) supported by three unequivocal synapomorphies: number of temnospondyl taxa have produced alternative con-
the presence of an anteroposteriorly elongated postorbital that figurations regarding the stem of Stereospondylomorpha (e.g.,
tapers posteriorly (28:0), the presence of two depressions on the Milner, 1990; Yates and Warren, 2000; Ruta and Bolt, 2006;
ventral surface of the parasphenoid close to its suture with the Schoch, 2013; Pardo et al., 2017; Marjanovic and Laurin, 2019).
basioccipital (104:1), and the lateral border of the choana Schoch’s (2013) hypothesis shows the edopoids as the earliest
formed by the premaxilla and maxilla (85:3). Also, the retention diverging lineage of Temnospondyli, followed crownwards, by
of the intertemporal on the skull table and a reduced postglenoid “dendrerpetids” and dvinosaurs as successive sister-groups of
area in the mandible (130:1) are shared by most members of this Stereospondylomorpha. Similar results were obtained by Ruta
clade where the relevant areas are preserved. The remaining and Bolt (2006) with edopoids rootward of dvinosaurs, although
dvinosaurs, the Triassic tupilakosaurids and their Paleozoic out- in this case “dendrerpetontids” are polyphyletic with some of the
groups (Dvinosauroidea), share seven unequivocal synapomor- taxa placed at the base of Temnospondyli and others as the stem
phies: postparietals that taper abruptly laterally (51:1), tabulars of the clade Dvinosauria + Stereospondylomorpha. A sister-
reduced to thin slivers (not in Timonya) (53:1), the absence of group relationship between dvinosaurs and stereospondylo-
otic notch (57:2), the presence of a dorsal process of the palatine morphs also was hypothesized by Yates and Warren (2000). In
exposed on the lateral border of the orbit (apparently absent in contrast, the manually produced cladogram by Milner (1990)
Dvinosaurus) (20:1), the presence of a vaulted palate formed by shows the “dendrerpetids” as the most stemward group of tem-
the downturned quadrate ramus of the pterygoids (69:2), and in nospondyls with edopoids and dvinosaurs crownwards. Finally,
the mandible, the ventral margin of the angular is nearly flat a recent phylogeny of basal tetrapods by Marjanovic and
(150:1) with the glenoid fossa at or below the level of the dorsal Laurin (2019) resulted in the unique position of Dissorophoidea
surface of the dentary (141:1). as the basal-most group of Temnospondyli with “dendrerpetids”,
The Brazilian Timonya is recovered as an early-diverging dvinosaurs and edopoids as successive sister-groups of higher
member of Dvinosauroidea and is nested among Cisuralian temnospondyls. These alternative topologies reflect the continu-
North American taxa, such as Isodectes and Acroplous, and the ing uncertainty about the basal nodes of Temnospondyli and the
Lopingian Dvinosaurus from the Russian platform. This position poor branch support in this part of the phylogeny (also see
is the result of the retention of several plesiomorphic traits in Schoch, 2013). This uncertainty also is evidenced in the collapse
Timonya, such as the relatively large postfrontal (32:0) and tab- of most nodes in our strict consensus tree (see Fig. S2 in Sup-
ulars (53:0), the position of the quadrate and occipital condyles plemental Data) even when many taxa are represented by
nearly in the same transverse plane (62:1), the absence of a fairly complete specimens. Differences in taxon and character
Marsicano et al.—Brazilian Permian dvinosaurs (e1893181-12)

sampling and scoring among the datasets used by various for Research and Exploration (9601-14), Universidad de Buenos
authors, together with the high levels of homoplasy and possible Aires Ciencia y Técnica (UBACyT 20020170100643), Sofja
character state exhaustion that characterized the early evolution Kovalevskaja Award of the Alexander von Humboldt Foun-
of temnospondyls and early tetrapods in general (e.g., Ruta et al., dation, and the Natural History Museum of London. We thank
2003; Bernardi et al., 2016; Pardo et al., 2017; Marjanovic and S. Bessone and S. Gibson for preparation of the delicate
Laurin, 2019), make their relationships difficult to disentangle. Timonya specimens, A. Shinya for additional fossil preparation,
The two recently described Pedra de Fogo dvinosaurs show B. Smith (Varian Medical Systems) for CT-scanning assistance,
close relationships with Cisuralian taxa (e.g., Trimerorhachis, and R. Sadleir for assistance with processing the CT data. We
Acroplous, Isodectes) from the American southwest, which is thank the editor A. Huttenlocker and E. V. Dias and T. Arbez
the only other area where dvinosaurs are diverse and both for their constructive reviews. This is CAM’s contribution R-
major subclades (trimerorhachids and dvinosauroids) are 345 to the Instituto de Estudios Andinos Don Pablo Groeber.
known. The close paleogeographic connections between the tet-
rapods of the North American Permian and the Pedra de Fogo
Formation suggested by the temnospondyls are corroborated ORCID
by the presence of the captorhinid Captorhinikos in both areas Claudia Marsicano http://orcid.org/0000-0002-0121-6730
(Ianuzzi et al., 2018; Cisneros et al., 2020). Interestingly, the Bra- Juan C. Cisneros http://orcid.org/0000-0001-6159-1981
zilian dvinosaurs are not closely related to the Early Triassic tupi- Martha Richter http://orcid.org/0000-0002-9806-4816
lakosaurid Thabanchuia from southern Gondwana (Karoo Christian F. Kammerer http://orcid.org/0000-0002-0596-623X
Basin) (Warren, 1999). The latter taxon is more closely related Roger M. H. Smith http://orcid.org/0000-0001-6806-1983
to contemporaneous Eurasian taxa from Russia and Greenland
(Tupilakosaurus spp.), suggesting that it represents a separate
dispersal event. The unnamed dvinosaur from the Early Triassic LITERATURE CITED
of the Paraná Basin (Uruguay) is too fragmentary to clearly Berman, D. 1973. A trimerorhachid amphibian from the Upper
assess its affinities (Marsicano et al., 2000), so it is unclear Pennsylvanian of New Mexico. Journal of Paleontology 47:932–945.
which of these dispersal events best explains its presence in Bernardi, M., K. D. Angielczyk, J. S. Mitchell, and M. Ruta. 2016.
southern Gondwana. Phylogenetic stability, tree shape, and character compatibility: a
case study using early tetrapods. Systematic Biology 65:737–758.
Iannuzzi et al. (2018) recently discussed the Permian floral and
Bernardi, M., F. M. Petti, E. Kustatscher, M. Franz, C. Hartkopf-Fröder,
faunal content of the Parnaíba Basin and the paleogeographic C. C. Labandeira, T. Wappler, J. H. A. van Konijnenberg-van
implications of the fossils preserved in the Pedra de Fogo For- Cittert, B. R. Peecook, and K. D. Angielczyk. 2017. Late Permian
mation (PFF). The somewhat limited floral record of the unit, (Lopingian) terrestrial ecosystems: a global comparison with new
mostly represented by fossil tree trunks, shows some links with data from the low-latitude Bletterbach Biota. Earth-Science
the Euramerican Floral Province which, together with the lack Reviews 175:18–43.
of the characteristic glossopterids from the Gondwanan Floral Botha, J., and R. M. H. Smith. 2020 Biostratigraphy of the Lystrosaurus
Province, point to a closer paleogeographic relationship declivis Assemblage Zone (Beaufort Group, Karoo Supergroup),
between the Parnaíba Basin and Euramerica. However, the South Africa. South African Journal of Geology 123:207–216.
PFF flora also exhibits strong endemism that points to a distinct Brocklehurst, N., M. O. Day, B. S. Rubidge, and J. Fröbisch. 2017. Olson’s
extinction and the latitudinal biodiversity gradient of tetrapods in
phytogeographic unit that occupied the paleotropical belt of the Permian. Proceedings Royal Society, B 284, 20170231.
northern Gondwana during the Cisuralian (Iannuzzi et al., Bystrow, A. P. 1938. Dvinosaurus als neotenische Form der
2018; da Conceição et al., 2020). Similarly, the vertebrates Stegocephalen. Acta Zoologica 19:209–295.
recorded in the unit also show relationships with equatorial Case, E. C. 1935. Description of a collection of associated skeletons of
faunas of Euramerica (North American SW), particularly the tet- Trimerorhachis. Contributions of the Museum of Paleontology,
rapods (Cisneros et al., 2015, 2020; Iannuzzi et al., 2018), University of Michigan 4:227240.
although a degree of endemism is evident. Chase, J. N. 1965. Neldasaurus wrightae, a new rhachitomous labyrintho-
As noted above, our phylogenetic hypothesis for Dvinosauria dont from the Texas Lower Permian. Bulletin of the Museum of
Comparative Zoology 133: 153–225.
(Fig. 9) supports a closer relationship of the PFF taxa with those
Cisneros, J. C., C. Marsicano, K. D. Angielczyk, R. M. H. Smith, M.
from the Cisuralian of Euramerica than to southern Gondwanan Richter, J. Fröbisch, C. F. Kammerer, and R. W. Sadleir. 2015.
taxa from the Early Triassic (see Cisneros et al., 2015). The pres- New Permian fauna from tropical Gondwana. Nature
ence of representatives of both major dvinosaurian linages in the Communications 6:8676. doi: 10.1038/ncomms9676.
PFF, together with the position of Timonya as a basal dvinosaur- Cisneros J. C., K. D. Angielczyk, C. F. Kammerer, R. M. H. Smith, J.
oid, strongly suggests a dispersal of dvinosaurs into tropical Fröbisch, C. Marsicano, and M. Richter. 2020. Captorhinid reptiles
Gondwana as early as the beginning of the Pennsylvanian (late from the lower Permian Pedra de Fogo Formation, Piauí, Brazil: the
Carboniferous). Following the Carboniferous–Permian bound- earliest herbivorous tetrapods in Gondwana. PeerJ 8:e8719 https://
ary, a protracted amelioration of the climatic conditions in doi.org/10.7717/peerj.8719
central Pangea, characterized by the intensification of seasonality da Conceição, D. M., A. Crisafulli, R. Iannuzzi, R. Neregato, J. C.
Cisneros, and L S. de Andrade. 2020. New petrified gymnosperms
and aridity and the establishment of latitudinal climatic belts from the Permian of Maranhão (Pedra de Fogo Formation),
(e.g., Gibbs et al., 2002; Tabor and Poulsen, 2008), likely initiated Brazil: Novaiorquepitys and Yvyrapitys. Review of Palaeobotany
the climate-controlled endemism in the region, which continued and Palynology 276:104177.
across Pangea until the end of the Paleozoic (e.g., Sidor et al., Coldiron, R. W. 1978. Acroplous vorax Hotton (Amphibia:
2005; Bernardi et al., 2017; Brocklehurst et al., 2017). Saurerpetontidae) restudied in light of new material. American
Museum Novitates 2662:1–27.
Cox, C. B., and P. Hutchinson. 1991. Fishes and amphibians from the Late
Permian Pedra de Fogo Formation of northern Brazil.
ACKNOWLEDGEMENTS Palaeontology 34:561–573.
Dias-da-Silva, S., S. P. Modesto, and C .L. Schultz. 2007. New material of
Research was supported by grants from The Negaunee Foun- Procolophon (Parareptilia: Procolophonoidea) from the Lower
dation, The Grainger Foundation, the Field Museum of Natural Triassic of Brazil, with remarks on the ages of the Sanga do
History, Conselho Nacional para a Ciencia e Tecnologia (CNPq Cabral and Buena Vista formations of South America. Canadian
401848.2010-8, 456608/2014-1), National Geographic Committee Journal of Earth Sciences 43:1685–1693.
Marsicano et al.—Brazilian Permian dvinosaurs (e1893181-13)

Englehorn J., B. J. Small, and A. Huttenlocker. 2008. A redescription of Sawin, H. J. 1941.The cranial anatomy of Eryops megacephalus. Bulletin
Acroplous vorax (Temnospondyli: Dvinosauria) based on new Museum of Comparative Zoology Harvard 88:407–463.
specimens from the Early Permian of Nebraska and Kansas, Schoch, R. R. 1999. Studies on braincases of early tetrapods: structure,
U.S.A. Journal of Vertebrate Paleontology 28: 291–305. homology, and phylogeny 1. Trimerorhachis and other primitive
Gibbs, M. T., P. M. Rees, J. E. Kutzbach, A. M. Ziegler, P. J. Behling, and D. temnospondyls. Neues Jahrbuch fuer Geologie und
B. Rowley. 2002. Simulations of Permian climate and comparisons Palaeontologie, Abhandlungen, 213:233–259.
with climate-sensitive sediments. The Journal of Geology 110:3–55. Schoch, R. R. 2013. The evolution of major temnospondyl clades: an
Goloboff, P. A., and S. A. Catalano. 2016. TNT version 1.5, including a inclusive phylogenetic analysis. Journal Systematic Palaeontology
full implementation of phylogenetic morphometrics. Cladistics 32: 11:67–70.
221–238. Schoch, R. R. 2018. Osteology of the temnospondyl Neldasaurus and the
Hotton, N. III. 1959. Acroplous vorax, a new and unusual labyrinthodont evolution of basal dvinosaurians. Neues Jahrbuch für Geologie und
amphibian from the Kansas Permian. Journal of Paleontology Paläontologie, Abhandlungen 278:1–16.
33:161–178. Schoch, R. R., and S. Voigt. 2019. A dvinosaurian temnospondyl
Iannuzzi, R., R. Neregato, J. C. Cisneros, K. D. Angielczyk, R. Rössler, R. from the Carboniferous-Permian boundary of Germany sheds
Rohn, C. A. Marsicano, J. Fröbisch, T. Fairchild, R. M. H. Smith, F. light on dvinosaurian phylogeny and distribution. Journal of
Kurzawe, M. Richter, M. C. Langer, T. M. V. Tavares, C. F. Vertebrate Paleontology, 39: e1577874. DOI:10.1080/02724634.
Kammerer, D. M. da Conceição, J. D. Pardo, and G. A. Roesler. 2019.1577874
2018. Re-evaluation of the Permian macrofossils from the Sequeira, S. E. K. 1998. The cranial morphology and taxonomy of the
Parnaíba Basin: biostratigraphic, palaeoenvironmental and palaeo- saurerpetontid Isodectes obtusus comb. nov. (Amphibia:
geographical implications. Geological Society, London, Special Temnospondyli) from the Lower Permian of Texas. Zoological
Publications 472:223–249. Journal of the Linnean Society 122:237–259.
Marjanovic, D., and M. Laurin. 2019. Phylogeny of Paleozoic limbed ver- Shishkin, M. A. 1961. New data on Tupilakosaurus. Doklady Akademii
tebrates reassessed through revision and expansion of the largest pub- Nauk SSSR 136: 938–941.
lished relevant data matrix. PeerJ 6:e5565 DOI 10.7717/peerj.5565 Shishkin, M. A. 1973. The morphology of the early Amphibia and some
Marsicano, C., D. Perea, and M. Ubilla. 2000. A new temnospondyl problems of the lower tetrapod evolution. Trudy
amphibian from the Lower Triassic of South America. Alcheringa Paleontologicheskogo Instituta 137:1–260.
24:119–123. Sidor, C. A., F. R. O’Keefe, R. Damiani, J. S. Steyer, R. M. H. Smith, H. C.
Milner, A. R. 1980. The temnospondyl amphibian Dendrerpeton from the Larsson, P. Sereno, O. Ide, and A. Maga. 2005. Permian tetrapods
upper Carboniferous of Ireland. Palaeontology 23:125–141. from the Sahara show climate-controlled endemism in Pangaea.
Milner, A. R. 1990. The radiations of temnospondyl amphibians. 321–349. Nature 434:886–889.
In Taylor, P. D. and Larwood, G. P. (eds). Major evolutionary radi- Tabor, N. J., and C. J. Poulsen. 2008. Palaeoclimate across the Late
ations. Clarendon Press, Oxford, 437 pp. Pennsylvanian–Early Permian tropical palaeolatitudes: a review of
Milner, A. R., and R. R. N. Schoch. 2013. Trimerorhachis (Amphibia: climate indicators, their distribution, and relation to palaeophysio-
Temnospondyli) from the Lower Permian of Texas and New graphic climate factors. Palaeogeography, Palaeoclimatology,
Mexico: cranial osteology, taxonomy and biostratigraphy. Neues Palaeoecology 268:293–310.
Jahrbuch für Geologie und Paläontologie, Abhandlungen 270:91–128. Warren, A. A. 1999. Karroo tupilakosaurid: a relict from Gondwana.
Milner, A. R., and S. E. K. Sequeira. 2011. The amphibian Erpetosaurus Transactions of the Royal Society of Edinburgh: Earth Sciences
radiatus (Temnospondyli, Dvinosauria) from the Middle 89:145–160.
Pennsylvanian of Linton, Ohio: morphology and systematic pos- Warren A. A., and T. Black. 1985. A new rhytidosteid (Amphibia:
ition. Special Papers in Palaeontology 86:57–73. Labyrinthodontia) from the Early Triassic Arcadia Formation of
Modesto, S.P., and J. Botha-Brink. 2010. Problems of correlation of South Queensland, Australia, and the relationships of Triassic temnospon-
African and South American tetrapod faunas across the Permian– dyls. Journal of Vertebrate Paleontology 5:303–327.
Triassic boundary. Journal of African Earth Sciences 57:242–248. Watson, D. M. S. 1956. The brachyopid labyrinthodonts. Bulletin of the
Nielsen, E. 1967. New observations on the skull roof of the holotype of British Museum of Natural History 2:317–392.
Tupilakosaurus heilmani Nielsen. Zoological Journal of the Witzmann, F. 2007. The evolution of the scalation pattern in temnospon-
Linnean Society 47:225–229. dyl amphibians. Zoological Journal of the Linnean Society 150: 815–
Olson, E. C. 1955. Fauna of the Upper Vale and Choza: 10. 834.
Trimerorhachis: including a revision of preVale species. Fieldiana: Witzmann, F. 2013. Phylogenetic patterns of character evolution in the
Geology 10:225–274. hyobranchial apparatus of early tetrapods. Transactions of the
Olson, E. C.1979. Aspects of the biology of Trimerorhachis (Amphibia: Royal Society of Edinburgh: Earth Sciences 104: 145–167.
Temnospondyli). Journal of Paleontology 53:1–17. Witzmann, F., H. Scholtz, J. Müller, and N. Kardjilov. 2010. Sculpture and
Pardo, J. D., B. J. Small and A. K. Huttenlocker. 2017. Stem caecilian vascularization of dermal bones, and the implications for the physi-
from the Triassic of Colorado sheds light on the origins of ology of basal tetrapods. Zoological Journal of the Linnean Society
Lissamphibia. Proceedings of the National Academy of Sciences 160:302–240.
of the United States of America 114: E5389–E5395. Yates, A. M., and A. A. Warren. 2000. The phylogeny of the ‘higher’ tem-
Piñeiro, G., M. Verde, M. Ubilla, and J. Ferigolo. 2003. First basal synap- nospondyls (Vertebrata: Choanata) and its implications for the
sids (‘‘pelycosaurs”) from the Upper Permian–?Lower Triassic of monophyly and origins of the Stereospondyli. Zoological Journal
Uruguay, South America. Journal of Paleontology 77:389–392. of the Linnean Society 128:77–121.
Price, L. I. 1948. Um anfíbio labirintodonte da Formação Pedra de Fogo, Zittel, K. A., von. 1887–1890. Handbuch der Palaeontologie. 1 Abt
estado do Maranhão. Boletim do Departamento Nacional de Palaeozoologie, III Band, Vertebrata (Pisces, Amphibia, Reptilia,
Produção Mineral, Divisão de Geologia e Mineralogia 124:–33. Aves). Munich and Leipzig.
Ruta, M., and J. R. Bolt. 2006. A reassessment of the temnospondyl
amphibian Perryella olsoni from the Lower Permian of Submitted July 30, 2020; revisions received November 24, 2020;
Oklahoma. Transactions of the Royal Society of Edinburgh Earth accepted January 8, 2021.
Sciences 97:113–165. Handling Editor: Adam Huttenlocker

También podría gustarte