Jurassic mammaliaform petrosals from Western Siberia (Russia) and implications for early mammalian inner-ear anatomy

Abstract

Five partially preserved mammaliaform petrosals recovered from Middle Jurassic sediments of the Berezovsk coal mine (Krasnoyarsk Krai, Russia) show similarities to other early mammaliaforms like the morganucodontan Morganucodon and the docodontan Haldanodon in having an inflated promontorium and a curved and apically inflated cochlear canal, but they are distinct from dryolestoid and derived mammalian petrosals by the weak coiling of the cochlear duct and the presence of a perilymphatic foramen with an open perilymphatic sulcus. The two larger and robust specimens exhibit striking similarities to docodontan petrosals. Inside the bone an intricate circumpromontorial venous plexus was discovered, as recently described for the docodontan Borealestes, confirming that this structure is consistently present in basal non-mammalian mammaliaforms. The three smaller and slender petrosals probably belong to haramiyidans and are unique in showing a septum-like structure medially along the cochlear nerve entrance. The protruding perforated bony bar, which is preserved in two of the three, is interpreted here to be a remnant of a bony septum with multiple foramina for cochlear nerve fibres, representing an autapomorphic feature of Haramiyida. This newly described passageway for nerve fibres shows that the formation of the osteological structure surrounding the nervous pathways of the cochlea is more plastic among the non-mammalian mammaliaforms than previously thought.

Full text

Zoological Journal of the Linnean Society, 2021, XX, 1–26. With 9 figures.
© The Author(s) 2021. Published by Oxford University Press on behalf of The Linnean Society of London.
All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 1
Jurassic mammaliaform petrosals from Western
Siberia (Russia) and implications for early mammalian
inner-ear anatomy
JULIA A. SCHULTZ1,*,, IRINA RUF2, ALEXANDER O. AVERIANOV1,3,4, RICO SCHELLHORN1,,
ALEXEY V. LOPATIN4 and THOMAS MARTIN1
1Institute of Geosciences, Section Palaeontology, Rheinische Friedrich-Wilhelms-Universität Bonn, 53115
Bonn, Germany
2Abteilung Messelforschung und Mammalogie, Senckenberg Forschungsinstitut und Naturmuseum
Frankfurt, 60325 Frankfurt am Main, Germany
3Zoological Institute, Russian Academy of Sciences, St. Petersburg 199034 Russia
4Borissiak Paleontological Institute, Russian Academy of Sciences, 117647 Moscow, Russia
Received 19 May 2021; revised 20 August 2021; accepted for publication 5 October 2021
Five partially preserved mammaliaform petrosals recovered from Middle Jurassic sediments of the Berezovsk
coal mine (Krasnoyarsk Krai, Russia) show similarities to other early mammaliaforms like the morganucodontan
Morganucodon and the docodontan Haldanodon in having an inflated promontorium and a curved and apically
inflated cochlear canal, but they are distinct from dryolestoid and derived mammalian petrosals by the weak
coiling of the cochlear duct and the presence of a perilymphatic foramen with an open perilymphatic sulcus. The
two larger and robust specimens exhibit striking similarities to docodontan petrosals. Inside the bone an intricate
circumpromontorial venous plexus was discovered, as recently described for the docodontan Borealestes, confirming
that this structure is consistently present in basal non-mammalian mammaliaforms. The three smaller and
slender petrosals probably belong to haramiyidans and are unique in showing a septum-like structure medially
along the cochlear nerve entrance. The protruding perforated bony bar, which is preserved in two of the three, is
interpreted here to be a remnant of a bony septum with multiple foramina for cochlear nerve fibres, representing an
autapomorphic feature of Haramiyida. This newly described passageway for nerve fibres shows that the formation
of the osteological structure surrounding the nervous pathways of the cochlea is more plastic among the non-
mammalian mammaliaforms than previously thought.
ADDITIONAL KEYWORDS: Docodonta – Haramiyida – inner-ear endocasts – Mammaliaformes.
INTRODUCTION
The Berezovsk coal mine near Sharypovo in Krasnoyarsk
Krai (Western Siberia, Russia) has yielded a diverse
assemblage of Middle Jurassic (Bathonian) vertebrates
(Averianov et al., 2017a). The fossil-bearing layers belong
to the upper Itat Formation and were discovered in 2000
(Averianov et al., 2005). The vertebrate fossils occur in
fluviolacustrine claystones and fine-grained sandstones
on top of a coal measure of more than 50 m thickness.
Vertebrates comprise hybodontiform sharks, dipnoans,
palaeonisciform and amiiform actinopterygians,
caudate and anuran amphibians, the cryptodiran
turtle Annemys Sukhanov & Narmandakh, 2006,
primitive lepidosauromorphs, scincomorph lizards,
choristoderes, crocodylomorphs, various ornithischian
and saurischian dinosaurs, pterosaurs, tritylodontids
and diverse non-mammalian mammaliaforms and
mammals (Alifanov et al., 2001; Averianov et al., 2005,
2008, 2010a, b, 2011, 2014, 2017a, b; 2019a, b, 2021a, b;
Lopatin & Averianov, 2005, 2007, 2009; Skutschas et al.,
2005, 2020; Averianov & Lopatin, 2006; Skutschas,
2006; Averianov & Krasnolutskii, 2009; Skutschas &
Krasnolutskii, 2011).
Several hundred mammaliaform specimens have
been recovered to date from the Bathonian Itat
Formation of the Berezovsk coal mine during a joint
*Corresponding author: e-mail: jaschultz@uni-bonn.de
applyparastyle “fig//caption/p[1]” parastyle “FigCapt”
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

2 J. A. SCHULTZ ET AL.
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
Russian–German field project in 2010–2013. This is
the second-largest Middle Jurassic mammaliaform
assemblage after that from the Bathonian Forest
Marble Formation in England (Martin et al., 2014).
The fossil remains from the Berezovsk coal mine shed
light on the diversity and disparity of mammaliaforms
during an early stage of mammalian evolution in Asia.
Isolated teeth, jaws and jaw fragments of docodontans,
haramiyidans, eutriconodontans, dryolestids and
amphitheriids were reported from this locality (e.g.
Averianov et al., 2017a). Like teeth and lower jaws, the
petrosal bone (part of the temporal bone in humans) is
more resistant to erosion than other skeletal elements,
because it is the hardest and densest bone in the
mammal body (Frisch et al., 1998). Therefore, petrosals
are frequently found isolated from the rest of the skull
in fluviolacustrine sediments.
The present study describes five mammaliaform
petrosals recovered from the Berezovsk coal mine, the first
reported from northern Asia. The knowledge of Middle
Jurassic mammaliaform petrosals is limited and we add
substantial new information on early mammaliaform ear
anatomy. If the taxonomic assignment is corroborated,
we present the first comprehensive description of the
haramiyidan inner-ear.
MATERIAL AND METHODS
Five petrosal bones (PIN 5087/37, PIN 5087/38, PIN
5087/69, PIN 5087/70 and PIN 5087/71) were found
during screen-washing operations in the Berezovsk
coal mine. The specimens come from a bone-rich
sediment layer in the upper part of the Itat Formation
yielding diverse microvertebrate remains (Averianov
et al., 2005). The petrosals were picked from the
> 2.0 mm fraction of the screen-washed clay and were
scanned with the 180 kV X-ray tube of the v|tome|x
s µCT device (GE Sensing & Inspection Technologies
GmbH phoenix|x-ray) housed in the Institute of
Geosciences, Section Palaeontology, Rheinische
Friedrich-Wilhelms-Universität Bonn, Germany (see
Table 1 for scan parameters). Produced image size
was 1024 × 1024 pixels. The µCT data were processed
with the reconstruction software datos|x rec (GE
Sensing & Inspection Technologies GmbH phoenix|x-
ray) and VG Studio Max 2.0 (Volume Graphics). For
reconstructing the inner-ear endocast AVIZO 6.3
(VSG Visualization Sciences Group, FEI Company)
was used. The dimensions of the five petrosals were
measured using a digital calliper. Additionally, linear
measurements were taken from the 3D reconstructions
using AVIZO 6.3 according to Ruf et al. (2009) and Luo
et al. (2012). All measurements are provided in Table
2. For visualization purposes, all five petrosals with
reconstructed endocasts, innervation and blood vessels
are available as 3D PDF files. The 3D PDF files were
created using DAZ studio v.4.15 and Adobe Acrobat X
Pro. The original CT image stacks and scan info sheets
for each specimen are available from digital data
repository Dryad along with 3D PDFs and STL files
(https://doi.org/10.5061/dryad.t1g1jwt2d).
In order to determine the taxonomic attribution
of the five Berezovsk petrosals, we used the classical
detailed anatomical descriptions of petrosal bones of
different Mesozoic taxa published so far. For Mesozoic
key taxa, such as Borealestes Waldman & Savage, 1972,
Dryolestes Marsh, 1878, Haldanodon Kühne & Krusat,
1972, Henkelotherium Krebs, 1991, Morganucodon
Kühne, 1949 and Sinoconodon Patterson & Olson, 1961,
we refer to the works of Kermack et al. (1981), Crompton
& Sun (1985), Crompton & Luo (1993), Ruf et al. (2009,
2013), Luo et al. (2012), Panciroli et al. (2019, 2021)
and further literature. The comparative morphological
works of Luo (2001: Yunnanodon Cui, 1986) and
Rodrigues et al. (2013: Brasilitherium Martinelli &
Schultz, 2003) were used for comparisons with non-
mammaliaform cynodont and especially tritylodontid
inner-ear morphology. For multituberculate petrosal
features we refer to Luo & Ketten (1991), Lillegraven
& Hahn (1993), Fox & Meng (1997), Hurum (1998),
Ladevèze et al. (2010) and Wible et al. (2019). For
petrosal descriptions of monotremes, stem marsupials
and placentals we follow Luo et al. (1995), Meng &
Fox (1995), Wible et al. (2001), Ekdale & Rowe (2011)
and Schultz et al. (2017). For comparative anatomy
of petrosal bones and inner-ear structures, including
vascular patterns, Rougier et al. (1992, 1996), Wible
& Hopson (1993, 1995), Harper & Rougier (2019) and
Luo & Manley (2020), among others, were consulted.
The stapedial ratio was calculated according to Segall
(1970).
Institutional abbreviation: PIN, Borissiak Paleontological
Institute, Russian Academy of Sciences, Moscow, Russia.
RESULTS
Two general morphologies can be distinguished
among the investigated petrosal bones: robust and
Table 1. Scan parameters for the five Siberian petrosals
Specimen no. kV mA Timing (ms) Resolution (µm)
PIN 5087/37 135 135 667 7.5
PIN 5087/38 120 120 400 7.9
PIN 5087/69 84 79 667 6.7
PIN 5087/70 120 120 667 9.0
PIN 5087/71 120 120 667 11.0
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

MAMMALIAFORM PETROSALS FROM SIBERIA 3
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
large (PIN 5087/38, PIN 5087/71), as well as slender
and small (PIN 5087/37, PIN 5087/69, PIN 5087/70).
Measurements on petrosals and endocasts of the bony
labyrinth are presented in Table 2.
Petrosal bone PIn 5087/71
Ventral side
Right petrosal PIN 5087/71 is the largest (~8 mm
in length, see Table 2) and most complete specimen
(Fig. 1A). It shows abraded surfaces (i.e. rounded
edges) due to fluvial transportation. Both the osseous
pars cochlearis (containing the membranous parts of
saccule and cochlea) and pars canalicularis (containing
the membranous utricle and semicircular canals) are
complete in this specimen. The inflated promontorium
has a prominent bony ridge with several circular
holes, which were caused by the abrasion during
transportation indicated by the worn and rounded
edges of the holes, but it cannot be fully ruled out
that such damage occurred during the screen-washing
process. In PIN 5087/71, the bony ridge on the
promontorium extends from the crista interfenestralis
towards the anterior end of the promontorium. The
crista interfenestralis separates the perilymphatic
foramen (ancestral structure, no bony subdivision of
the fenestra cochleae and the perilymphatic duct) and
the fenestra vestibuli. The lateral trough [the broad
concave space between the promontorium and the
lateral flange following Rougier & Wible (2006)] and
lateral flange are fully preserved. The lateral flange
bordering half of the lateral trough laterally, forms a
prominent curved wall enclosing a deep cavity lateral
to it. The cavity is best visible from the lateral view.
In the centre of this deep cavity lies the ventromedial
opening of the facial canal, identified based on the 3D
reconstruction. The canal connects to the foramen of
the facial nerve (CN VII) inside the internal acoustic
meatus (i.e. primary facial foramen) on the dorsal side
and thus transmitted the fibres of CN VII (Figs 2E, 3C).
Because the facial canal is identified inside this cavity,
the cavity must contain the cavum supracochleare.
In PIN 5087/71, the cavity is deep and channel-like,
and there are no bony crests or sulci in the walls.
We interpret that the cavum epiptericum lies dorsal
to the cavum supracochleare inside this cavity-like
configuration, and thus both spaces are confluent.
Several openings perforate the curved wall of the
lateral flange (Fig. 1A). A prominent opening for
the prootic canal (for the prootic sinus) is present
anterolateral to the fenestra vestibuli. Two openings are
evident anteromedial to the prootic canal and anterior
to the fenestra vestibuli. We interpret the one closer
to the prootic canal to have transmitted vasculature,
as is evident from a shallow sulcus in the bone
anteromedially to the opening and the connection to the
anterior transcochlear sinus [= ‘anterior epicochlear
sinus’ of Harper & Rougier (2019)] via a small canal.
The connection to the transcochlear sinus is only visible
through the 3D reconstruction of the vascular spaces
(Fig. 3A). We, therefore, identify the one closer to the
prootic canal as a vascular foramen that passes a vein
that connects to the anterior transcochlear sinus, as it
pierces through the lateral flange. The second opening
(anteromedial to the vascular foramen) is interpreted
as the secondary facial foramen, the exit for the facial
nerve to enter the lateral trough. This foramen is the
opening in the tympanic surface of the petrosal by
which the hyomandibular branch of the facial nerve
(CN VII) enters the middle-ear space from the cavum
supracochleare or cavum epiptericum [following Wible
& Rougier (2000)]. Anterior to the two openings lies
a shallow bony sulcus running in anterior direction
to meet the deep groove of the inferior ramus of the
stapedial artery on the lateral side of the anterior
end of the promontorium. The soft-tissue structure
associated with this sulcus is the inferior ramus of the
stapedial artery. The same relationship of openings
and grooves is found in specimens PIN 5087/37, PIN
5087/38 and PIN 5087/69. A small opening on the
anterior end of the lateral flange is interpreted as the
hiatus Fallopii for the greater petrosal nerve (Fig. 1A).
The mastoid region at the posterolateral margin
of the petrosal bone in PIN 5087/71 is complete and
shows a large and deep pneumatized cavity (Fig. 4D),
the mastoid pneumatic recess [following Ruf et al.
(2013)].
The stapedius muscle fossa for the origin of the
stapedius muscle sits anterolateral to the mastoid
pneumatic recess and forms a slight depression inside
the sulcus for the lateral head-vein medial to the crista
parotica (Fig. 1A). Lateral to the mastoid pneumatic
recess, the depression of the paroccipital pneumatic
recess is located. The crista parotica separates the
paroccipital pneumatic recess from the stapedius
muscle fossa anteromedially and connects to the
lateral flange forming a bridge over the broad sulcus
for the lateral head vein (Fig. 1A). The bridging forms
the large pterygoparoccipital foramen at the lateral
end of the sulcus for the lateral head-vein, marking
the entrance to a long canal (Fig. 4C).
Dorsal side
Several small nutritive foramina perforate the dorsal
side of the petrosal connecting to a fine vascular
network (Figs 1B, 3A, 4A, B). The complete internal
acoustic meatus forms a deep depression centrally
divided by the transverse crest with the typical three
large openings: the foramen for the cochlear part of
the vestibulocochlear nerve (cranial nerve [CN] VIII),
the primary foramen for the facial nerve (CN VII) and
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

4 J. A. SCHULTZ ET AL.
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
Table 2. Measurements taken on the bony labyrinth of the investigated specimens. Abbreviations: ASC anterior semicircular canal; LSC lateral semicircular
canal; PSC posterior semicircular canal
?Docodontan petrosal
PIN 5087/71
?Docodontan petrosal
PIN 5087/38
?Haramiyidan
petrosal PIN 5087/37
?Haramiyidan
petrosal PIN
5087/69
?Haramiyidan
petrosal PIN
5087/70
Max. petrosal length (mm) 7.93a7.29a6.52a- -
Max. petrosal width (mm) 5.70a5.98a4.34a- -
Promontorium lengthb (mm) 4.37a4.07a4.07a4.09a3.70a
Promontorium heightc (mm) 3.13a2.41a2.08a2.19 1.96
Promontorium width d (mm) 3.03a3.03a2.73 2.36a2.42a
Length of cochlear canal from anterior border of
fenestra vestibuli to apex (mm)
3.96 3.93 3.82a3.17 -
Length of cochlear canal from posterior border of
fenestra vestibuli to apex (mm)
5.25 5.19 4.81 3.96a-
Length of cochlear canal from anterior border of
fenestra vestibuli to apex along midline (mm)
4.26a4.45 3.93 - 4.65
Length of cochlear canal from posterior border
of fenestra vestibuli to apex along outer curva-
ture (mm)
5.31 5.75 - - 5.86
Height of cochlear canal at apical swellinge (mm) 1.06 1.29 1.06 1.01 -
Width of cochlear canal at apical swellinge (mm) 1.24 1.46 1.31 1.37a-
Area of the perilymphatic foramen (mm²) [max.
length (mm) × max. width (mm)]f
0.97 (0.93 × 1.28) 1.01 (0.97 × 1.30) 0.75 (0.78a × 1.10a) - 0.87 (0.90 × 1.20)
Area of fenestra vestibuli (mm²) [max. length
(mm) × max. width (mm)]h
0.77 (1.02a × 0.96) 1.13 (0.76a × 1.19) n. p.g (0.90a max.
width)
- 1.10 (1.29 × 1.08)
Stapedial ratio 1.06 1.02 - - 1.19
Inner height of LSC (mm) 0.75 1.15 - - 1.17
Inner width of LSC (mm) 1.02 0.94 - - 0.99
Inner height of PSC (mm) - 1.43a- - 1.66a
Inner width of PSC (mm) - - - - 1.35a
Inner radius of curvature of LSC (mm) 0.44 0.52 - - 0.54
Inner radius of curvature of PSC (mm) - - - - 0.75a
Diameter of LSC (mm)i0.33 0.56 - - 0.55
Diameter of PSC (mm)i- 0.51a- - 0.48a
Diameter of ASC (mm)i- - - - 0.34a
aMeasurement taken of incomplete/broken structures.
bMeasured from anterior border between fenestra vestibuli and perilymphatic straight to rostral apex of promontorium (not along curvature of promontorial surface).
cGreatest distance between anterior rim of internal acoustic meatus and promontorium.
dGreatest distance between medial and lateral side of promontorium, straight line.
eWidth and height approximately perpendicular.
fGreatest width measured from deepest point of perilymphatic sulcus, greatest length = perpendicular to greatest width.
gStructure not preserved.
hGreatest length = approximately anterior-posterior direction, greatest width = perpendicular to greatest lengt.
iMeasured in the plane of SC, measure point close to greatest height.
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

MAMMALIAFORM PETROSALS FROM SIBERIA 5
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
Figure 1. Virtual 3D models of ?docodontan petrosals (right side) from Berezovsk Quarry (Western Siberia, Russia). A,
ventral view of PIN 5087/71; B, dorsal view of PIN 5087/71; C, ventral view of PIN 5087/38; D, dorsal view of PIN 5087/38.
Anterior to the top. See also Supporting Information, available from digital data repository Dryad (https://doi.org/10.5061/
dryad.t1g1jwt2d). Abbreviations: basc, bony anterior semicircular canal; bpsc, bony posterior semicircular canal; ccc, canal
containing crus commune; ci, crista interfenestralis; cips, canal connecting to the inferior petrosal sinus; cp, crista parotica; cv,
canaliculus vestibuli (= bony canal for the membranous endolymphatic duct, foramen is broken); ef, endolymphatic foramen;
fcn, foramen for the cochlear nerve; fsa, fossa subarcuata; fv, fenestra vestibuli; fvn, foramen for the vestibular nerve;
hF, hiatus Fallopii; jn, jugular notch; lf, lateral flange; ?lff, possibly lateral flange foramen; lt, lateral trough; mfp, medial
flat facet of promontorium; mpr, mastoid pneumatic recess; nfa, nutritive foramina; p, promontorium; pf, perilymphatic
foramen; pff, primary facial foramen; poc, prootic canal; ppr, paroccipital pneumatic recess; ptf, pterygoparoccipital foramen;
sf, saccular foramen; sff, secondary facial foramen; sirsa, sulcus for inferior ramus of stapedial artery; slhv, sulcus for lateral
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

6 J. A. SCHULTZ ET AL.
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
the foramen for the vestibular part of CN VIII. The
latter two are lateral to the transverse crest. In PIN
5087/71, the separation between the primary foramen
for the facial nerve (CN VII) and the foramen for the
vestibular part of CN VIII is broad (Fig. 1B). The
cochlear part of CN VIII enters the petrosal through
the medially positioned single circular opening.
A small foramen occurs on the transverse crest like
in all other specimens. This foramen contained the
saccular branch of the vestibular division of the
vestibulocochlear nerve (CN VIII).
The bone posterior to the internal acoustic meatus is
broken, and this reveals the internal morphology of two
canals. This part of the petrosal normally encloses the
aquaeductus vestibuli and crus commune of the inner-
ear semicircular canal system. The visible smaller
canal enclosed the membranous endolymphatic
duct and the larger canal posterior to the smaller
one enclosed the membranous crus commune. More
posterior to the canal for the crus commune, a third
canal is visible due to the breakage, which is part
of the canal that housed the membranous posterior
semicircular duct. Lateral to the three broken canals
lies a deep and almost complete fossa subarcuata.
Petrosal bone PIn 5087/38
Ventral side
The right petrosal PIN 5087/38 is almost complete. The
promontorium is inflated and has a prominent bony
ridge that extends from the crista interfenestralis
towards the anterior end of the promontorium
(Fig. 1C). This bony ridge is largely worn away and
several holes are visible, providing a view into canals
and cavities in this highly vascularized region. The
crista interfenestralis separates the perilymphatic
foramen from the fenestra vestibuli. The area of the
perilymphatic foramen of PIN 5087/38 is larger than in
PIN 5087/71, but the area of the fenestra vestibuli is of
similar size in both specimens (Table 2). The structures
lateral to the promontorium (i.e. lateral trough and
lateral flange) are preserved mainly undamaged.
PIN 5087/38 shows a complete bony lateral flange
bordering two-thirds of the lateral trough. The rim
of the lateral flange forms a prominent swelling that
roofs a deep cavity visible in medial view (Fig. 2E). The
space of this cavity is interpreted to have contained
both the cavum supracochleare and the cavum
epiptericum, because the cavum supracochleare can
be clearly identified by the large opening of the facial
canal piercing the bony floor of this cavity. The position
of the trigeminal ganglion can be identified by a bony
crest separating the cavity posterolaterally from the
prootic region. The space of cavum epiptericum and
cavum supracochleare is confluent. Therefore, we
interpret that the trigeminal ganglion (of CN V) and
the geniculate ganglion (of CN VII) were situated
closely in living animal.
The wall of the lateral flange is perforated by
several openings (Figs 1C, 2D). The prominent prootic
canal for the prootic sinus is present anteromedial to
the fenestra vestibuli. A large, oval-shaped opening,
medial to the prootic canal and anterior to the
fenestra vestibuli, contains a passage for two adjacent
structures indicated by two grooves on the medial side
of the lateral trough. A clear bony separation inside
this oval opening is not evident. A venous vessel
leading to the inferior petrosal sinus ran through the
lateral corner of the oval opening based on a small
canal piercing through the bone in the lateral corner
of the oval opening. This canal connects to the anterior
transcochlear sinus crossing the cochlea inside the
bone. We, therefore, identify the lateral side of the oval
opening as a vascular foramen holding a venous vessel
that connects to the anterior transcochlear sinus (Fig.
2D, E). Based on the somewhat deeper second sulcus
leading from the medial corner of the oval opening, we
assume that this is the position of the secondary facial
foramen, the exit of the facial nerve to enter the lateral
trough. A similar condition is observed in PIN 5087/71
(Fig. 2D, E).
A small opening on the anteromedial wall of the
lateral flange is interpreted as the hiatus Fallopii
(Fig. 2D, E) through which the greater petrosal nerve
pierced the lateral flange. A small sulcus leads from
this opening in antero–medial direction into the
lateral trough.
The mastoid region at the posterolateral end of
PIN 5087/38 shows a deep mastoid pneumatic recess.
The stapedius muscle fossa is anterolateral to the
mastoid pneumatic recess as evident by a round
rugosity on the surface of the sulcus for the lateral
head vein (Figs 1C, 2D). A shallow groove lateral to
the mastoid pneumatic recess forms the paroccipital
pneumatic recess. The crista parotica separates the
paroccipital pneumatic recess from the stapedius
muscle fossa anteromedially (Figs 1C, 2D). The crista
parotica limiting the paroccipital pneumatic recess
anteromedially is separated from the paroccipital
process and lateral flange by the broad channel-like
sulcus for the lateral head vein. A well-defined notch
between the paroccipital process and the posterior
head vein; smf, stapedius muscle fossa; spd, sulcus for perilymphatic duct; ssb, sulcus for saccular branch; tc, transverse
crest; waa, broken wall of ampulla of anterior semicircular canal; vf atcs, vascular foramen for the venous vessel connecting
to anterior transcochlear sinus.
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

MAMMALIAFORM PETROSALS FROM SIBERIA 7
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
Figure 2. Detailed anatomy of the lateral trough area of three right petrosals based on virtual 3D surface models. A,
?haramiyidan petrosal PIN 5087/37 ventrolateral view; B, ?haramiyidan petrosal PIN 5087/37 lateral view; C, ?haramiyidan
petrosal PIN 5087/69 ventrolateral view; in comparison to: D, ?docodontan petrosal PIN 5087/38 ventrolateral view; E,
?docodontan petrosal PIN 5087/38 lateral view. Anterior to the top. Scalebars equal 1 mm. Red areas mark broken edges
of the lateral flange. Abbreviations: atcsf, foramen leading to anterior transcochlear [= ‘epicochlear’ of Harper & Rougier
(2019)] sinus; cep, cavum epiptericum; ci, crista interfenestralis; cp, crista parotica; csc, cavum supracochleare; fc, facial
canal; fv, fenestra vestibuli; hF, hiatus Fallopii; jn, jugular notch; lf, lateral flange; mpr, mastoid pneumatic recess; poc,
prootic canal; ppr, paroccipital pneumatic recess; ptcsf, foramen leading to posterior transcochlear [= ‘epicochlear’ of Harper
& Rougier (2019)] sinus; ptf, pterygoparoccipital foramen; sff, secondary facial foramen; sirsa, sulcus for inferior ramus of
stapedial artery; slhv, sulcus for the lateral head vein; smf, stapedius muscle fossa; vf atcs, vascular foramen for venous
vessel connecting to the anterior transcochlear sinus.
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

8 J. A. SCHULTZ ET AL.
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
Figure 3. Reconstruction of the vascularization of the Berezovsk petrosals with inner ear endocasts (magenta), innervation
(yellow) and venous system (blue) inside translucent petrosal bone. A, dorsal view of ?docodontan petrosal PIN 5087/71;
B, dorsal view of ?docodontan petrosal PIN 5087/38; C, dorsal view of ?haramiyidan petrosal PIN 5087/37; D, detailed
internal acoustic meatus of (1) PIN 5087/38, (2) PIN 5087/71 and (3) PIN 5087/37; E, ventral view of ?docodontan petrosal
PIN 5087/38; F, dorsal view of ?haramiyidan petrosal PIN 5087/70; G, dorsal view of ?haramiyidan petrosal PIN 5087/69;
H, inner-ear endocast of the extant monotreme Ornithorhynchus without petrosal, endocast in grey, innervation in yellow
[modified from Schultz et al. (2017)]. Anterior to the top. Not to scale. See also Supporting Information, available from
digital data repository Dryad (https://doi.org/10.5061/dryad.t1g1jwt2d). Abbreviations: ats, anterior transcochlear sinus; cb,
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

MAMMALIAFORM PETROSALS FROM SIBERIA 9
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
Figure 4. µCT slices (A–D) through the ?docodontan petrosal PIN 5087/71. Orientation for virtual petrosal in left column
is anterior to the top. Orientation of µCT images is indicated on the left upper petrosal; dorsal to the top. Abbreviations:
apsc, ampulla of posterior semicircular canal; ats, anterior transcochlear sinus; cc, crus commune; cca, cochlear canal; ci,
crista interfenestralis; cnc, cochlear nerve canal; ec, endolymphatic canal; fv, fenestra vestibuli; ips, inferior petrosal sinus;
mpr, mastoid pneumatic recess; pf, perilymphatic foramen; poc, prootic canal; ptf, pterygoparoccipital foramen; spd, sulcus
for perilymphatic duct; v, vestibule.
cochlear branch on CN VIII; ccp, circumpromontorial sinus; fn, facial nerve; ips, inferior petrosal sinus; lag, lagenar branch
of CN VIII; pts, posterior transcochlear sinus; sb, saccular branch of CN VIII; uab, utriculo-ampullar branch of CN VIII.
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

10 J. A. SCHULTZ ET AL.
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
end of the lateral flange forms a partially open
pterygoparoccipital foramen in PIN 5087/38, which in
comparison is a fully closed foramen in specimen PIN
5087/71 (compare Fig. 1A and C).
Dorsal side
On the dorsal side, which forms the ventral floor of
the braincase, specimen PIN5087/38 shows several
small nutritive foramina, which lead into the
cochlear canal of the bony labyrinth (Fig. 1D). The
internal acoustic meatus is complete, showing three
large openings [foramen for the cochlear part of the
vestibulocochlear nerve (CN VIII), primary foramen
for the facial nerve (CN VII), foramen for the
vestibular part of CN VIII] divided by the transverse
crest (Fig. 1D). The latter two are lying in the deeper
part of the depression formed by one anterolaterally
directed foramen that divides into two canals. The
cochlear part of CN VIII enters the petrosal trough
the large opening positioned posteromedially from
the transverse crest. A small foramen pierces the
transverse crest which contained the saccular branch
of the vestibular division of vestibulocochlear nerve
(CN VIII).
Posterolateral to the internal acoustic meatus, two
confluent holes are visible, of which the posterior one
is much larger. These two holes are artificial due to
breakage of the posterolateral part of the petrosal
bone. The larger one enclosed the crus commune of the
inner-ear semicircular canal system, while the smaller
one represents the bony canal for the endolymphatic
duct (Fig. 1D). Posterolateral to the latter canal there
is a second hole, which represents the anterior part
of the broken posterior semicircular canal. The fossa
subarcuata, although incomplete, forms a deep cavity.
On the anteromedial margin of the petrosal a canal is
found also due to breakage, where the tributary canals
of the inferior petrosal sinus are visible that run inside
the petrosal bone near the cochlear apex.
Petrosal bone PIn 5087/37
Ventral side
The osseous pars cochlearis of the left petrosal bone
is almost complete in specimen PIN 5087/37, whereas
the osseous pars canalicularis lacks the parts that
enclose the anterior and posterior semicircular canals
due to breakage (Fig. 5A). From the µCT slices it is
obvious that the bone surrounding the cochlear canal
is strongly vascularized like in PIN 5087/71. The
promontorium is an inflated and elongated prominent
bulging on the ventral aspect of the petrosal.
A prominent bony ridge extends along half of the
anteroposterior length of the promontorium towards
the anterior end of the promontorium (Fig. 5A).
A bony groove extends along the anterior part of the
promontorium on the lateral side, parallel to the bony
ridge. This groove was probaby occupied by the inferior
ramus of the stapedial artery in the living animal.
A slender, bony crista interfenestralis separates the
fenestra vestibuli and the perilymphatic foramen;
the presence of a perilymphatic duct is indicated by the
bony sulcus in the posteromedial wall of the foramen
and no bony separation to the fenestra cochleae exists.
The perilymphatic duct leads to the anterior margin of
the jugular foramen.
The lateral trough, spread antero–laterally along
the promontorium, is only partly preserved in this
specimen. The lateral flange, which formed the
lateral border of the lateral trough, is broken; it
separated the space that enclosed the confluent cavum
supracochleare and cavum epiptericum, the former
space housing the geniculate and trigeminal ganglia
and blood vessels. In this area, several openings for
blood supply and innervation are preserved, although
incomplete due to the broken lateral flange. A shallow,
broken, bony ridge indicates a bony separation of the
prootic canal (holding the prootic sinus) and a vascular
foramen for a venous vessel that connected to the
anterior transcochlear sinus anterior to the fenestra
vestibuli (Fig. 2A, B). In PIN 5087/37, three further
openings are identifiable anteromedial to the prootic
canal (Fig. 5A): (1) the opening directly medial to the
prootic canal is for a venous vessel, evident by an
intraosseous connection to the posterior transcochlear
sinus via the small canal leading in dorsal direction, (2)
medial to the opening of the venous vessel connecting
to the posterior transcochlear sinus sits the secondary
facial foramen located in the anterior part of the lateral
flange, which separates the cavum supracochleare
from the lateral trough, and (3) the small opening in
the lateral flange anteromedially from the secondary
facial foramen is the hiatus Fallopii (for the greater
petrosal nerve).
The mastoid region at the posterior end of the
petrosal bone shows a large and deep pneumatized
cavity, the mastoid pneumatic recess (Fig. 5A). The
stapedius muscle fossa is the shallow, oval-shaped
depression with a rugose surface anterolateral to the
mastoid pneumatic recess, sitting inside the broad
sulcus for the lateral head vein. A small depression
lateral to the mastoid pneumatic recess forms the
paroccipital pneumatic recess. A bony crest separates
the paroccipital pneumatic recess anteromedially from
the stapedius muscle fossa (Fig. 5A). We identify this
crest as part of the crista parotica, which continues
in antero–lateral direction and borders the sulcus for
the lateral head vein. The petrosal is broken along
the posterolateral end and the crista parotica is
incomplete.
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

MAMMALIAFORM PETROSALS FROM SIBERIA 11
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
Figure 5. Virtual 3D models of ?haramiyidan petrosals (right side) from Berezovsk Quarry (Western Siberia, Russia). A,
ventral view of PIN 5087/37; B, dorsal view of PIN 5087/37; C, ventral view of PIN 5087/69; D, dorsal view of PIN 5087/69.
Anterior to the top. See also Supporting Information, available from digital data repository Dryad (https://doi.org/10.5061/
dryad.t1g1jwt2d). Abbreviations: ccc canal containing crus commune; ci, crista interfenestralis; cips, canal connecting to the
inferior petrosal sinus; cnf, cochlear nerve fibre foramina; cp, crista parotica; ef, endolymphatic foramen; fcn, foramen for
the cochlear nerve; fsa, fossa subarcuata; fv, fenestra vestibuli; fvn, foramen for the vestibular nerve; hF, hiatus Fallopii;
jn, jugular notch; lf, lateral flange; lt, lateral trough; mfp, medial flat facet of promontorium; mpr, mastoid pneumatic
rescess; nfa, nutritive foramina; p, promontorium; pf, perilymphatic foramen; pff, primary facial foramen; ?poc, potential
remnant of prootic canal; ppr, paroccipital pneumatic recess; ptcsf, posterior transcochlear sinus foramen; ?ptf, potential
pterygoparoccipital foramen; sf, saccular foramen; sff, secondary facial foramen; sirsa, sulcus for inferior ramus of stapedial
artery; slhv, sulcus for lateral head vein; smf, stapedius muscle fossa; spd, sulcus for perilymphatic duct; tc, transverse crest;
vf atcs, vascular foramen for venous vessel connecting to anterior transcochlear sinus.
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

12 J. A. SCHULTZ ET AL.
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
Dorsal side
At the posterolateral end of PIN 5087/37 the fossa
subarcuata is broken and the anteromedial border
of PIN 5087/37 is less complete on the dorsal side
than in both PIN 5087/38 and PIN 5087/71 (compare
Fig. 5B with Fig. 1A, C). PIN 5087/37 shows several
small nutritive foramina and a fine intraosseous
network for blood supply of the cochlear duct inside
the bony labyrinth, which are also present in all other
specimens, except PIN 5087/70. The fully preserved
internal acoustic meatus forms a depression centrally
divided by the transverse crest. The three typical large
openings occur: the foramen for the cochlear branch
of the vestibulocochlear nerve (CN VIII), the foramen
for the vestibular branch of CN VIII and the primary
facial foramen for CN VII leading into the facial canal
(Fig. 5B). The foramen for the vestibular branch of
CN VIII and the primary facial foramen are lying
in the deeper part of the depression anterolateral
to the larger foramen for the cochlear branch of the
vestibulocochlear nerve (CN VIII). The posteromedial
rim of the oval foramen for the cochlear branch of
CN VIII appears irregular by a series of tiny, broken,
bony crests, suggesting the presence of a row of small
foramina in this region (Figs 5B, 6A). In comparison,
the lateral rim of that foramen is a straight line.
A bony sulcus opens into a small foramen on the
transverse crest, the entrance for the saccular branch
of the vestibular division of vestibulocochlear nerve
(CN VIII).
Figure 6. Virtual horizontal cut through the three ?haramiyidan promontoria, specimens PIN 5087/37 (A), PIN 5087/69
(B), and PIN 5087/70 (C). Remnants of a bony bar on the medial side of the cochlear nerve foramen are visible in each
specimen inside the cochlear canal (indicated by black arrow heads). White rectangle in B depicts area seen close up in D,
light source was virtually adjusted in D to make the sulci visible. E, reconstruction of the perforated bony bar with single
cochlear nerve fibres (yellow) piercing through; number of holes random and only for illustration purpose. Anterior to the
top, not to scale.
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

MAMMALIAFORM PETROSALS FROM SIBERIA 13
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
At the posterior end PIN 5087/37 is broken, revealing
parts of the inner morphology of the pars canalicularis,
such as the visible canal that normally encloses the
crus commune of the membranous semicircular duct
system. Anterior to that lies the smaller endolymphatic
foramen.
Petrosal bone PIn 5087/69
Ventral side
The pars canalicularis of right petrosal PIN 5087/69
is broken off and the general morphology of the pars
cochlearis of the petrosal resembles specimen PIN
5087/37 (Figs 5C, D, 6). Like in the other petrosals,
PIN 5087/69 shows strong vascularization around the
cochlear canal and an intraosseous network of vessels.
On the ventral side, a similar prominent bony ridge is
present in the middle of the inflated and elongated
promontorium, like in the aforementioned specimens.
However, the orientation of this ridge is different. In
PIN 5087/37, PIN 5087/38 and PIN 5087/71, the ridge
extends from the crista interfenestralis towards the
anterior end of the promontorium. In PIN 5087/69, the
ridge is more transverse and almost perpendicular to
the promontorium longitudinal axis. Laterally, the bony
groove for the inferior ramus of the stapedial artery
extends along the anterior part of the promontorium
like in specimen PIN 5087/37. The crista interfenestralis,
separating the perilymphatic foramen from the fenestra
vestibuli, is partially broken and displaced. The crista is
broader than in specimen PIN 5087/37, but more slender
than in specimen PIN 5087/38. The posterior edge of
the perilymphatic foramen is broken, but recognizable
by the bony sulcus for the perilymphatic duct on the
posteromedial floor. The lateral flange is severely
damaged, only shallow, broken, bony edges mark the
former area containing the cavum epiptericum and cavum
supracochleare, but several openings are recognizable.
Identification of the opening remains difficult, but by
comparison to the more complete specimens we identify
the openings as follows (but some with a question mark):
(1) the ?prootic canal lies in close proximity and anterior
to the fenestra vestibuli, (2) anteromedially to that lies
the secondary facial foramen, a sulcus indicates the
exit of the facial nerve to enter the lateral trough, (3)
an opening anterolateral to that sulcus connects to the
anterior transcochlear sinus internally and thus forms a
foramen for the vascular system and (4) a small opening
perforating the anterior part of the broken lateral flange
in the lateral most corner is the ?hiatus Fallopii.
Dorsal side
On the dorsal side, specimen PIN 5087/69 shows
several small nutritive foramina (Fig. 5D), which
lead to the cochlear canal of the bony labyrinth,
forming a fine intraosseous vascular network. The
internal acoustic meatus is complete and forms a deep
depression centrally divided by the transverse crest,
with the typical three large foramina: medially, one
for transmitting the cochlear part of vestibulocochlear
nerve (CN VIII) and, laterally, the primary facial
foramen for CN VII and the foramen for the vestibular
part of vestibulocochlear nerve (CN VIII). Medially,
inside the foramen for the cochlear part of CN VIII,
a remnant of a thin, perforated, bony bar and several
grooves are visible, suggesting the presence of some
kind of bony supporting structure for cochlear nerve
fibres (Fig. 5B, D). The foramen for the cochlear part of
CN VIII is round and smaller compared to PIN 5087/37,
PIN 5087/38 and PIN 5087/70, but PIN 5087/71 has a
similar small round foramen for the cochlear part of
CN VIII like PIN 5087/69. A small foramen pierces the
transverse crest like in all other specimens, marking
the entrance for the saccular branch of the vestibular
division of vestibulocochlear nerve (CN VIII).
Posterolateral to the internal acoustic meatus, two
adjacent partly preserved openings are visible right in
the broken edge of the petrosal, of which the posterior is
much larger (Fig. 5D). The larger one enclosed the crus
commune of the inner-ear semicircular canal system,
while the smaller one is the broken endolymphatic
foramen. On the anteromedial end of the petrosal, a
broken canal represents the entrance of the tributary
vessel of the inferior petrosal sinus into the petrosal
near the cochlear apex.
Petrosal bone PIn 5087/70
Ventral side
Only the bony housing of the cochlear canal is
preserved in the right petrosal PIN 5087/70 (Fig. 7A).
This part of the petrosal is cancellous, but not to the
degree as in the other specimens. The bone appears
more compact in the µCT slices (Fig. 7C–E). It is not
clear from the µCT scans if the large circular opening
on the anterior part of the promontorium is artificial
or an anatomical feature. Specimen PIN 5087/70
shares the bony ridge on the promontorium that is
also present in the other Berezovsk specimens, but is
unique in having a sharp edge leading to the anterior
tip. Like in specimens PIN 5087/37 and PIN 5087/69,
the bony ridge stands slightly oblique to the crista
interfenestralis. The crista interfenestralis itself is
not preserved in PIN 5087/70. Only the anterior edge
of the fenestra vestibuli is preserved. Most of the
posterior part of the perilymphatic foramen is lost due
to breakage, but the foramen is recognizable by the
deep, bony imprint of a sulcus for the perilymphatic
duct on the posteromedial floor.
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

14 J. A. SCHULTZ ET AL.
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
The lateral flange and most parts of the lateral
trough are severely broken, but some openings are
recognizable. Strikingly, a bony sulcus extends from a
large opening in anterior direction along what is left
of the lateral trough. 3D-renderings of the µCT scans
reveal that, posteriorly, this sulcus connects to an
opening that leads into the cavity that contained both
the cavum epiptericum and cavum supracochleare.
Figure 7. The ?haramiyidan petrosal PIN 5087/70 (left side) from Berezovsk Quarry (Western Siberia, Russia). Virtual
3D model in: A, ventral view; B, dorsal view; C–E, µCT images illustrating the perforated bony bar inside the cochlear
nerve foramen. Anterior to the top. Scale bars in µCT images equal 1 mm. See also Supporting Information, available from
digital data repository Dryad (https://doi.org/10.5061/dryad.t1g1jwt2d). Abbreviations: cca, cochlear canal; cnc, cochlear
nerve canal; cnf, cochlear nerve foramina; fcn, foramen for the cochlear nerve; fv, fenestra vestibuli; fvn, foramen for the
vestibular nerve; hF, hiatus Fallopii; irsaf, inferior ramus of stapedial artery foramen; lf, lateral flange; mfp, medial flat facet
of promontorium; pff, primary facial foramen; poc, prootic canal; sf, saccular foramen; sff, secondary facial foramen; vf atcs,
vascular foramen for venous vessel connecting to anterior transcochlear sinus.
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

MAMMALIAFORM PETROSALS FROM SIBERIA 15
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
This opening is interpreted to be the secondary facial
foramen that transmitted the facial nerve (CN VII).
As in all other specimens, the cavum epiptericum and
cavum supracochleare lie in close proximity inside
a deep cavity lateral to the lateral trough. Medial to
the bony sulcus inside the lateral trough lies a second
shallow, bony sulcus running in anterior direction and
coming from a small foramen that we interpret as the
hiatus Fallopii, the exit for the greater petrosal nerve.
The prootic canal lies anterior to the fenestra
vestibuli, like in the other four specimens, but its
natural periosteal surface is broken off. The open canal
is partially hidden in ventral view by a protruding
piece of bone on the medial side, as a result of the
breakage (Fig. 7A). The lateral flange covering the
cavity holding both the cavum epiptericum and cavum
supracochleare is completely broken off and only
shallow, irregular bone ridges mark the former area
of the cavity.
Medially from the broken prootic canal, two
openings share one oval orifice. Inside this oval space
in the anteromedial corner runs a canal connecting to
both the anterior transcochlear sinus and the inferior
petrosal sinus. The second opening is not clearly
identifiable, but is also a possible position of the
secondary facial foramen.
Dorsal side
The internal acoustic meatus is visible on the dorsal
side, but the surrounding bone does not show the
typical small nutritive foramina like in PIN 5087/38
or PIN 5087/71 (compare Fig. 1B, C with Fig. 7B) and
is less vascularized, as mentioned above. The internal
acoustic meatus forms a deep depression, which is
centrally divided by the transverse crest. As in all
other specimens, three large openings are visible: the
foramen for the cochlear part of vestibulocochlear
nerve (CN VIII) on the medial side of the transverse
crest, the primary facial foramen for CN VII and the
foramen for the vestibular part of CN VIII on the
lateral side. Strikingly, the foramen for the cochlear
part of CN VIII is long and oval-shaped and extends
in anterior direction. Inside this oval opening a thin,
bony lamella is visible that forms a thin, irregular bony
bar (Figs 6C, 7B). From the µCT scans it is evident
that this bony bar is perforated by channels leading
into the cochlear canal (Fig. 7C–E). The bony bar is
medially fused with the petrosal bone (Figs 6C, 7C).
The facial nerve (CN VII) and the vestibular part
of CN VIII enter the petrosal through the rounded
opening lateral to the transverse crest. This deep
depression divides into two canals. A small foramen
on the transverse crest occurs like in the other four
petrosals, which contained the saccular branch of the
vestibular division of vestibulocochlear nerve (CN VIII).
reconstructed endocasts of bony labyrInths
Specimens PIN 5087/37, PIN 5087/38 and PIN
5087/71 show almost fully preserved cochlear canals
and vestibules (sacculus and utriculus), but parts of
the semicircular canal systems are broken. Specimens
PIN 5087/69 and PIN 5087/70 lack most of the
vestibule and only the cochlear canal is fully preserved
(Fig. 8). In PIN 5087/38 and PIN 5087/71, the lateral
semicircular canal and the base of the anterior and
posterior semicircular canals, including the associated
ampullae, are preserved. PIN 5087/37 shows a partly
preserved anterior ampulla. In the three specimen
with parts of the vestibule preserved, the base of the
common crus and the aquaeductus vestibuli for the
ductus endolymphaticus are preserved. The endocasts
of these three almost complete specimens have a
secondary crus commune formed by the fusion of the
posterior arm of the lateral semicircular canal and the
inferior arm and ampulla of the posterior semicircular
canal. In all three reconstructed bony labyrinths, the
three ampullae of the semicircular canal system are
prominent structures of approximately similar size.
The semicircular canals, as far as preserved, of PIN
5087/38 are stouter than those of PIN 5087/37 and
PIN 5087/71 with a larger diameter (Table 2) and an
oval-shaped cross-section. In comparison, both PIN
5087/37 and PIN 5087/71 show a rounded cross-section
of the semicircular canals. Anterior to the canaliculus
vestibuli lies a short canal for the vestibular part of
CN VIII (i.e. utriculo-ampullar branch) that enters the
vestibule to innervate the sensory fields of the utricle
(Figs 3A, C, D, F, G, 8).
The reconstructed endocasts of the bony cochlear
canal of specimens PIN 5087/37, PIN 5087/38, PIN
5087/69 and PIN 5087/71 indicate a curved cochlear
duct with a curvature of up to 180° and an oval-shaped
cross-section (width greater than height, see Table 2).
All reconstructed cochlear canals show a distinct
swelling of the most apical part of the cochlear duct,
but a bony canal for the lagenar nerve is not present.
However, specimens PIN 5087/69 and PIN 5087/71
show a sulcus running from the cochlear nerve foramen
in apical direction that might have housed the lagenar
nerve.
DISCUSSION
The non-mammalian mammaliaform and mammal
remains so far reported from the Berezovsk coal
mine comprise the docodontans Hutegotherium
yaomingi Averianov et al., 2010, Itatodon tatarinovi
Lopatin & Averianov, 2005 and Simpsonodon
sibiricus Averianov et al., 2010, the haramiyidans
Maiopatagium sibiricum Averianov et al., 2019,
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

16 J. A. SCHULTZ ET AL.
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
Sharypovoia arimasporum Averianov et al., 2019 and
S. magna Averianov et al., 2019, the eleutherodontid
‘Sineleutherus’ issedonicus Averianov et al., 2011 and
one unidentified amphilestid-grade eutriconodontan,
the multituberculates Tagaria antiqua Averianov
et al., 2020, Tashtykia primaeva Averianov et al. ,
2020 and two multituberculates incertae sedis, as well
as two cladotherians, the dryolestid Anthracolestes
sergeii Averianov et al., 2014 and the amphitheriid
Amphibetulimus krasnolutskii Lopatin & Averianov,
2007 (Averianov et al., 2005, 2010b, 2011, 2014, 2019b;
Averianov & Lopatin, 2006). In addition, isolated
postcanine teeth of the tritylodontid Stereognathus
sp. have been reported from the Berezovsk coal mine
(Averianov et al., 2017b). We tentatively assign the
two larger and more robust Berezovsk petrosals, PIN
Figure 8. Dorsal view of the reconstructed inner ear endocasts of the Berezovsk petrosals. A, ?docodontan petrosal PIN
5087/71. B, ?docodontan petrosal PIN 5087/38; C, ?haramiyidan petrosal PIN 5087/37; D, ?haramiyidan petrosal PIN
5087/69; E, ?haramiyidan petrosal PIN 5087/70. Anterior to the top, scalebars equal 1 mm. See also Supporting Information,
available from digital data repository Dryad (https://doi.org/10.5061/dryad.t1g1jwt2d). Abbreviations: aasc, ampulla of the
anterior semicircular canal; alsc, ampulla of the lateral semicircular canal; apsc, ampulla of the posterior semicircular
canal; asc, anterior semicircular canal; bpa CN VIII, branch for posterior ampulla of CN VIII; cc, crus commune; cp CN
VIII, cochlear part of CN VIII; ed, endolymphatic duct; fn CN VII, facial nerve; icca, inflated cochlear canal apex; lsc, lateral
semicircular canal; psc, posterior semicircular canal; sb CN VIII, saccular branch of CN VIII; scc, secondary crus commune;
vp CN VIII, vestibular (utriculo-ampullar) part of CN VIII.
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

MAMMALIAFORM PETROSALS FROM SIBERIA 17
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
5087/38 and PIN 5087/71, to Docodonta and the three
smaller petrosals, PIN 5087/37, PIN 5087/69 and PIN
5087/70, to Haramiyida based on anatomical features
and because docodontan and haramiyidan jaws and
teeth are the most abundant mammaliaform fossil
remains in the Berezovsk locality.
The inner-ear bony housing of tritylodontids is
derived compared to other non-mammaliaform
cynodonts in that the periotic bones (prootic and
opisthotic) are fused (Rowe, 1988; Luo, 2001).
Important to note is that in the non-mammaliaform
cynodont Brasilitherium riograndensis Martinelli
& Schultz, 2003 the periotic bones are also fused
forming a bony housing of the inner ear (Rodrigues
et al., 2013). Rodrigues et al. (2013) report an inflated
promontorium for the brasilodontid cynodont
Brasilitherium riograndensis similar to that of
the tritylodontid Yunnanodon, but less inflated
than in the morganucodontan Morganucodon.
In all Berezovsk specimens the promontorium is
more inflated than in Morganucodon [compare
Morganucodon promontorium in Kermack et al.
(1981)] and do not resemble a non-mammaliaform
cynodont condition like present in Brasilitherium or
the tritylodont Yunnanodon. Therefore, it is unlikely
that the Berezovsk petrosals belong to a tritylodontid
or brasilodontid cynodont.
A bony ridge, as seen on the ventral side of the
promontoria of all known Berezovsk petrosals,
has also been reported for the docodontan
Borealestes (Panciroli et al., 2019) and is evident
on the promontorium of the haramiyidan
Arboroharamiya Zheng et al., 2013 (Han et al.,
2017: extended data fig. 5). The three smaller
?haramiyidan specimens from Berezovsk show
a flattened bone surface on the medioposterior
side of the promontorium limited laterally by the
bony ridge, a basal feature that has also been
described for the morganucodontan Sinoconodon
and docodontan Haldanodon [i.e. medial flat facet
of the promontorium in Luo et al. (1995, and Ruf
et al. (2013)]. In the crushed but well-preserved
basicranium of the eleutherodont haramiyidan
Vilevolodon Luo et al., 2017, one petrosal is
preserved, and structures resembling the bony
ridge and a medio-posteriorly flattened surface
like in the ?haramiyidan petrosals from Berezovsk
can be observed (see Luo et al., 2017: extended
data fig. 2d, e). The fossil record for haramiyidan
petrosals and inner-ear endocasts is limited, and
detailed descriptions of anatomical features are
scarce. However, Han et al. (2017) provided a
photograph and a computed laminography image
of the petrosal of Arboroharamiya allinhopsoni
Han et al., 2017 from which it is evident that
the promontorium of this taxon has a bony ridge
perpendicular to the crista interfenestralis similar
to that of PIN 5087/69 and PIN 5087/70.
Lillegraven & Hahn (1993) reported a strong ‘rib’ of
bone extending antero–laterally along a paulchoffatid
multituberculate promontorium, which they termed
‘processus promontorii’. The bony ridge of the
Berezovsk specimens is distinct in its centred position
and bulbous shape at the posterior end. In this feature,
the petrosals tentatively assigned here to docodontans
and haramiyidans are different from the promontoria
of paulchoffatiid multituberculates.
The inner ears of djadochtatherioid multituber-
culates Nemegtbaatar Kielan-Jaworowska, 1974
and cf. Tombaatar Rougier et al., 1997 differ
fundamentally from the Berezovsk specimens by their
slender cochlear canal and the proportions of the pars
canalicularis and pars cochlearis. The slender anterior
and posterior semicircular canals of cf. Tombaatar sp.
are elongated in postero–lateral and dorsal direction
with a larger height, giving the pars canalicularis a
high and slim appearance (Ladevèze et al., 2010).
Nemegtbaatar in comparison has a slim cochlear
canal like cf. Tombaatar sp., but the proportion of the
pars canalicularis is larger than the pars cochlearis
(Hurum, 1998). Inflated vestibules are reported from
the taeniolabidid multituberculates Lambdopsalis
Chow & Qi, 1978, ?Catopsalis Cope, 1884 and
Meniscoessus Cope, 1882 (Miao, 1988; Luo & Ketten,
1991; Meng & Wyss, 1995; Luo et al., 2016: fig. 6.9K),
which is not the case in the Berezovsk specimens.
Inflated vestibules are mostly known from fossorial
animals and are considered to be an adaptation to
low-frequency hearing via bone conduction (e.g. Lewis
& Narins, 1985; Wever, 1985; Kearney et al., 2005).
Luo & Ketten (1991) have suggested that inflated
vestibules are synapomorphic for Multituberculata,
but Fox & Meng (1997) and Ladevèze et al. (2010)
have concluded that this feature evolved in different
lineages of Multituberculata independently. Ladevèze
et al. (2010) based their conclusion on the finding that
the vestibule of cf. Tombaatar sp. is not larger than
that of other mammals, but Laaß (2015) found large
variations in vestibule volumes of multituberculates,
and all of them were larger than those of other
mammals that were investigated, including cf.
Tombaatar sp. However, Hurum (1998) describes the
vestibule of Nemegtbaatar as small and not much
expanded, but mentions that it is still larger than
that of monotremes, and Wible & Rougier (2000) state
that there is no evidence of vestibular inflation for
Kryptobaatar Kielan-Jaworowska, 1970.
Most derived multituberculates have a significantly
enlarged lateral flange that overlaps the lateral
trough to contact the promontorium medially (Wible &
Rougier, 2000; Kielan-Jaworowska et al., 2005; Rougier
& Wible, 2006; Wible et al., 2019). The lateral flange is
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

18 J. A. SCHULTZ ET AL.
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
fully preserved in Berezovsk specimens PIN 5087/38
and PIN 5087/71 only. In both, the flange is short and
forms a cavity overlapping a laterally situated area
that is occupied by the cavum epiptericum and cavum
supracochleare, which is fundamentally different
from the multituberculate condition. However, the
knowledge of the inner ear and petrosal morphology
of early multituberculates is limited, and from the
few things that are known, the Berezovsk petrosals
share features with early mulituberculates like the
presence of the bony ridge on the ventral surface of
the promontorium. Hahn (1988) described the lateral
flange of European paulchoffatiid multituberculates
as well raised at its posterior end and flattened
anteriorly, which is the case for both PIN 5087/38 and
PIN 5087/71, whereas the lateral flange appears much
shorter in the other Berezovsk specimens. In addition,
Lillegraven & Hahn (1993) reported a deep and
extensive subarcuate fossa in several paulchoffatid
multituberculate petrosals, which is also the case in
specimens PIN 5087/38 and PIN 5087/71. Although
some multituberculate incisors, premolars and molars
of two taxa are known from the Berezovsk coal mine
(Averianov et al., 2017a, 2021b), the majority of
features that the petrosals from Berezovsk show do
not fit a multituberculate origin.
The Berezovsk specimens PIN 5087/37, PIN
5087/38 and PIN 5087/71 show circular fenestrae
vestibuli reflected by stapedial ratios ranging near 1
(Table 2). However, note that in PIN 5087/37 a small
section of the anterior rim and in PIN 5087/38 a small
section of the medial rim of the fenestra vestibuli are
broken. The stapedial ratios for both PIN 5087/69
and PIN 5087/70 are not determinable, because the
posterior rim of the fenestra vestibuli is not preserved.
A circular or slightly elliptical shape of the fenestra
vestibuli is common for Mesozoic mammaliaforms and,
as a general rule, the shape becomes progressively
more oval in more derived groups (Rougier & Wible,
2006). An almost circular fenestra vestibuli has been
inferred for the docodontan Haldanodon exspectatus
Kühne & Krusat, 1972 by the shape of the stapedial
footplate (Ruf et al., 2013). However, some early taxa
also show oval fenestrae vestibuli. For example, the
Early Cretaceous eutriconodontan Chaoyangodens
lii Hou & Meng, 2014 shows a unique massive stapes
with an elongate oval stapedial footplate (Meng &
Hou, 2016), thus the shape of the fenestra vestibuli
(although not described) must have been different from
that of the Berezovsk petrosals and other Mesozoic
mammaliaforms. The stapes of two species of the
euharamiyidan Arboroharamiya is well known, but
the exact shape of the footplate is only inferred from
the shape and size of the fenestra vestibuli, which is
oval in both species (Han et al., 2017; Meng et al., 2018,
2020). Multituberculates, in general, appear to have
circular fenestrae vestibuli, as evidenced by either
the preserved stapes or the shape of the fenestrae
vestibuli themselves (Wible, 1990; Meng, 1992; Fox &
Meng, 1997). However, Schultz et al. (2018) reported
an elliptical stapedial footplate and, therefore, an
elliptical fenestra vestibuli (ratio 1.5) for the Jurassic
multituberculate Pseudobolodon oreas Hahn, 1977.
For some Cretaceous multituberculates, stapedial
ratios are reported indicating a general slightly
elliptical to elliptical pattern for the footplate of the
stapes in this group (e.g. Kryptobaatar 1.39 Wible &
Rougier, 2000; cf. Tombaatar sp. 1.13, Ladevèze et al.,
2010; Mangasbaatar 1.3, Rougier et al., 2016). It
is important to note that the stapedial ratio for the
Jurassic cladotherian Dryolestes leiriensis Martin,
1999 was reported to be 1.3 with a more or less circular
fenestra vestibuli when seen in straight ventral view
(Luo et al., 2012). The ratio was later revised to 1.13
(Hughes et al., 2015). A nearly circular fenestra
vestibuli has also been described for the Miocene
cladotherian Necrolestes patagonensis Ameghino,
1891 (Rougier et al., 2012). In extant monotremes the
shape of the fenestra vestibuli is circular, but shape
and size vary considerably among modern therians
(Doran, 1878; Fleischer, 1973; Zeller, 1993; Nummela
& Sánchez-Villagra, 2006, Ekdale, 2013).
The presence of a perilymphatic foramen is regarded
as a plesiomorphic feature among mammals (Wible,
1990). A perilymphatic foramen is, for example,
found in the morganucodontid Morganucodon,
the eutriconodontid Priacodon Marsh, 1887,
the docodontan Haldanodon and paulchoffatiid
multituberculates, and is also found in Cretaceous
multituberculates (Kermack et al., 1981; Lillegraven
& Hahn, 1993; Rougier et al., 1996, 2016; Ruf et al.,
2013; Wible et al., 2019). In these taxa, the presence
of a perilymphatic duct is marked by a sulcus in the
dorsomedial edge of the fenestra cochleae that leads
to the jugular foramen, which is also the case in the
Berezovsk specimens. The presence of a perilymphatic
foramen indicates that the petrosals are not of
dryolestoid origin or do not belong to zatherians that
possess a separated bony canaliculus cochleae (closed
canal for the perilymphatic duct) and, therefore, a true
fenestra cochleae (Meng & Fox, 1995; Luo et al., 2011,
2012; Ruf et al., 2013).
The two ?docodontan petrosals, PIN 5087/38 and
PIN 5087/71, show a large and deep mastoid pneumatic
recess. In specimens PIN 5087/69 and PIN 5087/70
this region is broken. A mastoid pneumatic recess
is also present in the docodontans Borealestes and
Haldanodon (Ruf et al., 2013; Panciroli et al., 2019).
Panciroli et al. (2019) suggest that this deep mastoid
pneumatic recess in connection with pneumatization
in the paroccipital region and the high degree of
vascularization is unique to docodontans. Interestingly,
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

MAMMALIAFORM PETROSALS FROM SIBERIA 19
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
petrosal PIN 5087/37 here tentatively assigned to a
haramiyidan origin also shows a mastoid pneumatic
recess, although not as deep as in the two ?docodontan
specimens. However, the bone of PIN 5087/37 is not
as highly vascularized (compare Fig. 3D with Fig .
3A, B) and also the paroccipital region appears not
to be pneumatized. Therefore, the combination of a
deep mastoid pneumatic recess in connection with
pneumatization in the paroccipital region and the high
degree of vascularization is still unique to docodontans.
In the docodontan Haldanodon the crista parotica
and the lateral flange are connected (Ruf et al., 2013),
which is also the case in the Berezovsk specimen PIN
5087/71. The crista parotica and the lateral flange
of specimen PIN 5087/38 are separated by the broad
channel-like sulcus. In PIN 5087/37, the lateral flange
and crista parotica are broken, and thus it is not
determinable if the two structures were connected.
In the three petrosals with the sulcus for the lateral
head vein preserved, the stapedius muscle fossa is
located inside the sulcus, indicated by a rugosity
anterior to the crista parotica. The area of the rugosity
appears circular in the two ?docodontan specimens,
but oval-shaped in the ?haramiyidan specimens. Like
in the docodontan Haldanodon (Ruf et al., 2013),
the stapedius muscle fossa is large and positioned
posterolateral to the fenestra vestibuli in the two
?docodontan petrosals, PIN 5087/38 and PIN 5087/71,
from Berezovsk. In all three specimens, the stapedius
muscle fossa is a rugose area inside the sulcus for the
lateral head vein on the posterolateral border. This
is not the case in Haldanodon in which the stapedial
muscle fossa is depicted to be in a posterior extension
of the sulcus (Ruf et al., 2013). A similar condition to
the Berezovsk petrosals has been illustrated for the
cladotherians Vincelestes Bonaparte, 1986 (Rougier
et al., 1992: fig. 1) and Dryolestes (Luo et al., 2012:
fig. 2A), the early eutherian Prokennalestes Kielan-
Jaworowska & Dashzeveg, 1989 (Wible et al., 2001:
fig. 1A) and a Late Cretaceous placental (Wible &
Hopson, 1993: fig. 5.3F).
The docodontans Borealestes and Haldanodon both
show a complete pterygoparoccipital foramen anterior
to the crista parotica (Ruf et al., 2013; Panciroli et al.,
2019). Through the pterygoparoccipital foramen passes
the superior ramus of the stapedial artery in extant
mammals and early mammaliaforms (Wible, 1990;
Rougier et al., 1992; Wible & Hopson, 1995). In non-
mammaliaform cynodonts and the morganucodontid
Morganucodon it is a simple notch, which resembles
the plesiomorphic condition (Kermack et al., 1981;
Rougier et al., 1992). Only in the ?docodontan specimen
PIN 5087/71 is this foramen fully preserved and lies at
the lateral end of the sulcus of the lateral head vein.
In the second ?docodontan petrosal, PIN5087/38, the
pterygoparoccipital foramen appears to be a notch
at the lateral end of the sulcus for the lateral head
vein, and the lateral flange and paroccipital process
are not connected via a bony bridge like in specimen
PIN 5087/71. It is not fully clear if this notch is in its
original condition in PIN5087/38, but the rounded
edges of the lateral flange and paroccipital process
seem natural. However, this specimen shows several
rounded areas that indicate transportation, which
alters the surface. In the ?haramiyidan specimen PIN
5087/37 the respective area is mostly broken.
The uniquely short lateral flange of the Berezovsk
petrosals covers a space lateral to the lateral flange,
forming a cave-like structure in medial view. We
hypothesize that this cave, although relatively small,
contained the confluent cavum epiptericum and
cavum supracochleare, because of the position of
the facial canal centrally inside this cave. The facial
canal connects to the primary facial foramen inside
the internal acoustic meatus on the dorsal side of the
petrosal. The facial nerve leaves the space containing
the cavum epiptericum and cavum supracochleare
via the secondary facial foramen on the ventral side,
and enters the lateral trough. In the docodontan
Borealestes the secondary facial nerve foramen is
positioned close to an opening leading to the anterior
transcochlear sinus and it was reconstructed that
both the anterior transcochlear sinus and the facial
nerve share the same foramen to exit the cavum
epiptericum and cavum supracochleare (Panciroli
et al., 2019). A similar anatomical organization occurs
in the Berezovsk petrosals. Close proximity between
the facial nerve and the vessel that connects to the
anterior transcochlear sinus when exiting the cavum
area is found in all five specimens. In the ?docodontan
specimen, 5087/38, they even share one oval-shaped
opening.
A confluence of cavum supracochleare and cavum
epiptericum is also present in the early mammaliaforms
Morganucodon and Sinoconodon (Kermack et al.,
1981; Crompton & Luo, 1993). A similar condition
is known from multituberculates (Wible & Rougier,
2000; Ladevèze et al., 2010; Wible et al., 2019). In the
docodontan Haldanodon, the cavum supracochleare is
also confluent with the cavum epiptericum anteriorly
(Ruf et al., 2013). Cavum supracochleare and cavum
epiptericum seem to be more separated (and are only
in connection via the fenestra semilunaris (see
Rougier et al., 1992)) in stem therians such as
Vincelestes and probably also in the Henkelotherium
and Dryolestes, although clear evidence is lacking due
to damage in these taxa (Wible, 1990; Rougier et al.,
1992; Wible et al., 2001; Ruf et al., 2009; Luo et al.,
2012). In extant mammals, the cavum epiptericum
houses the trigeminal ganglion of the trigeminal nerve
(CN V) and the cavum supracochleare houses the
geniculate ganglion of facial nerve. The two ganglia
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

20 J. A. SCHULTZ ET AL.
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
lie outside the braincase of most non-mammalian
amniotes (Kuhn & Zeller, 1987). The secondary side-
wall of the mammalian skull incorporates both the
trigeminal and geniculate ganglia into the braincase
during mammalian evolution (Kuhn & Zeller, 1987).
Interestingly, embryos of modern mammals have
their geniculate ganglion (cavum supracochleare)
and the trigeminal (i.e. semilunar) ganglion (cavum
epiptericum) capsules in close contact; only through
later chondrification and ossification of the tegmen
tympani, in a zone anterior to the prefacial commissure,
a segregated cavum supracochleare is produced, which
separates the two ganglia (Presley, 1993).
Besides determining the position of the geniculate
ganglion, the almost complete preservation of
specimens PIN 5087/71 and PIN 5087/38 made it
possible to reconstruct the major blood vessels of the
?docodontan petrosals. The sulcus on the lateral side
of the apex of the promontorium is the imprint of the
inferior ramus of the stapedial artery that connects to
the internal carotid artery medially via the stapedial
artery (Fig. 9A). The stapes of both docodontans
Haldanodon and Borealestes has a large stapedial
foramen (Ruf et al., 2013; Panciroli et al., 2019). The
same is true for the haramiyidan Arboroharamiya and
the paulchoffatiid multituberculate Pseudobolodon
(Meng et al., 2018; Schultz et al., 2018). Therefore, we
conclude that this was also the case in the Berezovsk
specimens and the stapedial artery passed through
the stapedial foramen when it crossed the fenestra
vestibuli, in which the stapedial footplate sat (Fig.
9). However, no stapes was preserved in the vestibule
in any of the Berezovsk specimens, as was found, for
example, in two different specimens of paulchoffatiid
multituberculates (Schultz et al., 2018).
In several non-therian mammaliaforms, like
Morganucodon or Vincelestes, and taeniolabidoid
multituberculates and also the two Cretaceous
multituberculates Kryptobaatar and Mangasbaatar
Rougier et al., 2016 (Rougier et al., 1992, Wible &
Rougier, 2000; Wible et al., 2019), the stapedial artery
splits into a superior and inferior ramus, approximately
at the level of the fenestra vestibuli, a condition that
we also adopt for the Berezovsk petrosals. The inferior
ramus runs in anterior direction in a shallow sulcus
on the lateral side of the promontorium, best seen
in the ?docodontan specimen PIN 5087/71 and the
?haramiyidan specimen PIN 5087/37 (Fig. 9). The
superior ramus runs in posterior direction and then
turns laterally to run parallel to the lateral head
vein. Both vessels course dorsally after the split off of
the prootic sinus. The lateral head vein then passes
through the large pterygoparoccipital foramen, either
a fully preserved opening, like in PIN 5087/71, or
forming a partially open notch between the paroccipital
process and lateral flange, like in PIN 5087/38.
Figure 9. Reconstruction of the vascular system of the ?docodontan petrosal PIN 5087/38 (A) and ?haramiyidan petrosal
PIN5087/37 (B) from Siberia.
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

MAMMALIAFORM PETROSALS FROM SIBERIA 21
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
A similar condition is found in the non-mammalian
cynodont Thrinaxodon in which the lateral head vein
also turns dorsally to pass through the incomplete
pterygoparoccipital foramen (Rougier et al., 1992).
The prootic vein connects to the lateral head vein
posteromedially from the posterior end of the lateral
flange. It has been suggested that the prootic vein
may be homologous with the lateral head vein of other
mammals, but without developmental data, the exact
identity of the vessel cannot be determined (Ekdale
et al., 2004). A connection to the posterior transcochlear
sinus exists via a short canal inside the sulcus for the
lateral head vein in PIN 5087/71, PIN 5087/38 and
PIN 5087/37, forming an intraosseous connection to
the prootic sinus.
The bone of all Berezovsk petrosals is vascularized
(Fig. 3), similar to the Middle Jurassic European
docodontan Borealestes (Panciroli et al., 2019) and
Late Jurassic docodontan Haldanodon (Ruf et al.,
2013). Compared to the other Berezovsk specimens,
PIN 5087/69 has the strongest vascularization and
displays a network of large venous vessels crossing the
cochlea on the endocranial side (Fig. 3F). All specimens
have two distinct main venous passage-ways crossing
the cochlear canal, embracing the cochlear nerve
entrance anteriorly and posteriorly. The same venous
passages were described for the petrosals of Borealestes
(Panciroli et al., 2019) and termed the anterior and
posterior transcochlear sinuses. Harper & Rougier
(2019) recently reported similar venous pathways in
Priacodon, but suggested a different terminology and
named them anterior and posterior epicochlear sinuses,
which these authors considered to be homologous to
the transcochlear sinuses as identified in docodontans.
In addition, PIN 5087/38 shows a highly vascularized
circum-promontorium plexus along the ventral side
of the cochlear canal (Fig. 3B), which is also present
in Borealestes (Panciroli et al., 2019). Interestingly,
extant monotremes (the only extant mammal with a
sensory lagena at the apex of the cochlear canal) do not
show such strong vascularization around the cochlea
(Kuhn & Zeller, 1987; Schultz et al., 2017).
The reconstructions of the endocasts of the pars
canalicularis show a secondary crus commune
in PIN 5087/37, PIN 5087/38 and PIN 5087/71, a
plesiomorphic feature that is also known from several
non-mammalian cynodonts (e.g. Denker, 1901; Meng
& Fox, 1995; Sánchez-Villagra & Schmelzle, 2007;
Ruf et al., 2009; Ekdale & Rowe, 2011). The endocasts
demonstrate that the aquaeductus vestibuli is not
confluent with the lumen of the crus commune, which
is different from the condition in the docodontan
Haldanodon (Ruf et al., 2013). In the docodontan
Borealestes the condition is similar to that of the
?docodontan endocasts from Siberia. The aquaeductus
vestibuli lies separate from the lumen of the crus
commune (see Panciroli et al., 2019: fig. 7D, B, p. 10;
endolymphatic duct not labelled but visible).
In comparison to the two docodontans Haldanodon
and Borealestes, the cochlear canals reconstructed
from the Berezovsk endocasts of the pars cochlearis are
similarly curved (nearly 180°), but the apical inflation
is less prominent [compare Ruf et al. (2013) with
Panciroli et al. (2019)]. The curvature of the cochlear
canal up to 180° resembles the pattern also found in
the extant monotreme Ornithorhynchus Blumenbach,
1800, but differs from that of Morganucodon with a
straight or only slightly curved cochlear canal (Denker,
1901; Graybeal et al., 1989; Fox & Meng, 1997; Luo
et al., 2011; Schultz et al., 2017). The reconstructed
cochlear endocasts of all Berezovsk specimens differ
from cladotherians in their comparably weak coiling of
a little less than 180°, as well as in lacking the primary
and secondary bony laminae (Meng & Fox, 1995; Ruf
et al., 2009; Luo et al., 2011). Interestingly, in the
?haramiyidan specimens, PIN 5087/31, PIN 5087/69
and PIN 5087/70, remnants of a perforated bony bar
is preserved on the medial side of the cochlear nerve
entrance in the internal acoustic meatus. The medial
position of the perforated bony bar are unique, because
it differs from the normal position of the primary bony
lamina of modern mammals. The perforation resembles,
in part, the tractus foraminosus of monotremes, but
a concurrent wide opening of the cochlear nerve
entrance, together with a perforated bony structure,
does not occur in the two monotremes Ornithorhynchus
or Tachyglossus Illiger, 1811. In both taxa, the cochlear
nerve fibres perforate the cochlear canal via multiple
unordered small openings (Schultz et al., 2017). The
cladotherians Dryolestes and Henkelotherium have a
primary bony lamina, but the cochlear nerve entrance
is structurally different from that of monotremes
(Ruf et al., 2009; Luo et al., 2012). In Dryolestes, the
channels for the cochlear nerve fibres show a curved
pattern on the ossified cribriform floor of the internal
acoustic meatus, different from the bony bar in the
?haramiyidan petrosals from Siberia. In Dryolestes,
the nerve fibre channels are more regular inside the
cribriform plate than in monotremes, and the pattern
resembles more that of therian mammals, in which
each of the channels transmits an individual cochlear
nerve fibre strand. In addition to the organized fibre
pattern, Dryolestes shows a separate bony channel
for the cochlear nerve ganglion (Luo et al., 2012),
a feature that is not found in any of the Berezovsk
petrosals. A cribriform structure is not reported for
Henkelotherium, because the preservation in the area
of the internal acoustic meatus was insufficient (Ruf
et al., 2009). The perforated bony bar of petrosals
PIN 5087/37, PIN 5087/69 and PIN 5087/70 is
different, because it does not fill the whole opening
for the cochlear nerve, the bony bar is only medially
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

22 J. A. SCHULTZ ET AL.
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
connected to the petrosal bone and had a supporting
function only on the medial side. On the medial wall
of the three petrosals with a perforated bony bar, faint
sulci are visible (Fig. 6A, B, D). We interpret these as
imprints of single nerve fibres leading to the cochlea.
Thus, the initial cochlear nerve fibres are channelled
along the holes of the perforated bony bar, while the
rest fan out into the cochlear canal without piercing
through the bony bar (Fig. 6E).
Luo & Ketten (1991) reported a relatively straight
and slender cochlear canal without apical inflation for
the Late Cretaceous multituberculate Meniscoessus
[also illustrated by Luo et al. (2016: fig. 6.9K) and as 3D
rendering in Luo & Manley (2020: fig. 9)] and the Early
Palaeocene multituberculate Catopsalis from North
America. However, Ladevèze et al. (2010) have reported
a slightly curved cochlear canal with a somewhat
inflated apex for the Late Cretaceous multituberculate
cf. Tombaatar sp. from China. The reconstructions of
Hurum (1998: fig. 6, p. 73) of the inner ear of derived
multituberculates show the discrepancy between
the larger vestibule and, in comparison to that, the
relatively short and thin cochlear canal. Unfortunately,
Lillegraven & Hahn (1993) could not provide a
reconstruction of the cochlear canal for paulchoffatiid
multituberculates. The so far known multituberculate
petrosals are different from the Berezovsk specimens
in the morphology of the cochlear canal and vestibule,
which makes a multituberculate origin unlikely, as
stated above.
The inflated apex of the reconstructed cochlear
canals of the Berezovsk specimens indicates that a
lagena probably was present in the living animal,
as in extant monotremes (Schultz et al., 2017) ,
and a distinct bony sulcus for possible lagenar
innervation, as known from Haldanodon (Ruf et al.,
2013) is evident in the ?docodontan specimens, PIN
5087/38 and PIN 5087/71, but also visible in the
?haramiyidan petrosal PIN 5087/69. In monotremes,
the membranous cochlear system (i.e. scala tympani,
scala media, scala vestibuli and lagena) shows a
coiling at the tip inside the cochlear canal causing
an inflation at the end of the osseous canal (Schultz
et al., 2017). This morphology is directly connected
to the presence of the lagena and a helicotrema
in subapical position. The presence of the apical
inflation in combination with a lagenar sulcus
makes it likely that the Berezovsk specimens
also possessed a lagena, even though a separate
bony canal for the lagenar nerve is not present.
A lagena was also present in the morganucodontan
Morganucodon or the mammaliaform Hadrocodium
Luo et al., 2001, paulchoffatiid and cimolodontan
multituberculates and the gondwanatherian
Adalatherium Krause et al., 2020 from Madagascar
(Luo et al., 2017; Krause et al., 2020).
All five petrosals have a small foramen on the
transverse crest for the saccular branch of CN VIII (Fig.
3E). The branch of CN VIII innervating the ampulla of
the posterior semicircular canal has a separate sulcus
on the posterior end of the cochlear nerve foramen,
evident in petrosals PIN 5087/37, PIN 5087/38 and
PIN 5087/69 (Fig. 3A, D, F). The position of the branch
of CN VIII innervating the ampulla of the posterior
semicircular canal is similar to that described for the
monotreme Ornithorhynchus (Schultz et al., 2017)
and the innervation of the ampulla of the posterior
semicircular canal is thus fully separated from the
saccular branch. However, in Ornithorhynchus, the
branch for the posterior ampulla is enclosed in a bony
canal, fully separated from the cochlear nerve (Fig.
3H). The often used anatomical term ‘sacculoampullar
foramen’ implies a transmission of the combined
saccular innervation and ampullar innervation of
the posterior semicircular canal through one and the
same opening. Because of the similar condition found
in the Berezovsk petrosals and Ornithorhynchus
(Schultz et al., 2017), and the separate reconstruction
of both the saccular and posterior semicircular branch
demonstrated here, we choose to term the foramen
of the transverse crest just saccular foramen. The
term sacculo-ampullar foramen is improper, because
the branch innervating the saccular macula and
the branch innervating the ampulla of the posterior
semicircular canal are clearly separate structures
with different bony canals associated.
In summary, the taxonomic assignment of the two
larger and more robust Berezovsk petrosals PIN
5087/38 and PIN 5087/71 to docodontans is supported
by the following characters: (1) the presence of a
perilymphatic foramen and a less curved cochlear
canal exclude a dryolestoid or other derived therian
mammal origin for the specimens and suggests a
more primitive state like in Morganucodonta and
Docodonta; (2) the wide pneumatized cavity posterior
to the stapedius muscle fossa is similar to the
derived deep mastoid pneumatic recess found in the
docodontan Haldanodon; (3) the apical inflation of
the cochlear canal is similar to the condition known
from the docodontans Haldanodon and Borealestes,
or extant monotremes; (4) both anterior and posterior
transcochlear sinuses and a circum-promontorium
plexus are present as found in the docodontan
Borealestes; and (5) a bony ridge on the promontorium
occurs as an elongation of the crista interfenestralis.
Even though the Berezovsk specimens are about
12 Myr older than the Kimmeridgian Haldanodon,
the overall morphology of the petrosals and the
reconstructed endocasts of PIN 5087/38 and PIN
5087/71 show striking similarities. They are about the
same age as Borealestes and are the third record of
docodontan ear regions with important information on
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

MAMMALIAFORM PETROSALS FROM SIBERIA 23
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
the diversity of the petrosal and inner ear morphology
of this group.
The assignment of the smaller and more slender
petrosals PIN 5087/37, PIN 5087/69 and PIN
5087/70 to the haramiyidans is supported by
the following characters: (1) the presence of a
perilymphatic foramen and a less curved cochlear
canal distinguishes the specimens from dryolestoids
and other derived therian mammals suggesting a
more primitive origin; (2) the occurrence of a thin
and short perforated bony bar medially visible
inside the foramen for the cochlear part of CN VIII
or the medial rim of this opening being perforated
itself distinguish the three petrosals from PIN
5087/38 and PIN 5087/71 excluding a docodontan
origin; and (3) the bony ridge on the promontorium
perpendicular to the crista interfenestralis is visible,
like in the haramiyidan Arboroharamiya. We note
that the petrosal PIN 5087/69 has some features
that distinguish it from PIN 5087/38 and PIN
5087/71. For example, this specimen shows distinctly
thicker blood vessels surrounding the cochlear duct
(compare Fig. 3A–C). In addition, the entrance of
the cochlear portion of CN VIII is more circular and
not elongated as in PIN 5087/37 and PIN 5087/38,
and there is a groove running in anterior direction
inside the cochlear canal. This groove is comparable
to a structure found in the docodontan Haldanodon,
which is interpreted as a sulcus for a separate
lagenar nerve (Ruf et al., 2013). In addition, the
inflation of the apex of the cochlear canal seems
slightly larger than in the other specimens.
CONCLUSIONS
So far, three docodontan species and four haramiyidan
species have been identified based on teeth and jaw
fragments from the Berezovsk locality (Averianov et al.,
2010b, 2019b). It is likely that the slight differences
between petrosals PIN 5087/38 and PIN 5087/71
may represent different docodontan species or even
genera. PIN 5087/37, PIN 5087/69 and PIN 5087/70
are strikingly different from the other two specimens
(e.g. perforated bony bar and different arrangement
of the bony ridge on the promontorium) and probaby
belong to a different group. The second-most abundant
group, according to the findings of isolated teeth, are
haramiyidans. We thus tentatively assign the petrosals
PIN 5087/37, PIN 5087/69 and PIN 5087/70 to be of
haramiyidan origin. Although not known from other
Mesozoic taxa due to missing fossil evidence, it cannot
be excluded that the size differences represent sexual
dimorphism. The state of ossification of the petrosals
makes it unlikely that the size differences are due to
ontogenetic variation.
ACKNOWLEDGEMENTS
For assistance in the field and/or picking the
concentrate, we thank I. Danilov, T. Engler,
D. Grigoriev, O. Grigorieva, R. Hielscher, S. Hoffmann,
S. Ivantsov, K. Jäger, J. Könen, I. Kuzmin, A. Lang,
B. Mähler, B. Peters, D. Rohkamp, M. Scheske,
A. Schwermann, L. Schwermann, E. Syromyatnikova
and A. Valeev. We thank B. Mähler for helping with the
preparation of the 3D PDF files that are part of the
Supporting Information, available from digital data
repository Dryad. Financial support was provided by
the Deutsche Forschungsgemeinschaft (DFG) (grant
MA 1643/14-1, 3), the Board of the President of the
Russian Federation (MD-802.2009.4), the Russian
Foundation for Basic Research (projects 07-04-
00393, 10-04-01350, 13-04-01401 and 11-04-91331-
NNIO) and the Program of the Presidium of the
Russian Academy of Sciences ‘Origin of the Life and
Establishment of Biosphere.’ AA was supported by
the Zoological Institute, Russian Academy of Sciences
(project АААА-А17-117022810195-3). The laboratory
research by AA received support from the Russian
Scientific Fund (19-14-00020). We thank P. Göddertz
for µCT scanning specimen PIN 5087/38. The authors
declare no conflicts of interest.
DATA AVAILABILITY
The data underlying this article are available from
the digital data repository Dryad at https://doi.
org/10.5061/dryad.t1g1jwt2d, and contain the original
µCT image stacks, scan info sheets for each specimen
along with 3D PDFs and STL files.
REFERENCES
Alifanov VR, Krasnolutskii SA, Markov VN,
Martynovich NV. 2001. About discovery of the Middle
Jurassic dinosaurs in the Krasnoyarsk Territory. Scientific-
practical conference problems of the struggle against illegal
excavations and illegal turnover of the objects of archaeology,
mineralogy, and paleontology. Proceedings Volume.
Krasnoyarsk: 71-74.
Averianov AO, Krasnolutskii SA. 2009. Stegosaur remains
from the Middle Jurassic of West Siberia. Proceedings of the
Zoological Institute of the Russian Academy of Sciences 313:
59–73.
Averianov AO, Lopatin AV. 2006. Itatodon tatarinovi
(Tegotheriidae, Mammalia), a docodont from the Middle
Jurassic of Western Siberia and phylogenetic analysis of
Docodonta. Paleontological Journal 40: 668–677.
Averianov AO, Lopatin AV, Skutschas PP,
Martynovich NV, Leshchinskiy SV, Rezvyi AS,
Krasnolutskii SA, Fayngertz AV. 2005. Discovery of
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

24 J. A. SCHULTZ ET AL.
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
Middle Jurassic mammals from Siberia. Acta Palaeontologica
Polonica 50: 789–797.
Averianov AO, Lopatin AV, Krasnolutskii SA. 2008. An
amphilestid-grade eutriconodontan from the Middle Jurassic
of Russia. Russian Journal of Theriology 7: 1–4.
Averianov AO, Krasnolutskii SA, Ivantsov SV. 2010a. A
new basal coelurosaur (Dinosauria: Theropoda) from the
Middle Jurassic of Siberia. Proceedings of the Zoological
Institute of the Russian Academy of Sciences 314: 42–57.
Averianov AO, Lopatin AV, Krasnolutskii SA, Ivantsov SV.
2010b. New docodontans from the Middle Jurassic of Siberia
and reanalysis of Docodonta interrelationships. Proceedings
of the Zoological Institute of the Russian Academy of Sciences
314: 121–148.
Averianov AO, Lopatin AV, Krasnolutskii SA. 2011. The
first haramiyid (Mammalia, Allotheria) from the Jurassic of
Russia. Doklady Biological Sciences 437: 103–106.
Averianov AO, Martin T, Lopatin AV. 2014. The oldest
dryolestid mammal from the Middle Jurassic of Siberia.
Journal of Vertebrate Paleontology 34: 924–931.
Averianov AO, Martin T, Skutschas PP, Danilov I,
Schultz JA, Schellhorn R, Obraztsova E, Lopatin AV,
Sytchevskaya E, Kuzmin I, Krasnolutskii SA,
Ivantsov SV. 2017a. Middle Jurassic vertebrate assemblage
of Berezovsk coal mine in western Siberia (Russia). Global
Geology 19: 187–204.
Averianov AO, Martin T, Lopatin AV, Schultz JA,
Skutschas PP, Schellhorn R, Krasnolutskii SA. 2017b.
A tritylodontid synapsid from the Middle Jurassic of Siberia
and the taxonomy of derived tritylodontids. Journal of
Vertebrate Paleontology 37: e1363767.
Averianov AO, Krasnolutskii S, Ivantsov S, Skutschas P,
Schellhorn R, Schultz J, Martin T, 2019a. Sauropod
remains from the Middle Jurassic Itat Formation of West
Siberia, Russia. PalZ 93: 691–701.
Averianov AO, Martin T, Lopatin AV, Schultz JA,
Schellhorn R, Krasnolutskii S, Skutschas P,
Ivantsov S. 2019b. Haramiyidan mammals from the Middle
Jurassic of Western Siberia, Russia. Part 1: Shenshouidae
and Maiopatagium. Journal of Vertebrate Paleontology 39:
e1669159.
Averianov AO, Osochnikova A, Skutschas P,
Krasnolutskii S, Schellhorn R, Schultz JA, Martin T.
2021a. New data on the tyrannosauroid dinosaur Kileskus
from the Middle Jurassic of Siberia, Russia. Historical
Biology 33: 897–903.
Averianov AO, Martin T, Lopatin AV, Schultz JA,
Schellhorn R, Krasnolutskii S, Skutschas P,
Ivantsov S. 2021b. Multituberculate mammals from
the Middle Jurassic of western Siberia, Russia, and the
origin of Multituberculata. Papers in Palaeontology 7:
769–787.
Crompton AW, Luo Z-X. 1993. Relationships of the Liassic
mammals Sinoconodon, Morganucodon oehleri, and
Dinnetherium. In: Szalay FS, Novacek MJ, McKenna MC,
eds. Mammal phylogeny: Mesozoic differentiation,
multituberculates, monotremes, early therians, and
marsupials. New York: Springer, 30–44.
Crompton AW, Sun A-L. 1985. Cranial structure and
relationships of the Liassic mammal Sinoconodon. Zoological
Journal of the Linnean Society 85: 99–119.
Denker A. 1901. Zur Anatomie des Gehörorgans
der Monotremata. Denkschriften der medicinisch-
naturwissenschaftlichen Semon Zoologische
Forschungsreisen in Australien 3: 635–662.
Doran AHG. 1878. XVIII. Morphology of the mammalian
Ossicula auditûs. Transactions of the Linnean Society of
London, 2nd Series, Zoology 1: 371–497.
Ekdale EG. 2013. Comparative anatomy of the bony labyrinth
(inner ear) of placental mammals. PLoS One 8: e66624.
Ekdale EG, Rowe T. 2011. Morphology and variation within
the bony labyrinth of zhelestids (Mammalia, Eutheria) and
other therian mammals. Journal of Vertebrate Paleontology
31: 658–675.
Ekdale EG, Archibald JD, Averianov, AO. 2004. Petrosal
bones of placental mammals from the Late Cretaceous of
Uzbekistan. Acta Palaeontologica Polonica 49: 161–176.
Fleischer G. 1973. Studien am Skelett des Gehörorganes der
Säugetiere, einschließlich des Menschen. Säugetierkundliche
Mitteilungen 21: 131–239.
Fox RC, Meng J. 1997. An X-radiographic and SEM study of
the osseous inner ear of multituberculates and monotremes
(Mammalia): implications for mammalian phylogeny and
evolution of hearing. Zoological Journal of the Linnean
Society 121: 249–291.
Frisch T, Sørensen MS, Overgaard S, Lind M, Bretlau P.
1998. Volume-referent bone turnover estimated from the
interlabel area fraction after sequential labeling. Bone 22:
677–682.
Graybeal A, Rosowski JJ, Ketten DR, Crompton AW.
1989. Inner-ear structure in Morganucodon, an early
Jurassic mammal. Zoological Journal of the Linnean Society
96: 107–117.
Hahn G. 1988. Die Ohr-Region der Paulchoffatiidae
(Multituberculata, Ober-Jura). Palaeovertebrata 18: 155–185.
Han G, Mao F, Bi S, Wang Y, Meng J. 2017. A Jurassic
gliding euharamiyidan mammal with an ear of five auditory
bones. Nature 551: 451–456.
Harper T, Rougier GW. 2019. Petrosal morphology and
cochlear function in Mesozoic stem therians. PLoS One 14:
e0209457.
Hughes EM, Wible JR, Spaulding M, Luo Z-X. 2015.
Mammalian petrosal from the Upper Jurassic Morrison
Formation of Fruita, Colorado. Annals of Carnegie Museum 83:
1–17.
Hurum JH. 1998. The inner ear of two Late Cretaceous
multituberculate mammals, and its implications for
multituberculate hearing. Journal of Mammalian Evolution
5: 65–93.
Kearney M, Maisano JA, Rowe T. 2005. Cranial anatomy of
the extinct amphisbaenian Rhineura hatcherii (Squamata,
Amphisbaenia) based on high-resolution x-ray computed
tomography. Journal of Morphology 264: 1–33.
Kermack KA, Mussett F, Rigney HW. 1981. The skull of
Morganucodon. Zoological Journal of the Linnean Society
71: 1–158.
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

MAMMALIAFORM PETROSALS FROM SIBERIA 25
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
Kielan-Jaworowska Z, Hurum JH, Lopatin AV. 2005.
Skull structure in Catopsbaatar and the zygomatic ridges in
multituberculate mammals. Acta Palaeontologica Polonica
50: 487–512.
Krause DW, Hoffmann S, Hu Y, Wible JR, Rougier GW,
Kirk EC, Groenke JR, Rogers RR, Rossie JB, Schultz JA,
Evans AR, Koenigswald Wv, Rahantarisoa LJ. 2020.
Skeleton of a Cretaceous mammal from Madagascar reflects
long-term insularity. Nature 581: 421–427.
Kuhn HJ, Zeller U. 1987. The cavum epiptericum in
monotremes and therian mammals. Mammalia Depicta 13:
51–70.
Laaß M. 2015. Bone-conduction hearing and seismic
sensitivity of the late Permian anomodont Kawingasaurus
fossilis. Journal of Morphology 276: 121–143.
Ladevèze S, de Muizon C, Colbert M, Smith T. 2010.
3D computational imaging of the petrosal of a new
multituberculate mammal from the Late Cretaceous of
China and its paleobiologic inferences. Comptes Rendus
Palevol 9: 319–330.
Lewis ER, Narins PM. 1985. Do frogs communicate with
seismic signals? Science 227: 187–189.
Lillegraven JA, Hahn G. 1993. Evolutionary analysis of the
middle and inner ear of Late Jurassic multituberculates.
Journal of Mammalian Evolution 1: 47–74.
Lopatin AV, Averianov AO. 2005. A new docodont
(Docodonta, Mammalia) from the Middle Jurassic of Siberia.
Doklady Biological Sciences 405: 434–436.
Lopatin AV, Averianov AO. 2007. The earliest Asiatic
pretribosphenic mammal (Cladotheria, Amphitheriidae)
from the Middle Jurassic of Siberia. Doklady Biological
Sciences 417: 432–434.
Lopatin AV, Averianov AO. 2009. Mammals that coexisted
with dinosaurs. Finds of the Russian territory. Herald of the
Russian Academy of Sciences 79: 268–273.
Luo Z-X. 2001. The inner ear and its bony housing in
tritylodontids and implications for evolution of the
mammalian ear. Bulletin of the Museum of Comparative
Zoology 156: 81–97.
Luo Z-X, Ketten DR. 1991. CT scanning and computerized
reconstructions of the inner ear of multituberculate
mammals. Journal of Vertebrate Paleontology 11: 220–228.
Luo Z-X, Manley G. 2020. Origins and early evolution of
mammalian ears and hearing function. In: Fritzsch B, ed.
The senses: a comprehensive reference, 2nd edn. London:
Academic Press, 207–252.
Luo Z-X, Crompton AW, Lucas SG. 1995. Evolutionary
origins of the mammalian promontorium and cochlea.
Journal of Vertebrate Paleontology 15: 113–121.
Luo Z-X, Ruf I, Schultz JA, Martin T. 2011. Fossil evidence
on evolution of inner ear cochlea in Jurassic mammals.
Proceedings of the Royal Society, Series B 278: 28–34.
Luo Z-X, Ruf I, Martin T. 2012. The petrosal and inner ear of
the Late Jurassic cladotherian mammal Dryolestes leiriensis
and implications for ear evolution in therian mammals.
Zoological Journal of the Linnean Society 166: 433–463.
Luo Z-X, Schultz JA, Ekdale EG. 2016. Evolution of the
middle and inner ears of mammaliaforms: the approach to
mammals. In: Clack JA, Fay RR, Popper AN, eds. Evolution
of the vertebrate ear. Cham: Springer, 139-174.
Luo Z-X, Meng QJ, Grossnickle DM, Liu D, Neander AI,
Zhang YG, Ji Q. 2017. New evidence for mammaliaform ear
evolution and feeding adaptation in a Jurassic ecosystem.
Nature 548: 326–329.
Martin T, Averianov AO, Lopatin AV, Schultz JA. 2014.
Mammals from the Middle Jurassic of Western Siberia. 74th
Annual Meeting of the Society of Vertebrate Paleontology in
Berlin 2014. Supplement to the online Journal of Vertebrate
Paleontology November 2014: 180.
Meng J. 1992. The stapes of Lambdopsalis bulla
(Multituberculata) and transformational analyses on some
stapedial features in Mammaliaformes. Journal of Vertebrate
Paleontology 12: 459–471.
Meng J, Wyss AR. 1995. Monotreme affinities and low-
frequency hearing suggested by multituberculate ear. Nature
377: 141–144.
Meng J, Fox RC. 1995. Osseous inner ear structures and
hearing in early marsupials and placentals. Zoological
Journal of the Linnean Society 115: 47–71.
Meng J, Hou SL. 2016. Earliest known mammalian stapes
from an Early Cretaceous eutriconodontan mammal and
implications for evolution of mammalian middle ear.
Palaeontologia Polonica 67: 181–196.
Meng J, Bi S, Zheng X, Wang X. 2018. Ear ossicle morphology
of the Jurassic euharamiyidan Arboroharamiya and
evolution of mammalian middle ear. Journal of Morphology
279: 441–457.
Meng J, Mao F, Han G, Zheng XT, Wang XL, Wang Y. 2020.
A comparative study on auditory and hyoid bones of Jurassic
euharamiyidans and contrasting evidence for mammalian
middle ear evolution. Journal of Anatomy 236: 50–71.
Miao D. 1988. Skull morphology of Lambdopsalis bulla
(Mammalia, Multituberculata) and its implications to
mammalian evolution. Contributions to Geology, University
of Wyoming, Special Paper 4: 1–104.
Nummela S, Sánchez-Villagra MR. 2006. Scaling of the
marsupial middle ear and its functional significance. Journal
of Zoology 270: 256–267.
Panciroli E, Schultz JA, Luo Z-X. 2019. Morphology of
the petrosal and stapes of Borealestes (Mammaliaformes,
Docodonta) from the Middle Jurassic of Skye, Scotland.
Papers in Palaeontology 5: 139–156.
Panciroli E, Benson RBJ, Fernandez V, Butler RJ,
Fraser NC, Luo Z-X, Walsh S. 2021. New species
of mammaliaform and the cranium of Borealestes
(Mammaliformes: Docodonta) from the Middle Jurassic of
the British Isles. Zoological Journal of the Linnean Society
192: 1323–1362.
Presley R. 1993. Development and the phylogenetic features
of the middle ear region. In: Szalay FS, Novacek MJ,
McKenna MC, eds. Mammal phylogeny: Mesozoic
differentiation, multituberculates, monotremes, early
therians, and marsupials. New York: Springer, 31–39.
Rougier GW, Wible JR. 2006. Major changes in the ear region
and basicranium of early mammals. In: Carrano MT, Gaudin TJ,
Blob RW, Wible JR, eds. Amniote paleobiology: perspectives on the
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021

26 J. A. SCHULTZ ET AL.
© 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–26
evolution of mammals, birds and reptiles. Chicago: University of
Chicago Press, 269–311.
Rougier GW, Wible JR, Hopson JA. 1992. Reconstruction
of the cranial vessels in the Early Cretaceous mammal
Vincelestes neuquenianus: implications for the evolution
of the mammalian cranial vascular system. Journal of
Vertebrate Paleontology 12: 188–216.
Rougier GW, Wible JR, Hopson JA. 1996. Basicranial
anatomy of Priacodon fruitaensis (Triconodontidae,
Mammalia) from the Late Jurassic of Colorado, and a
reappraisal of mammaliaform interrelationships. American
Museum Novitates 3183: 1–38.
Rougier GW, Wible JR, Beck RMD, Apesteguía S. 2012.
The Miocene mammal Necrolestes demonstrates the survival
of a Mesozoic nontherian lineage into the late Cenozoic of
South America. Proceedings of the National Academy of
Sciences 109: 20053–20058.
Rodrigues PG, Ruf I, Schultz CL. 2013. Digital
reconstruction of the otic region and inner ear of the non-
mammalian cynodont Brasilitherium riograndensis (Late
Triassic, Brazil) and its relevance to the evolution of the
mammalian ear. Journal of Mammalian Evolution 20:
291–307.
Rougier GW, Sheth AS, Spurlin BK, Bolortsetseg M,
Novacek MJ. 2016. Cranio dental anatomy of a new Late
Cretaceous multituberculate mammal from Udan Sayr,
Mongolia. Palaeontologia Polonica 67: 197–248.
Rowe T. 1988. Definition, diagnosis, and origin of Mammalia.
Journal of Vertebrate Paleontology 8: 241–264.
Ruf I, Luo Z-X, Wible JR, Martin T. 2009. Petrosal anatomy
and inner ear structures of the Late Jurassic Henkelotherium
(Mammalia, Cladotheria, Dryolestoidea): insight into the
early evolution of the ear region in cladotherian mammals.
Journal of Anatomy 214: 679–693.
Ruf I, Luo Z-X, Martin T. 2013. Reinvestigation of the
basicranium of Haldanodon exspectatus (Mammaliaformes,
Docodonta). Journal of Vertebrate Paleontology 33:
382–400.
Sánchez-Villagra MR, Schmelzle T. 2007. Anatomy and
development of the bony inner ear in the woolly opossum,
Caluromys philander (Didelphimorphia, Marsupialia).
Mastozoología Neotropical 14: 53–60.
Schultz JA, Zeller U, Luo Z-X. 2017. Inner ear labyrinth
anatomy of monotremes and implications for mammalian
inner ear evolution. Journal of Morphology 278: 236–263.
Schultz JA, Ruf I, Martin T. 2018. Oldest known
multituberculate stapes suggests an asymmetric bicrural
pattern as ancestral for Multituberculata. Proceedings of the
Royal Society, Series B 285: 20172779.
Segall W. 1970. Morphological parallelisms of the bulla and
auditory ossicles in some insectivores and marsupials.
Fieldiana Zoology 51: 169–205.
Skutschas PP. 2006. Mesozoic amphibians from Siberia,
Russia. In: Barrett PM, Evans SE, eds. 9th International
Symposium on Mesozoic Terrestrial Ecosystems and Biota.
Abstracts and Proceedings Volume, Natural History Museum,
London, 123–126.
Skutschas PP, Krasnolutskii SA. 2011. A new genus and
species of basal salamanders from the Jurassic of Western
Siberia, Russia. Proceedings of the Zoological Institute of the
Russian Academy of Sciences 315: 167–175.
Skutschas PP, Leshchinskiy SV, Rezvyi AS, Fayngerts AV,
Krasnolutskii SA. 2005. Remains of salamanders from the
Middle Jurassic of the Krasnoyarsk Territory. In: Rozanov AY,
Lopatin AV, Parkhaev PY, eds. Modern paleontology: classical
and newest methods. Moscow: Paleontological Institute
Russian Academy of Sciences, 121–124 [In Russian].
Skutschas P, Kolchanov V, Krasnolutskii S,
Averianov AO, Schellhorn R, Schultz JA, Martin T.
2020. A new small-sized stem salamander from the Middle
Jurassic of Western Siberia, Russia. PLoS One 15: e0228610.
Wever EG. 1985. The amphibian ear. Princeton: Princeton
University Press, 488.
Wible JR. 1990. Petrosals of Late Cretaceous marsupials
from North America, and a cladistic analysis of the petrosal
in therian mammals. Journal of Vertebrate Paleontology 10:
183–205.
Wible JR, Hopson JA. 1993. Basicranial evidence for
early mammal phylogeny. In: Szalay FS, Novacek MJ,
McKenna MC, eds. Mammal phylogeny: Mesozoic
differentiation, multituberculates, monotremes, early
therians, and marsupials. New York: Springer, 45–62.
Wible JR, Hopson JA. 1995. Homologies of the prootic canal
in mammals and non-mammalian cynodonts. Journal of
Vertebrate Paleontology 15: 331–356.
Wible JR, Rougier GW. 2000. The cranial anatomy of
Kryptobaatar dashzevegi (Mammalia, Multituberculata),
and its bearing on the evolution of mammalian characters.
Bulletin of the American Museum of Natural History 247:
1–120.
Wible JR, Shelley SL, Bi S. 2019. New genus and species of
djadochtatheriid multituberculate (Allotheria, Mammalia)
from the Upper Cretaceous Bayan Mandahu Formation of
Inner Mongolia. Annals of Carnegie Museum 85: 285–327.
Wible JR, Rougier GW, Novacek MJ, McKenna MC.
2001. Earliest eutherian ear region: a petrosal referred to
Prokennalestes from the Early Cretaceous of Mongolia.
American Museum Novitates 3322: 1–44.
Zeller U. 1993. Ontogenetic evidence for cranial homologies
in monotremes and therians, with special reference to
Ornithorhynchus. In: Szalay FS, Novacek MJ, McKenna MC,
eds. Mammal phylogeny: Mesozoic differentiation,
multituberculates, monotremes, early therians, and
marsupials. New York: Springer, 45–62.
SUPPORTING INFORMATION
All 3D models and reconstructions are available as interactive 3D PDF files for download from the digital data
repository Dryad at https://doi.org/10.5061/dryad.t1g1jwt2d. In addition a short instruction how to use 3D PDF is
provided as supplementary online material.
Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlab096/6472402 by Paleontological Institute of the Russian Academy of Sciences user on 28 December 2021