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Abstract

Neuroanatomical reconstructions of extinct animals have long been recognized as powerful proxies for palaeoecology, yet our understanding of the endocranial anatomy of dromaeosaur theropod dinosaurs is still incomplete. Here, we used X-ray computed microtomography (µCT) to reconstruct and describe the endocranial anatomy, including the endosseous labyrinth of the inner ear, of the small-bodied dromaeosaur, Velociraptor mongoliensis. The anatomy of the cranial endocast and ear were compared with non-avian theropods, modern birds, and other extant archosaurs to establish trends in agility, balance, and hearing thresholds in order to reconstruct the trophic ecology of the taxon. Our results indicate that V. mongoliensis could detect a wide and high range of sound frequencies (2,368–3,965 Hz), was agile, and could likely track prey items with ease. When viewed in conjunction with fossils that suggest scavenging-like behaviours in V. mongoliensis, a complex trophic ecology that mirrors modern predators becomes apparent. These data suggest that V. mongoliensis was an active predator that would likely scavenge depending on the age and health of the individual or during prolonged climatic events such as droughts.
Journal of Anatomy. 2020;00:1–9.
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  1wileyonlinelibrary.com/journal/joa
1 | INTRODUCTION
Velociraptor mongoliensis Osborn, 1924 is a velociraptorine dro-
maeosaur found in Late Cretaceous formations of China and
Mongolia (Osborn, 1924; Godefroit et al., 2008) that has been
made famous in recent years thanks to its portrayal in numer-
ous Holly wood movies. V. mongoliensis has also been the subject
of a number of cranial and postcranial publications (Sues, 1977;
Norell et al., 1997; 2004; Barsbold and Osmólska, 1999; Turner
et al., 2007; Manning et al., 20 09), with the cranial osteolog y,
including the braincase, being well-known thanks to the excep-
tionally preser ved specimens found in Mongolia (Barsbold and
Osmólska, 1999). Despite this heightened attention, the endo-
cranial anatomy of V. mongoliensis has not yet been described.
Indeed, the endocranial anatomy of Dromaeosauridae as a whole
is still relatively poorly known despite the initial osteological
description of Dromaeosaurus having occurred almost a centur y
ago (Matthew and Brown, 1922). Since that time, the endocast
Received: 10 Januar y 2020 
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  Revised: 30 April 2020 
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  Accepted: 22 M ay 2020
DOI: 10.1111/joa.13253
ORIGINAL ARTICLE
The endocranium and trophic ecology of Velociraptor
mongoliensis
J. Logan King1| Justin S. Sipla2| Justin A. Georgi3| Amy M. Balanoff4,5|
James M. Neenan6
This is an op en access article under t he terms of the Creat ive Commons Attributio n License, which permits use, dist ribution and reproduc tion in any medium,
provide d the orig inal work is proper ly cited .
© 2020 The Authors . Journa l of Anatomy publishe d by John Wiley & Sons Ltd on behalf of Anatomical Society
1School of Earth Science s, University of
Bristol, Bristol, UK
2Depar tment of A natomy and Cell Biology,
University of Iow a, Iowa City, IA, USA
3Depar tment of A natomy, Midwe stern
University, Glen dale, A Z, USA
4Divisio n of Paleontology, America n
Museum of N atural H istor y, New York, NY,
USA
5Depar tment of P sychological and Brain
Science s, Johns Hopkins University,
Baltim ore, MD, USA
6Oxford University Mus eum of Natural
Histor y, University of Ox ford, Ox ford, U K
Correspondence
James M. Neenan, Oxford University
Museum of N atural H istor y, University of
Oxford, Oxford OX1 3PW, UK.
Email: james.neenan@oum.ox.ac.uk
Funding information
Leverhulme Trust, G rant/Award Number :
ECF-2017-360
Abstract
Neuroanatomical reconstructions of extinct animals have long been recognized as
powerful proxies for palaeoecology, yet our understanding of the endocranial anat-
omy of dromaeosaur theropod dinosaurs is still incomplete. Here, we used X-ray
computed microtomography (µCT) to reconstruct and describe the endocranial
anatomy, including the endosseous labyrinth of the inner ear, of the small-bodied
dromaeosaur, Velociraptor mongoliensis. The anatomy of the cranial endocast and ear
were compared with non-avian theropods, modern birds, and other extant archo-
saurs to establish trends in agility, balance, and hearing thresholds in order to recon-
struct the trophic ecology of the taxon. Our results indicate that V. mongoliensis could
detect a wide and high range of sound frequencies (2,368–3,965 Hz), was agile, and
could likely track prey items with ease. When viewed in conjunction with fossils that
suggest scavenging-like behaviours in V. mongoliensis, a complex trophic ecology that
mirrors modern predators becomes apparent. These data suggest that V. mongoliensis
was an active predator that would likely scavenge depending on the age and health of
the individual or during prolonged climatic events such as droughts.
KEY WORDS
Dinosauria, Dromaeosauridae, endosseous labyrinth, neuroanatomy, sensory anatomy,
Theropoda
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   KING et al.
for Bambiraptor feinbergi (Burnham, 2004) has been partially
described and portions of the endocast of Saurornitholestes
langstoni, V. mongoliensis, Tsaagan mangas, and Deinonychus an-
tirrhopus have been measured for quantitative analysis or other-
wise imaged (Witmer and Ridgely, 2009; Zelenitsky et al., 2011;
Balanoff et al., 2013). There is, however, a distinct lack of de-
scribed endocasts with which to expand the palaeobiology of
dromaeosaurs in the formal literature to date. Although a few
publications have noted and discussed the implications of the
large endocranial space in dromaeosaurs (Hopson, 1977; Currie,
1995; Norell et al., 2004), relating the endocranial anatomy of
velociraptorine dromaeosaurs to their trophic ecology has yet to
be done in any c apacit y.
Evidence for the trophic ecology of V. mongoliensis, or at least
velociraptorine dromaeosaurs, is provided by a few different
sources. The most famous of these, the ‘fighting dinosaurs’ of
Inner Mongolia, preserves a glimpse into the predator–prey rela-
tionship between V. mongoliensis (IGM 100/25) and Protoceratops
andrewsi (IGM 100/512) (Carpenter, 1998). However, two other
V. mongoliensis specimens indicate what may be considered scav-
enging behaviour (Hone et al., 2010; 2012). Several previous
studies have explored the connection between endocranial anat-
omy, palaeoecology, and behaviour within theropod dinosaurs.
Medium- and large-bodied carnivorous theropods (e.g. tyranno-
saurids ( Witmer and Ridgely, 2009; Bever et al., 2011; Brusatte
et al., 2016; Kundrát et al., 2018; McKeown et al., 2020), abe-
lisaurids (Carabajal and Succar, 2015), carcharodontosaurids
(Franzosa and Rowe, 2005; Brusatte and Sereno, 2007; Carabajal
and Canale, 2010), megaraptorans (Carabajal and Currie, 2017),
and allosaurids (Rogers, 1999; Gleich et al., 2005)) as well as small
and medium-sized maniraptorans—e.g. oviraptorosaurs (Kundrát,
2007; Balanof f et al., 2018), therizinosaurs (Lautenschlager et al.,
2012), and others (Walsh et al., 2009; Zelenitsky et al., 2011)—
have been the focus of neurosensory studies. These studies often
are able to utilize structures reflected in the endocasts such as the
olfactory apparatus, cochlear ducts, and optic lobes to reconstruct
the posture and sensory capabilities for these extinct taxa. For
instance, quantitative and comparative analyses of tyrannosaurids
have found that they had the sensor y requirements for an active
predatory lifestyle (Witmer and Ridgely, 2009), and semicircular
canal morphologies have been found to correspond to quadru-
pedal and bipedal locomotor modes in dinosaurs (Georgi et al.,
2013). Even in herbivorous theropods, such as Erlikosaurus, strong
senses of smell, agility, eyesight, and hearing have been estimated
(Lautenschlager et al., 2012).
With this in mind, we explored the neuroanatomy of V. mongo-
liensis (IGM 100/976) in order to better estimate the trophic ecolog y
and sensory aptitude of this species—thus providing much needed
sensory and behavioural data for dromaeosaurs. Here, we describe
the anatomy of the hindbrain and inner ear of V. mongoliensis using
cranial endocasts and compare its neuroanatomy to extant reptil-
ian (including birds) taxa in order to place its sensor y abilities into a
broad palaeoecological context.
2 | METHODS
IGM 100/976 was collected as a part of the 1991 Joint Expedition
of the Mongolian Academy of Sciences and American Museum of
Natural History. This specimen was recovered from the Djadokhta
Formation at Tugrugeen Shireh, Mongolia (Norell et al., 1997) and
consists of a partial skeleton, including an incomplete braincase that
is missing the bones anterior to the basisphenoid and supraoccipitals
(Figure 1a,b). The braincase is comprised of a few incomplete ele-
ments—the exoccipitals, supraoccipital, and basioccipital. These four
element s are fused to form an incomplete adult endocranial space
where the sutures are obliterated along the surface (Norell et al.,
2004). Because of its incomplete nature, the endocast preserves the
entire hindbrain but only a featureless portion of the midbrain.
IGM 100/976 was scanned at the University of Texas High-
Resolution X-ray CT Facility in Austin, Texas, USA, producing
1024 × 1024 16-bit TIFF images. Scan parameters were as follows:
210 kV, 0.11 mA, intensity control on, high-power mode, no filter,
air wedge, no of fset, slice thick ness 1 line (0.08506 mm), source-ob-
ject distance 245 mm, 1,400 views, two samples per view, inter-slice
spacing 1 line (0.08506 mm), field of reconstruction 81 mm (max-
imum field of view 81.8084 mm), reconstruction of fset 8,700, re-
construction scale 4,000. Acquired with 31 slices per rotation and
25 slices per set. Ring-removal processing based on correction of
raw sinogram data using IDL routine ‘RK_SinoRingProcSimul’ with
parameter ‘bestof5 = 11’. Reconstruc ted with beam-hardening co-
efficients (0.0, 0.6, 0.1, 0.05), and a rotation of 4 degrees. Total final
slices = 450. Segmentation, reconstruction, and measurement col-
lection were conducted in Avizo Lit e (Thermo Fisher Scientific, 9.7.0)
and Amir A 2019.1 (Thermo Fisher Scientific).
The mean and high hearing frequencies for IGM 100/976 were
calculated following the method outlined in Walsh et al. (2009). To
accomplish these reconstructions, we took measurements from the
anterior-most extent of the basisphenoid to the posterior-most mar-
gin of the occipital condyle along with the length of the cochlear
duct (Table 1). The two measurement s were then used to calculate
a cochlear duct-basisphenoid ratio and then logarithmically trans-
formed. This normalized value was placed into pre-calculated formu-
lae found in Walsh et al. (2009).
Institutional abbreviations: IGM—Institute of Geology in Ulaan
Baatar, Mongolia; IVPP—Institute of Vertebrate Paleontolog y
and Paleoanthropology, Beijing, China; MPC-D—Paleontological
Laboratory of the Paleontological Center, Ulaan Baatar, Mongolia.
3 | RESULTS
3.1 | Cranial endocast
The identifiable regions of the brain preserved in the specimen are
limited to the hindbrain: the medulla and cerebellum, including its
floccular lobes. The flocculi are situated posterolaterally and orien-
tated posteriorly at 123° (Figure 1c,f) The bodies of the floccular
  
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KING et a l.
lobes are elongate, roughly circular in cross-section, and fill most of
the space between the anterior and posterior semicircular canals.
Each lobe extends well beyond the posterior margin of the anterior
canal and almost through the posterior semicircular canal of the en-
dosseous labyrinth. The flocculi together account for approximately
7% of the total hindbrain volume (Table 1).
The medulla is wider than tall and forms an almost oval shape
at the foramen magnum. As seen in most other maniraptorans, the
medulla is antero-posteriorly short and narrower than the rest of the
hindbrain (Kundrát, 2007; Balanoff et al., 2009; Lautenschlager et al.,
2012) (Table 1). Anteriorly, the medulla exhibits a gentle dorsolat-
eral constric tion between it and the cerebellum. Anteriorly, there is
a 132.94° angle between the hindbrain and midbrain. This pontine
flexure ( Table 1) implies that the brain exhibited a gentle curvature
and was not all located along the same horizontal plane. This cur va-
ture is unsurprising due to its presence in many non-maniraptoran
theropods (Sampson and Witmer, 2007; Witmer and Ridgely, 2009),
basal therizinosaurs (Lautenschlager et al., 2012), and oviraptoro-
saurs (Kundrát, 20 07; Balanoff et al., 2014).
As a whole, few anatomical structures are preserved on the en-
docast of the cerebellum. The hindbrain lacks a prominent dorsal
dural peak overlying the cerebellum that is found in some other man-
iraptorans such as Conchoraptor (Kundrát, 2007) and large-bodied
derived t yrannosaurs (Osborn, 1912; Witmer and Ridgely, 2009;
Bever et al., 2011; Brusat te et al., 2016). The absence of a large
dural peak is consistent with another velociraptorine dromaeosaur,
FIGURE 1 The braincase and
endocranium of Velociraptor mongoliensis
IGM 100/976. (a) Partial braincase in
anterolateral view. (b) Braincase rendered
transparent, revealing the in situ endocast
in anterolateral view. The labelled
endocast is presented in the right, (c), and
left (d) lateral, dorsal (e), and posterior
(f) views. Brain endocast is shown in
blue, veins in dark blue, cranial nerves in
yellow, and endosseous labyrinth in pink.
Scale bars: 5 mm. cb, cerebellum; pvcm,
posterior middle cerebral vein; fl, floccular
lobes; V, trigeminal nerve; VI, abducens
nerve; VII, facial nerve; X–XI, shared
foramina for the vagus and accessory
nerves
a
VI
V
cb
VII
pvcm
X-XI
fl
b
cd
ef
TABLE 1 Measurements taken from the endocast of IGM
100/976. Volumes do not account for vascularization, endosseous
labyrinths or cranial nerves.
Element measured
Minimum width 14.4 4 mm
Maximum width 28.49 mm
Cerebellum height 26.13 mm
Cerebellum width 15.75 mm
Total endocast length 22.79 mm
Pontine flexure angle 132.94°
Floccular lobe length 9.59 mm
Angle of floccular lobe orientation 123°
Total floccular volume 0.4 0 g/mm3
Total volume 5.73 g/mm3
Cochlear duct length 11.15 mm
Basisphenoid length 34.71 mm
4 
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   KING et al.
T. manga s (personal observation by the authors) and basal tyranno-
saurs (Kundrát et al., 2018); however, it is possible that this portion
of the endocast was not preser ved.
3.2 | Cranial nerves and vasculature
Both trigeminal ner ves (CN V) are preserved; each exiting the lateral
portions of the anteriormost endocast. The trigeminal is preserved
as a single nerve that likely diverged into its component branches
outside of the braincase as it does in other non-avian maniraptorans
(Figure 1c,d) (Currie, 1995). The abducens nerve (CN VI) is located
ventromedial to CN V (Figure 1c,d) and has an anterior trajec tory.
The endocasts of the abducens nerves are incomplete and project
anteriorly only a few millimetres before reaching the anterior limit of
the braincase. A short canal for the facial nerve (CN VII) lies on the
medulla at the level of the anterior edge of the endosseous labyrinth,
just posterolateral to CN V. Both the vagus and accessory nerves
(CN X–XI, respectively) exit a single ventrolaterally located foramen
along the posterior portion of the braincase (Figure 1e,f). While it is
located laterally near the posteriormost par t of the braincase, the
hypoglossal (CN XII) could not be reliably reconstruc ted even though
the CN XII foramina are visible on the external braincase (Norell
et al., 2004).
Norell et al. (2004) initially described the presence of vascula-
ture along the interior surfaces of the braincase in this specimen of
Velociraptor, although these could not be reconstructed digitally. The
occurrence of small veins in Velociraptor would not be surprising con-
sidering birds and their close relatives have a thin dural envelope and
a majority of their braincase filled with neural tissue (Norell et al.,
2004; Evans, 2005). Little of the venous architecture is preserved—
only the posterior middle cerebral veins are obser vable along the
posterodorsal surface of the cerebellum (Figure 1e).
3.3 | Endosseous labyrinth
Both endo sseous labyrint hs are preserve d in IGM 100/976 (Figure 2),
although the posterior por tion of the left labyrinth, i.e. where the
posterior semicircular canal meets the lateral canal, is not preserved
(Figure 2f ). In many respects, the vestibular anatomy of V. mo n-
goliensis is similar to that of other non-avian theropods (Balanoff
et al., 2009; Witmer and Ridgely, 2009; Lautenschlager et al., 2012).
Overall, the labyrinth has a somewhat triangular aspect in lateral
view, with all semicircular canals being approximately orthogonal to
each other. The anterior canal is taller than the posterior one and ex-
hibits only a slight curvature until it cur ves sharply ventrally to help
form the crus communis. The course of the anterior vertical canal
FIGURE 2 The endosseous labyrinth
of IGM 100/976. (a) Labelled right
labyrinth in lateral (left) and dorsal
(right) views. The right (b–e) and left
(f–i) labyrinths of IGM 100/976 shown
in lateral (b,f), posterior (c,g), anterior
(d,h), and dorsal (e,i) views. Scale bars:
5 mm. asc, anterior semicircular canal;
asca, ampulla of the anterior semicircular
canal; cc, crus communis; ecd, endosseous
cochlear duct; f v/fc, fenestra vestibuli and
fenestra cochleae (the division between
the two cannot be identified); lsc, lateral
semicircular canal; lsca, ampulla of the
lateral semicircular canal; psc, posterior
semicircular canal
ihg
f
edc
b
a
psc
fv/fc
ecd
cc asc
asca
lsca
asc
lsc
lsc
psc
ve
  
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KING et a l.
is planar and has a roughly uniform lumen thickness along its entire
length, except at the anterior ampulla where it meets the vestibule
(Figure 2).
The posterior and lateral canals are approximately equal in
length. The posterior canal deviates from planarity by exhibiting a
slight sinusoidal curvature along its course. Although the posterior
and lateral endosseous canals both appear to terminate posteriorly
in a confluence (Figure 2), the posterior semicircular duct of the
membranous labyrinth would have continued ventromedially and
expanded into its component ampulla (as discussed in Neenan et al.,
2018; Evers et al., 2019), and the lateral duct would have continued
medially to meet the vestibule. Similar to palaeognath birds, but
previously unknown in non-avian theropods, the medial extremity
of the posterior canal curves sharply ventrally and meet s the crus
communis in a position more anterolateral than the anterior canal
(Carabajal and Succar, 2015; Benson et al., 2017).
The lateral canal emerges anteriorly from a large but dorsoven-
trally compressed ampulla. Its course is planar and highly curved in
dorsal view, appearing to meet the vestibule at its posterior extreme
just anterior to the posterior vertical canal (Figure 2a,e,i). As men-
tioned above, however, the membranous duct would have continued
its loop medial to the posterior canal to meet the vestibule (e.g. Evers
et al., 2019).
The cochlear duct , which would have housed the basilar papilla,
the receptor organ for hearing, is relatively long in V. mongoliensis
compared with most non-avian theropods. It is also relatively wide
and follows a similar anteriorly orientated course as the crus com-
munis. The separation between the fenestra vestibuli and fenestra
cochleae (oval and round windows, respectively) cannot be dif feren-
tiated in this scan (Figure 2a,b,f).
4 | DISCUSSION
4.1 | Sensory abilities of Velociraptor
Floccular lobes are used to maintain head and eye stability during
movement within vertebrates and, as such, are frequently linked to
the agility of an organism (Witmer and Ridgely, 2009). As pointed
out in Walsh et al. (2013) and Ferreira-Cardoso et al. (2017), how-
ever, the size of the reconstructed flocculi do not necessarily reflec t
the actual volume of the lobes in life, as other anatomy (e.g. blood
vessels) may have also resided within the floccular fossae, making
them generally a poor indicator of flight style and ecology in birds
(e.g. powered flight vs. gliding). Nevertheless, relatively large floc-
cular fossae likely correlate with large flocculae despite extraneous
anatomical structures, and Walsh et al. (2013) further postulate that
enlarged flocculi in terrestrial birds could be an adaptation found
in bipeds to help stabilize the unstable nature of bipedalism. It is
therefore logical to interpret the floccular size in terrestrial, bipedal
maniraptorans, such as dromaeosaurs, as relating to balance—with
enlarged lobes corresponding to species that necessitated stable
bipedal movement. The flocculi of IGM 100/976 are massive and
suggest that quick movements and a stable gaze were essential to its
everyday life (Figure 1). This interpretation fits well with the current
idea that V. mongoliensis was a nimble predator that relied heavily on
its agility while pursuing and attacking prey. Moreover, as enlarged
floccular lobes have also been proposed to be indicative of strong
vestibulo-ocular (VOR) and vestibulocollic (VCR) reflexes (Hopson,
1977; Witmer and Ridgely, 2009), it can be reasoned that V. mongo-
liensis was able to track moving objects easily. With that being said,
because the optic lobes were not preser ved it is impossible to say at
this point to what degree IGM 100/976 relied on sight rather than
other senses. Based on the enlarged floccular lobes, elongated semi-
circular canals, and large orbit size of the species, it can be assumed
that the visual acuit y and field of view of V. mongoliensis was high
(Stevens, 20 06; Schmitz and Motani, 2011; Torres and Clarke, 2018).
This heightened optical sensitivity is not surprising considering the
hypothesized predatory lifestyle of V. mongoliensis. When combined
with its large flocculi and potentially sensitive VOR and VCR, it is
likely that V. mongoliensis was easily able to track and pursue its prey
smoothly based on its sensory neuroanatomy and stereoscopic vi-
sion (as determined from the position of the orbits).
In life, the endosseous cochlear duct of V. mongoliensis would
have housed the basilar papilla—the auditory organ of tetrapods
(Gleich et al., 2005; Walsh et al., 2009). As the length of the cochlear
duct has been interpreted as a rough measurement of the basilar
papilla, the length of the duc t can be used as an estimator of hear-
ing frequencies in non-avian dinosaurs (Witmer and Ridgely, 2009;
Lautenschlager et al., 2012). Moreover, the relationship between
the length of the cochlear duc t and the basisphenoid has also been
shown to correlate with hearing frequencies in modern archosaurs
(Walsh et al., 20 09), thus providing a way to calculate mean and high
frequencies of non-avian dinosaurs. A recent study using extant
turkeys demonstrated that a shape analysis of a single endosseous
labyrinth can be used to represent an entire population (Cerio and
Witmer, 2019); we therefore suggest that the hearing frequencies
calculated in this study can be used as proxies for high and average
hearing frequencies for V. mongoliensis. By measuring and logarith-
mically transforming the ratio between the cochlear duct leng th and
the total length of the basisphenoid, a mean hearing range (2,368 Hz)
and high-frequency hearing limit (3,965 Hz) was calculated for IGM
100/976—a range that is comparable to birds such as the common
raven (Corvus corax) and the African penguin (Spheniscus demersus)
(Walsh et al., 2009). Unsurprisingly, the scaled anteroposterior width
and length of the cochlear duct were much more similar to birds—
specifically neognaths such as budgerigars (Melopsittacus undulatus),
storks (Ciconia ciconia), and mute swans (Cygnus olor) —than to more
basal archosaurs and other reptiles (Figure 3).
Our results indicate that V. mongoliensis could hear, hunt, and
perhaps vocalize most efficiently in the range of 2,400 Hz. When
compared with other maniraptorans for which data are available,
the mean hearing frequency of V. mongoliensis is high. For instance,
the mean and high hearing frequencies estimated for the basally di-
verging therizinosaur Falcarius utahensis are 1,630 Hz and 4,0 00 Hz,
respectively (Lautenschlager et al., 2012). Similarly, the frequency
6 
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   KING et al.
range of the more derived therizinosaurid Erlikosaurus andrewsi has
a high range between 1,600 and 4,000 Hz (Lautenschlager et al.,
2012). Although the mean frequency range of V. mongoliensis is no-
tably higher than that of therizinosaurs, the high-frequency values
are roughly the same.
The elongate nature of the cochlear duct support s the hypoth-
esis that V. mongoliensis was capable of detecting a wide range of
sounds, indicating that hearing was likely an impor tant sensory
system in this taxon (Manley, 1990; Walsh et al., 2009; Witmer
and Ridgely, 2009; Brusatte et al., 2016; Carabajal et al., 2016).
In fact, IGM 100/976 plots closest to the social vocal learner
Melopsittacus undulatus (budgerigar), making it feasible that
V. mongoliensis utilized hearing in social interactions as well as ac-
tive predation (Figure 3).
4.2 | The trophic ecology of Velociraptor
Dinosaur feeding styles, such as predation vs. scavenging, have
been a topic of popular interest in the past but remain difficult
to diagnose in the fossil record (Holtz, 2008). Our current un-
derstanding of the trophic ecology of V. mongoliensis is provided
by several sources. The most famous of these, the ‘fighting di-
nosaurs’ (IGM 100/25) of Mongolia, preserves what has been
interpreted by some palaeontologists as a predation attempt of
a Velociraptor on a Protoceratops (Carpenter, 1998). However,
further evidence has emerged in recent years suggesting that
V. mongoliensis was not an obligate predator. This includes
Velociraptor tooth marks on bones, which have been interpreted
as late stage scavenging, and the preser ved gut contents of a
subadult individual (Hone et al., 2010; 2012). Each of these spec-
imens indicate that scavenging was a part of the trophic ecology
of V. mongoliensis. The neuroanatomical results described in this
study help flesh out the degree to which scavenging contributed
to the diet of V. mongoliensis.
Our current understanding of the neuroanatomy of V. mongolien-
sis suggests that predation likely made up a large part of its diet.
As with therizinosaurs and oviraptorosaurs, IGM 100/976 possesses
relatively enlarged flocculi (Figure 1c,e; Lautenschlager et al., 2012;
Balanoff et al., 2018). However, the flocculi of IGM 100/976 surpass
those of observed therizinosaurs and almost completely fill the in-
terior space between the semicircular canals. Enlarged flocculi have
been used to predict prey tracking capabilities and may imply that
the species had an acute vestibulo-ocular reflex (Walsh et al., 2013).
This evidence in conjunction with the wide field of binocular vision,
extended hearing range (as determined from this study), and skeletal
morphology indicates that rather than being equally or more reli-
ant on scavenging, V. mongoliensis was well-equipped to be an ac tive
pr ed at or.
The fossil record, however, indicates that scavenging was at
least a small part of the diet in V. mongoliensis (Hone et al., 2010,
2012). Opportunistic scavenging is supported by gut contents re-
covered from MPC-D100/54 that include a 75-mm-long bone of an
unidentified pterosaur. Whether this represents an act of osteoph-
agy or scavenging due to an injury or its small size, it is probable that
the pterosaur was dead prior to being eaten, given its incomplete
nature. In the case of IVPP V16137, a probable Protoceratops, multi-
ple bone fragment s including a dentary, exhibited bite marks char-
acteristic of velociraptorine dromaeosaurs. Velociraptorine teeth
(IVPP V16138) were also found in association with IVPP V16137,
further indicating that a velociraptorine dromaeosaur was feeding
on the carcass of IVPP V16137. Some of these tooth drag marks
found along the anterior portion of the dentary suggest that this
was an instance of late-stage scavenging by V. mongoliensis due to
the lack of significant muscle mass located along a dentary during
life. While this evidence for scavenging can be interpreted as being
somewhat circumstantial, we accept that the specimens neverthe-
less show enough evidence to be considered acts of scavenging
rather than active predation based on the conclusions of previous
studies (Hone et al., 2010; 2012).
This type of flexible hunting strateg y is not surprising given
that modern predator diets are a spectrum rather than an ‘either/
or’ scenario in which seasonality, fitness, and other ecological con-
straints are the primary drivers (Mattisson et al., 2016). Here we
propose the fossil evidence indicates a scavenging behaviour that
complimented an active predatory lifestyle—similar to what can be
found in the modern biota. Modern predators, including predatory
FIGURE 3 Scaled endosseous cochlear duct (ECD) length
against scaled ECD anteroposterior width, with some taxa
highlighted. Velociraptor mongoliensis grouped more closely with
birds rather than wiith Crocodyliformes and non-archosaurs. The
scaled measurements of IGM 100/976 most closely resembled
the upper range of vocal/social neognath birds. A.n, Ahaetulla
nasuta; C.j, Crocodylus johnstoni; C.n, Ciconia nigra; C.o, Cygnus olor;
C.s, Chelydra serpentina; Ci.c, Ciconia ciconia; Co.c, Corvus corax;
D.n, Dromaius novaehollandiae; G.g, Gymnodactylus geckoides; L.m,
Luscinia megarhynchos; M.u, Melopsittacus undulatus; P.e, Psittacus
erithacus; S.c, Struthio camelus; S.p, Sphenodon punctatus; T.a,
Tyto alba; T.s , Tomistoma schlegelii; V.m, Velociraptor mongoliensis.
Modified from Walsh et al. (20 09)
0.10 0.15 0.20 0.25 0.30 0.35 0.40 0.45
Scaled ECD anteroposterior width
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
Scaled ECD length
Velociraptor
Aves - Neognathae
Aves - Palaeognathae
Crocodylia
Testudines
Serpentes
Squamata excl. Serpentes
Rhynchocephalia
0.05
V.m
D.n
T.sC.j
C.s
S.p
S.c
A.n
G.g
M.u
L.m
Co.c
T.a
Ci.c
C.n
P.e
C.o
  
|
 7
KING et a l.
birds such as Aquila chrysaetos, often resort to changes in hunting
behaviour, or even scavenging, when prolonged weather patterns,
injury or ontogenetic stage forces them to find alternative food
sources (Tjernberg, 1981; Marchetti and Price, 1989; Wilmers
et al., 2003; Mattisson et al., 2016). It follows that the neuroanat-
omy of V. mongoliensis suggests a behaviour that is adapted for
active predation (C arpenter, 1998); however, young or injured in-
dividuals and those experiencing diet ary constraints brought on
by local climate would have actively sought out carcasses for an
easy meal.
5 | CONCLUSIONS
The neuroanatomy and sensory capabilities of V. mongoliensis are
described here for the first time and are subsequently used to put
this taxon into a larger palaeobiological context. Evidence from the
hindbrain and labyrinth of IGM 100/976 suggests that V. mongolien-
sis had an average hearing range near 2,400 Hz (similar to modern
social birds such as ravens and penguins), highly sensitive vestib-
ulo-ocular and vestibulocollic reflexes, and a fine-tuned sense of
balance—all of which would have been advantageous as an active
predator. Although previous studies have used gut contents and
tooth marks on Protoceratops mandibles to provide evidence that
scavenging was a part of V. mongoliensis trophic ecology, most evi-
dence, including the neuroanatomy, suggests an active predatory
lifestyle. Therefore, we interpret the presence of scavenging as a
facet of the trophic ecology for V. mongoliensis. Based on the behav-
iour of modern bird taxa, our better understanding of velocirapto-
rine senses, the apparent case of a predation event in the ‘fighting
dinosaurs’, and the age/health/environment of the scavenging indi-
viduals, it is likely that V. mongoliensis was an active predator that
would readily rely on carrion in the event that a ready source of
prey items was not available.
ACKNOWLEDGEMENTS
We thank Mark Norell (AMNH) for granting access to the specimen
and Matthew Colbert (University of Texas at Austin) for conduct-
ing the scanning. Additionally, we would like to thank Steve Brusatte
(University of Edinburgh) and Stig Walsh (National Museums
Scotland) for kindly reviewing the manuscript. Duncan Murdock and
Imran Rahman (both University of Oxford) are also thanked for fruit-
ful discussions. This project was funded by a Leverhulme Trust Early
Career Fellowship (ECF-2017-360) awarded to J.M.N.
CONFLICT OF INTEREST
The authors declare no conflict of interest.
AUTHOR CONTRIBUTIONS
J.L.K. and J.M.N conceived the study. J.L.K reconstructed the 3D
brain endocast, performed the sensory calculations, and drafted/
revised the manuscript. J.M.N reconstructed and described the
labyrinths and assisted in writing the manuscript. J.S.S. and J.A.G.
provided the CT data, gave anatomical considerations for the pro-
ject, and edited the initial drafts of the manuscript. A.M.B. provided
expert knowledge and edited the final drafts of the paper.
DATA AVAIL ABI LIT Y S TATEM ENT
The 3D models produced in this study are openly available from
MorphoSource at https://www.morphosource.org/Detail/Project
Detail/Show/project_id/1019.
ORCID
J. Logan King https://orcid.org/0000-0003-2104-4187
Justin S. Sipla https://orcid.org/0000-0001-8171-8126
Justin A. Georgi https://orcid.org/0000-0002-3859-9528
James M. Neenan https://orcid.org/0000-0002-8215-5748
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How to cite this article: King JL, Sipla JS, Georgi JA, Balanoff
AM, Neenan JM. The endocranium and trophic ecology of
Velociraptor mongoliensis. J. Anat. 2020;00:1–9. ht t p s :// d oi .
org /10.1111/j oa.13253
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... When compared to the vestibular portion of the endosseous labyrinth, the cochlear duct is approximately the same length with no evidence of twisting or further curvature beyond its medial de ection. The cochlear duct is also thick as is the case in Velociraptor (King et al. 2020). Both the left and right cochlear ducts are similar in size, shape, and angle. ...
... Both the left and right cochlear ducts are similar in size, shape, and angle. Laterally, the fenestra vestibuli and fenestra cochleae are not visible but do not seem to have created a small pro le that took do not seem to have taken up a large area -unlike those found in Velociraptor (King et al. 2020) Geometric Morphometric Analysis Prior to collection of landmark data from Sinovenator, the endocast was virtually mirrored to enable collection of arti cially 'left' sided landmarks, then subsequently retrodeformed using median and several pairs of bilaterally symmetric landmarks. While the retrodefomed virtual endocast still exhibited some deformation, we conducted shape analysis on clearly identi able landmarks that characterize the overall con guration of the neuroanatomical regions. ...
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... ambush predators, amphibious predators, scavengers) and diet breadth (e.g. birds, insects, lizards) [98][99][100][101][102][103][104][105][106] . Our analyses did not detect interactions between carnivorous families, which agrees with evidence from stable isotopes that theropods had different niches within the predator guild, suggesting plausible means by which ecospace was divided among the predatory dinosaurs 107,108 . ...
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Unraveling the origins of the character complexes diagnosing major crown clades is one of the greatest challenges in evolutionary biology. These origination events tend to optimize along extraordinarily long stem lineages where the comparative biology of extant lineages is relatively weak in its heuristic power. Here we add to a growing paleontological literature on the evolutionary origins of the modern avi an brain by describing the endocranial casts of two oviraptorosaur dinosaurs, Citipati osmolskae and Khaan mckennai. These fossil data confirm the antiquity of several avian features, including the expanded cerebrum. They also extend our appreciation of both the inherent variability in the brain-skull relationship along the avian stem and the dynamic nature of these crown characters in the earliest history of their expression.
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The bony labyrinth of vertebrates houses the semicircular canals. These sense rotational accelerations of the head and play an essential role in gaze stabilisation during locomotion. The sizes and shapes of the semicircular canals have hypothesised relationships to agility and locomotory modes in many groups, including birds, and a burgeoning palaeontological literature seeks to make ecological interpretations from the morphology of the labyrinth in extinct species. Rigorous tests of form–function relationships for the vestibular system are required to support these interpretations. We test the hypothesis that the lengths, streamlines and angles between the semicircular canals are related to body size, wing kinematics and flying style in birds. To do this, we applied geometric morphometrics and multivariate phylogenetic comparative methods to a dataset of 64 three-dimensional reconstructions of the endosseous labyrinth obtained using micro-computed tomography scanning of bird crania. A strong relationship between centroid size of the semicircular canals and body size indicates that larger birds have longer semicircular canals compared with their evolutionary relatives. Wing kinematics related to manoeuvrability (and quantified using the brachial index) explain a small additional portion of the variance in labyrinth size. We also find strong evidence for allometric shape change in the semicircular canals of birds, indicating that major aspects of the shape of the avian labyrinth are determined by spatial constraints. The avian braincase accommodates a large brain, a large eye and large semicircular canals compared with other tetrapods. Negative allometry of these structures means that the restriction of space within the braincase is intense in small birds. This may explain our observation that the angles between planes of the semicircular canals of birds deviate more strongly from orthogonality than those of mammals, and especially from agile, gliding and flying mammals. Furthermore, we find little support for relationships between labyrinth shape and flying style or wing kinematics. Overall, our results suggest that the topological problem of fitting long semicircular canals into a spatially constrained braincase is more important in determining the shape of the avian labyrinth than the specifics of locomotory style or agility. Our results tentatively indicate a link between visual acuity and proportional size of the labyrinth among birds. This suggests that the large labyrinths of birds compared with other tetrapods may result from their generally high visual acuities, and not directly from their ability to fly. The endosseous labyrinths of extinct birds and their close dinosaurian relatives may allow broad inferences about flight or vision, but so far provide few specific insights into detailed aspects of locomotion.