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Digital Cranial Endocasts of the Extinct Sloth Glossotherium robustum (Xenarthra, Mylodontidae) from the Late Pleistocene of Argentina: Description and Comparison with the Extant Sloths

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Journal of Mammalian Evolution
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The internal cranial morphology of the terrestrial sloth Glossotherium robustum is described here based on a neurocranium from the late Pleistocene of the Pampean region of Buenos Aires, northeastern Argentina. The first published data on the morphology of the brain cavity of this species date back to the latest nineteenth century. The novel techniques of CT scanning and digital reconstructions enable non-destructive access to the internal cranial features of both extinct and extant vertebrates, and thus improve our knowledge of anatomical features that had previously remained obscure. Therefore, we performed CT scans on the posterior half of a skull of G. robustum and created digital models of the endocasts and internal structures. The results reveal the morphology of the brain cavity itself, as well as the paranasal sinuses and the trajectory of several cranial nerves and blood vessels. These features have been compared with the two extant folivoran genera, the two-toed sloth Choloepus and the three-toed sloth Bradypus. For many characteristics, especially those related to the paranasal pneumaticity and the brain cavity, a closer similarity between Glossotherium and Choloepus is observed, in accordance with the most widely accepted phylogenetic scenarios. However, other features are only shared by the two extant genera, but are probably related to allometric effects and the convergence that affected the two modern lineages. This study, which represents the first exhaustive analysis of digital endocasts of a fossil sloth, reveals the importance of the application of new methodologies, such as CT scans, for elucidating the evolutionary history of this peculiar mammalian clade.
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ORIGINAL PAPER
Digital Cranial Endocasts of the Extinct Sloth Glossotherium robustum
(Xenarthra, Mylodontidae) from the Late Pleistocene of Argentina:
Description and Comparison with the Extant Sloths
Alberto Boscaini
1
&Dawid A. Iurino
2,3
&Raffaele Sardella
2,3
&German Tirao
4
&Timothy J. Gaudin
5
&François Pujos
1
#Springer Science+Business Media, LLC, part of Springer Nature 2018
Abstract
The internal cranial morphology of the terrestrial sloth Glossotherium robustum is described here based on a
neurocranium from the late Pleistocene of the Pampean region of Buenos Aires, northeastern Argentina. The first
published data on the morphology of the brain cavity of this species date back to the latest nineteenth century. The novel
techniques of CT scanning and digital reconstructions enable non-destructive access to the internal cranial features of both
extinct and extant vertebrates, and thus improve our knowledge of anatomical features that had previously remained
obscure. Therefore, we performed CT scans on the posterior half of a skull of G. robustum and created digital models of
the endocasts and internal structures. The results reveal the morphology of the brain cavity itself, as well as the paranasal
sinuses and the trajectory of several cranial nerves and blood vessels. These features have been compared with the two
extant folivoran genera, the two-toed sloth Choloepus and the three-toed sloth Bradypus. For many characteristics,
especially those related to the paranasal pneumaticity and the brain cavity, a closer similarity between Glossotherium
and Choloepus is observed, in accordance with the most widely accepted phylogenetic scenarios. However, other features
are only shared by the two extant genera, but are probably related to allometric effects and the convergence that affected
the two modern lineages. This study, which represents the first exhaustive analysis of digital endocasts of a fossil sloth,
reveals the importance of the application of new methodologies, such as CT scans, for elucidating the evolutionary history
of this peculiar mammalian clade.
Keywords Extinct sloth Glossotherium .Endocast .Brain cavity .Cranial nerves .Paranasal sinuses .Blood vessels
Introduction
Xenarthrans are among the most peculiar mammals of the
South American endemic Cenozoic fauna (Simpson 1980).
South Americas period of isolation began in the late
Paleocene, when its land connection with Antarctica was lost
(Reguero et al. 2014), and finished with the formation of the
Panamanian isthmus and connection with North America,
around 2.8 Ma (Woodburne 2010). During the Tertiary period,
only some sweepstakesor island hoppinginterchanges
took place, such as the middle Eocene and early Oligocene
immigration of rodents and primates, respectively, from
Africa (Antoine et al. 2012). Other migrations before the
G.A.B.I. (Great American Biotic Interchange) were observed
in the early Miocene (about 18 Ma, through the West Indies)
and in the late Miocene (about7 Ma, probably through Central
*Alberto Boscaini
aboscaini@mendoza-conicet.gob.ar; alberto.boscaini@gmail.com
1
Instituto Argentino de Nivología, Glaciología y Ciencias
Ambientales (IANIGLA), CCT-CONICET-Mendoza, Avda. Ruiz
Leal s/n, Parque Gral. San Martín, 5500 Mendoza, Argentina
2
Dipartimento di Scienze della Terra, Sapienza Università di Roma,
Piazzale A. Moro 5, 00185 Rome, Italy
3
PaleoFactory, Sapienza Università di Roma, Piazzale A. Moro 5,
00185 Rome, Italy
4
IFEG (CONICET), Facultad de Matemática, Astronomía y Física,
Universidad Nacional de Córdoba, Haya de la Torre y Medina
Allende, X5000HUA Córdoba, Argentina
5
Department of Biology, Geology, and Environmental Sciences,
University of Tennessee at Chattanooga, 615 McCallie Ave,
Chattanooga, TN 37403-2598, USA
Journal of Mammalian Evolution
https://doi.org/10.1007/s10914-018-9441-1
America) (MacPhee and Iturralde-Vinent 1994,1995; Pascual
2006; McDonald and De Iuliis 2008).
The fossil record of xenarthrans begins soon after the sepa-
ration of South America and Antarctica, in the early Eocene,
with armadillos from the Itaboraí fauna (Itaboraian SALMA
[South American Land Mammal Ages], southeastern Brazil;
Bergqvistetal.2004; Gelfo et al. 2009) and continues through-
out the Cenozoic, with representatives of all three major groups
of Xenarthra persisting to the present: Cingulata (armadillos;
also including extinct glyptodonts and pampatheres),
Vermilingua (anteaters), and Folivora (sloths) (e.g., Engelmann
1985;Gaudin2004).AccordingtoGaudinandCroft(2015), the
oldest representatives of these clades date back to the early
Eocene, the early Miocene, and the late Eocene, respectively.
Folivora (=Tardigrada = Phyllophaga; Delsuc et al. 2001;
Fariña and Vizcaíno 2003) includes all extant and extinct
sloths, the diversity of which is considerably more pro-
nounced in the fossil record than in the present day (more
than 90 fossil genera against the only two surviving ones,
Bradypus and Choloepus; McKenna and Bell 1997). The di-
phyletic origin of the two extant sloth genera is henceforth
accepted (e.g., Gaudin 2004; Pujos et al. 2017): recent phylo-
genetic analysis based on osteological characters (e.g., Gaudin
1995,2004) consider Bradypus thesolerepresentativeof
Bradypodidae and the sister taxon of the other sloths, and
Choloepus as the only living member of Megalonychidae.
The other three extinct sloth clades are the Nothrotheriidae,
the Megatheriidae, and the Mylodontidae (e.g., Engelmann
1985;Gaudin2004; McDonald and De Iuliis 2008), but their
relationships are still debated (e.g., Gaudin 2004; Slater et al.
2016). The successful radiations of mylodontid and
megalonychid sloths, the first to appear in the fossil record,
took place in the lateOligocene, as documented by the numer-
ous sloth skeletal remains referable to the Deseadan SALMA,
and persisted until the late Pleistocene/Holocene periods
(Gaudin and Croft 2015;Slateretal.2016; Pujos et al. 2017).
Among the Mylodontidae, Glossotherium (literally Tongue
Beast) was historically the first genus described (Owen 1839).
The name was inspired by the exceptional size of the stylohyal
fossa and the hypoglossal foramen, two basicranial structures
directly linked to the tongue (the first in providing a synovial
attachment for the stylohyal bone, part of the massive hyoid
apparatus (Pérez et al. 2010) that served for attachment of
tongue muscles, and the second for passage of the hypoglossal
nerve [XII] that innervates the tongue muscle; Owen 1839). The
robust tongue, coupled with the action of the lips, facilitated
food intake in this extinct sloth, the diet of which was mainly
comprisedofgrassandherbaceousplants(Bargoetal.2006b;
Bargo and Vizcaíno 2008). Glossotherium has, in fact, often
been associated with open and temperate habitats
(Czerwonogora et al. 2011) and commonly recovered in
Pleistocene localities from austral areas of the South American
continent (e.g., Pitana et al. 2013; Varela and Fariña 2016).
The taxonomic history of Glossotherium is confusing
(Mones 1986, listed 32 specific and sub-specific names), and
highly convoluted (for a resume, see Esteban 1996; Fernicola et
al. 2009;McAfee2009; De Iuliis et al. 2017). A recent detailed
systematic revision performed by Esteban (1996) recognized
only two Glossotherium species: G. robustum and G.
chapadmalensis.McAfee(2009) shared the same opinion, even
though he allowed for the possibility that G. chapadmalensis
belonged to another genus (i.e., Eumylodon), following the
original description of Kraglievich (1925). Recently, Pitana et
al. (2013) also considered valid G. lettsomi from the Pleistocene
of Argentina, Chile, and Uruguay (Ameghino 1889;Pitanaet
al. 2013 and references therein), G. wegneri from the
Pleistocene of Brazil and Ecuador (Hoffstetter 1952;Simpson
and Paula-Couto 1981), G. tropicorum from the late
Pleistocene of Ecuador and Venezuela (Hoffstetter 1952;
Bocquentin 1979), and an indeterminate Glossotherium spe-
cies, widely distributed into the intertropical latitudes of the
South American continent. In the most recently updated listing
of extant and extinct sloths, Pujos et al. (2017) ascribed four
species under the genus Glossotherium:G. robustum,G.
tarijensis,andG. tropicorum, and the intertropical
Glossotherium species (currently under study by Cartelle and
colleagues). Recently, De Iuliis et al. (2017) performed a com-
prehensive revision of G. tropicorum from the late Pleistocene
of Ecuador and Peru.
Considering this context, a detailed and comprehensive
revision of the genus is necessary. However, for the purposes
of the present study, the target taxon G. robustum, the type
species of the genus Glossotherium, remains indisputably rec-
ognized as a valid taxon. It is also the best known and geo-
graphically most widely distributed species of Glossotherium
in South America (McAfee 2009; Pitana et al. 2013).
In recent years, diverse studies have focused on G.
robustum, increasing knowledge of several aspects of its paleo-
biology, such as its body mass (Christiansen and Fariña 2003),
digging abilities (Bargo et al. 2000;Vizcaínoetal.2001), die-
tary preferences and food intake (Bargo et al. 2006a,b;Bargo
and Vizcaíno 2008; Pérez et al. 2010; Czerwonogora et al.
2011), and hearing capabilities (Blanco and Rinderknecht
2008,2012). Furthermore, its paleobiogeography has been an-
alyzed in detail (i.e., Varela and Fariña 2016), and several diag-
nostic anatomical features have been clarified (McAfee 2009;
Pitana et al. 2013).
Nevertheless, studies on the internal cranial anatomy of
Glossotherium have been long neglected and, to date, digital
endocast reconstructions are unknown in this or any other fossil
sloth. Indeed, studies of the encephalic cavity of fossil sloths and
the brains of living sloths, date back to the nineteenth century
(e.g., Gervais 1869; Elliot-Smith 1898). Additional descriptive
works on the anatomy of the internal encephalic cavitiy of ex-
tinct sloths were conducted by Colette Dechaseaux in the mid-
twentieth century (Dechaseaux 1958,1962a,b,1971). This
J Mammal Evol
author described and figured many fossil genera, such as
Glossotherium,Hapalops, Lestodon, Megatherium,and
Oreomylodon, based on plaster casts of the brain cavity, the most
commonly employed technique at that time [(Dechaseaux 1958,
1962a,b,1971; regarding the latter genus, the revisions of St-
André et al. (2010) and Antoine et al. (2017) are followed here,
in recognizing Oreomylodon as a separate genus, rather than a
subgenus of Glossotherium, as in Hoffstetter (1952)]. Following
the same methodology, Dozo (1987,1994) studied the middle
Miocene forms Eucholoeops and Hapalops from Santa Cruz
Province.
To our knowledge,only limited information is available on
the paranasal pneumaticity in xenarthrans, and exhaustive
studies are restricted to two representatives of Cingulata: the
extant genus Dasypus (Billet et al. 2017) and the peculiar
extinct glyptodont Neosclerocalyptus (Fernicola et al. 2012).
The most detailed study on sinuses in anteaters is that of
Storch and Habersetzer (1991). The morphology of the frontal
sinuses in extant sloths was briefly mentioned by Moore
(1981), Langworthy (1935), and Goffart (1971)for
Choloepus, and illustrated for Bradypus and Choloepus by
Naples (1982) using radiographs. In extinct sloths, some an-
notations on the development of frontal and sphenoidal
sinuses are mentioned in Dechaseaux (1971) and McDonald
et al. (2013), respectively, concerning the mylodontid
Oreomylodon and the megalonychid Megistonyx. Pterygoid
and epitympanic sinuses in the squamosal are described by
Patterson et al. (1992) for several extinct sloths. These authors
noted the remarkable pneumatization of the skull in the large
Pleistocene Antillean sloth Megalocnus. Inflation of the pter-
ygoid and frontal bones was codified as characters 137 and
174 by Gaudin (2004:appendix2).
The aims of the present work are to provide the first digital
reconstruction of a fossil sloths endocranial casts, with pre-
liminary discussions on their possible phylogenetic, allome-
tric, and functional value. Particular emphasis is placed on the
brain cavity, along with the cranial nerves, the intracranial
vasculature, and the pneumatized structures of the cranium,
to provide an anatomical characterization of the main features,
alongside comprehensive comparisons with the available lit-
erature (Gervais 1869; Dechaseaux 1958,1962a,b,1971;
Dozo 1987,1994). However, due to a paucity of data on these
features in extinct sloths, the structures in Glossotherium will
be compared with their homologues in the extant Bradypus
and Choloepus.
Materials and Methods
The neurocranium of Glossotherium robustum (MACN Pv
13553; see below for institutional abbreviations) was recov-
ered in 1933 near the city of Tandil (Buenos Aires Province,
Argentina). It was scanned using the General Electric
Lightspeed CTscanner in FUESMEN institute. The scanning
resulted in 839 slices with a slice thickness of 0.62 mm. The
comparative sample is based on two complete skulls of the
extant sloths Choloepus hoffmanni (AMNH 30765) and
Bradypus variegatus (AMNH 95105). Their CT images were
downloaded from the Digital Morphology library (www.
digimorph.org). Choloepus hoffmanni (AMNH 30765) was
scanned with a slice thickness of 0.241 mm, producing a
total of 441 slices, whereas the slice thickness for B.
variegatus (AMNH 95105) was 0.197 mm, yielding a total
of 369 slices. The image segmentation process for the three
specimens was performed using the digital tools from OsiriX
v.5.6 32-bit and Materialise Mimics v.17. The 3D models of
skulls, brains, frontal sinuses, and inner ears, exported from
Mimics as .PLYfiles, were converted to .OBJformat and
imported into ZBrush 4R6 for the rendering process. Because
of the presence of infilled sediment in different cranial cavities
of MACN Pv 13553, the segmentation process was carried out
manually, slice-by-slice.
All the specimens considered in this study are adults, as
shown by the complete fusion of cranial sutures. Analyzing
taxa of comparable developmental stages helps to avoid var-
iability due to ontogenetic development.
Identification of endocranial structures was based on pre-
vious descriptions of sloth endocasts (e.g., Dechaseaux 1958,
1962a,b,1971;Dozo1987,1994), as well as classic manuals
on the anatomy of domestic mammals (Evans 1993;Barone
and Bortolami 2004; Constantinescu and Schaller 2012)and
extant xenarthrans (Hyrtl 1854; Tandler 1901; Bugge 1979).
All data generated or analyzed during the current study are
available from the corresponding author on reasonable request.
Institutional Abbreviations
A, Gervais Collection, Laboratoire dAnatomie Comparée du
Muséum National dHistorie Naturelle, Paris, France;
AMNH, American Museum of Natural History, New York,
USA; FUESMEN, Fundación Escuela de Medicina Nuclear,
Mendoza, Argentina; MACN Pv, Colección de Paleontología
de Vertebrados, Museo Argentino de Ciencias Naturales
Bernardino Rivadavia,Buenos Aires, Argentina.
Systematic Paleontology
Superorder XENARTHRA Cope, 1889
Order PILOSA Flower, 1883
Suborder FOLIVORA Delsuc et al., 2001
Family MYLODONTIDAE Gill, 1872
Subfamily MYLODONTINAE Gill, 1872
Genus Glossotherium Owen, 1839
Glossotherium robustum (Owen, 1842)
JMammalEvol
Referred Material MACN Pv 13553, neurocranium (Fig. 1).
This specimen consists of the posterior portion of a skull of
G. robustum. The cranial roof and the anterior half of the
skull are lacking, exposing the sinuses that comprise the
pneumatized structures around the braincase (Fig. 1). The
zygomatic processes of both squamosals are also broken at
their bases. The external aspect of this specimen and the
anatomy of the inner ear have been recently described in
detail by Boscaini et al. (2018).
Stratigraphic and Geographic Occurrence Upper Pampean
Formation (late Pleistocene), Tandil, Buenos Aires Province,
Argentina.
Description and Comparison
Brain Endocast
The 3D model of the brain digital endocast of Glossotherium
is almost complete, with the exception ofthe dorsal portion of
the left olfactory bulb, which was impossible to reconstruct
due to the lack of bony material (Fig. 2ad). In general, the
external surface is well preserved and the pattern of convolu-
tions and the majority of blood vessels and nerves are recog-
nizable. As expected, the brain of Glossotherium was consid-
erably larger than that of the extant forms Choloepus and
Bradypus, both in terms of linear measures and volume (Fig.
2). At first glance, the patterns of convolutions in the cerebral
hemisphere of these three genera are different, with
Glossotherium showing a higher level of complexity than
the endocasts of the two extant taxa (Fig. 2).
However, the seemingly higher degree of complexity is not
related to an increase in number of the convolutions, but to the
presence of surface irregularities. These latter are in fact small
recesses and protrusions of irregular shape and limited extent,
not compatible with the morphology of convolutions men-
tioned in the literature (e.g., Barone and Bortolami 2004). A
similar high degree of complexity is observed in other extinct
giant sloth genera such as Lestodon,Megatherium,Mylodon,
Oreomylodon,andScelidotherium (Gervais 1869;
Dechaseaux 1958,1962a,b,1971), and to a lesser extent in
the small-sized extinct early sloths Hapalops and
Eucholoeops (Dozo 1987,1994).
In Glossotherium, the cerebrum is globular. The cerebral
hemispheres arch strongly dorsally, and are separated by a very
deep longitudinal fissure (Fig. 2ad). In dorsal view the fissure
is especially deep and wide anteriorly, imparting a peculiar
walnut kernelshape to the brain. In Choloepus and
Bradypus, the hemispheres are less arched and the longitudinal
fissure less prominent than in Glossotherium (Fig. 2el). The
morphology of the extant sloths more closely resembles that of
Hapalops and Eucholoeops (Dozo 1987,1994).
In dorsal view (Fig. 2a, e, i), the symmetric convolutions are
represented mainly by the lateral and suprasylvian gyri, ar-
ranged similarly anteroposteriorly in Glossotherium,
Choloepus,andBradypus. The occipital gyri are oriented
mediolaterally, emphasizing the transverse fissure that separates
the telencephalon from the cerebellum. The entolateral sulcus,
which divides the lateral gyrus anteroposteriorly into medial
and lateral portions, is a feature shared only by Glossotherium
and Choloepus.ItisabsentinBradypus (Fig. 2a, e, i).
The dorsal surface of the telencephalon of Lestodon,
Megatherium,Mylodon,Oreomylodon,Scelidotherium
(Gervais 1869;Dechaseaux1958,1962a,b,1971), and the
Fig. 1 Posterior portion of the cranium of Glossotherium robustum (MACN Pv 13553) in dorsal (a) and ventral (b) views. Scale bar equals 5 cm
J Mammal Evol
Glossotherium specimen figured in Dechaseaux (A10.263;
1958,1971) is extremely similar to that of Glossotherium
MACN Pv 13553. It comprises two globose hemispheres di-
vided by a deep longitudinal fissure. The well-developed
suprasylvian gyri are always present in these fossil genera.
A deep entolateral sulcus is visible in A10.263 of
Glossotherium (Dechaseaux 1958,1971)andalsoin
Lestodon,Megatherium,Mylodon,Oreomylodon,and
Scelidotherium (Gervais 1869; Dechaseaux 1958,1962a,
1971), whereas it seems to be absent in Hapalops and
Eucholoeops (Dozo 1987,1994).
In Glossotherium,Oreomylodon,Lestodon,and
Megatherium, the entire dorsal brain surface is strongly arched
and the anterior portion is very wide, bulging mediolaterally
(Gervais 1869; Dechaseaux 1958,1962a,b,1971). However,
the width of the Megatherium brain (Gervais 1869) strongly
decreases along the pseudosylvian sulci, in contrast to the con-
dition observed in the mylodontids mentioned above (Gervais
1869;Dechaseaux1958,1962a,1971). In all these genera (in-
cluding Megatherium), the large olfactory gyrus is delimited by
a deep rhinal fissure, which is curved dorsally, its apex ap-
proaching the nearly vertical pseudosylvian sulcus (Fig. 2c;
Dechaseaux 1958,1962a,b,1971). Awell-developed pyriform
lobe is delimited by the posterior margin of the rhinal fissure in
Glossotherium (Fig. 2c) and Oreomylodon (Dechaseaux 1971:
fig. 13) as well as in both the extant taxa (Fig. 2g, k). This
fissure is generally used as an indication of the ventral limit of
the neocortex, which is considered the newest portion of the
cerebral hemisphere in mammals (Jerison 1991).
The olfactory bulbs of Glossotherium are prominent and
extend strongly dorsally, with a wide and flat anterior surface
covered by the ramifications of the olfactory nerve (I) (Fig.
2ad). In anterior view, these bulbs appear teardrop-shaped
with the dorsal part wider than the ventral one (Fig. 2d). Both
bulbs are flanked by two large symmetrical blood vessels and
some additional tiny vessels, which make the architecture of
the olfactory bulbs in Glossotherium very similar to that ob-
served in other terrestrial sloths such as Oreomylodon
(Dechaseaux 1971).Unfortunately, a detailed comparison
with the olfactory bulbs of G. robustum A10.263
(Dechaseaux 1958,1971) is not possible, due to the quality
of the cast of the latter. However, based on what is preserved,
the morphology of the whole brain would seem to be almost
identical in the two Glossotherium specimens.
The olfactory bulbs of Choloepus and Bradypus differ in
shape. In Choloepus, the olfactory bulbs are well separated
and their outline is rectangular in dorsal view (Fig. 2e). In
lateral view, the ventral surface (bearing the ramifications of
the olfactory nerve) is inclined anterodorsally (Fig. 2g), but
the dorsal edge is horizontal, in contrast to the inclined orien-
tation present in Glossotherium. The olfactory bulbs are reni-
form in anterior view, unlike the teardrop-shaped bulbs in
Glossotherium (Fig. 2h). On the other hand, the olfactory
bulbs in Bradypus are situated closer together. They are
anteroposteriorly elongated and triangular in outline in lateral
view, its margins converging to form a distinct point anterior-
ly, and with a horizontal dorsal edge like that of Choloepus
(Fig. 2i). A similar condition is also observed in Hapalops
(Dozo 1987) and Eucholoeops (Dozo 1994). Moreover, in
anterior view, the dorsoventral height of the olfactory bulbs
is greater than the transverse width in Glossotherium and
Choloepus (Fig. 2d, h), whereas the opposite is observed in
Bradypus (Fig. 2l). The general shape of the olfactory bulbs in
Glossotherium is more similar to Choloepus than to Bradypus,
Hapalops,orEucholoeops.
The cerebellum of Oreomylodon,Lestodon,Mylodon,
Scelidotherium,Megatherium, and especially Glossotherium
is large with both cerebellar hemispheres laterally expanded
(Fig. 2a, c; Gervais 1869; Dechaseaux 1958,1962a,1971). In
these taxa, the cerebellum is sub-triangular in dorsal view with
the apex formed by the posterior portion of the vermis. The
latter structure is well delineated (Fig. 2a; Gervais 1869;
Dechaseaux 1958,1962a,1971). Along the transverse fissure
of all these genera (with the exception of Scelidotherium and
Megatherium), the cerebellum is as wide as the posterior por-
tion of the cerebral hemisphere (Fig. 2a). The paraflocculus is
the lateral expansion of the cerebellum that is housed in the
subarcuate fossa of the petrosal bone (Dechaseaux 1971;
Macrinietal.2007a,b). In Glossotherium MACN Pv
13553, the bulge that comprises the paraflocculus is clearly
recognizable on the surface of the endocast (Fig. 2c), as it is in
the endocasts of Oreomylodon and Glossotherium figured in
Dechaseaux (1971). In both extant forms, the cerebellum is
roughly oval in shape with the maximal width always less
than that of the telencephalon (Fig. 2e, i). The lateral cer-
ebellar hemispheres have rounded and smooth surfaces.
The vermis is well developed in Choloepus, whereas it
leaves no distinctive impression on the endocast surface
of Bradypus (Fig. 2e, i).The parafloccular areas are poorly
marked in the extant sloths, and are located just dorsal to
the jugular foramen (Fig. 2g, k), as in Glossotherium and
Oreomylodon (Dechaseaux 1971).
Cranial Nerves
In Glossotherium, the emergence of the cranial nerves is vis-
ible in ventral, lateral, and anterior views (Fig. 2), and has
been identified on the basis of Dechaseaux (1971)and
Gaudin et al. (2015).
The anteriormost nerve leaving the encephalic cavity cor-
responds to the optic nerve (II), which extends through the
optic foramen (Fig. 2b). The optic foramen opens into the
sphenorbital fissure in all the observed specimens of
Glossotherium,Choloepus, and Bradypus. The confluence
of the optic foramen and the sphenorbital fissure is located
anterior to the olfactory bulbs in Glossotherium (Fig. 2b, c),
JMammalEvol
whereas it is posteriorly located in Choloepus (Fig. 2f, g) and
Bradypus (Fig. 2j, k). In all the sloths, the optic foramen and
the sphenorbital fissure share a common external aperture in
lateral view (Gaudin 2004).
The sphenorbital fissure transmits several nerves (i.e., III-
IV-V
1
-V
2
-VI) and is, therefore, the largest foramen in all the
observed specimens. In Glossotherium MACN Pv 13553
(Fig. 2bd) and Choloepus AMNH 30765 (Fig. 2fh), both
J Mammal Evol
the ophthalmic (V
1
) and the maxillary (V
2
) divisions of the
trigeminal nerve pass through the sphenorbital fissure, where-
as in Bradypus AMNH 95105 (Fig. 2jl), the maxillary divi-
sion extends through the foramen rotundum. This feature, ob-
served in the encephalic cavity of Glossotherium,Choloepus,
and Bradypus, agrees with the observations of Gaudin (2004)
on the external surface of the skull in lateral view. In fact, the
foramen rotundum is confluent with the sphenorbital fissure in
most Mylodontidae (excluding Nematherium and
Pseudoprepotherium) and also in Choloepus,Eremotherium,
Megatherium,andThalassocnus, whereas these two openings
are separate in all the other sloths.
The foramen ovale, which accommodates the mandib-
ular division (V
3
) of the trigeminal, is present posterior
and lateral to the sphenorbital fissure in all the examined
specimens (Fig. 2).
More posteriorly, at the level of the petrosal bone, the in-
ternal acoustic meatus is pierced by the facial (VII) and
vestibulocochlear (VIII) nerves (Fig. 2). The latter ends at
the level of the inner ear, whereas the facial nerve has a more
convoluted trajectory that has been reconstructed for
Glossotherium (Fig. 3). Emerging from the primary facial fo-
ramen of the petrosal, the facial nerve forms the geniculate
ganglion in the cavum supracochleare, just medial to the
anteroventral process of the tegmen tympani, and anterior to
the rostral end of the crista parotica. From this point, the facial
nerve turns posteriorly, travels through the secondary facial
foramen into the facial sulcus and, passing through the
stylomastoid foramen, leaves the cranium ventrally (Fig. 3).
Anterior to the geniculate ganglion, the greater petrosal nerve
Fig. 2 Brain endocasts of Glossotherium (MACN Pv 13553) (a-d),
Choloepus (AMNH 30765) (e-h), and Bradypus (AMNH 95105) (i-l), in
dorsal (a,e,i), ventral (b,f,j), lateral (c,g,k), and anterior (d,h,l) views.
Abbreviations: arf, anterior rhinal fissure; eg, ectosylvian gyrus; es,
entolateral sulcus; fov, foramen ovale; fr, foramen rotundum; fsph,
sphenorbital fissure; h, hypophysis; hf, hypoglossal foramen; iam,
internal acoustic meatus; jf, jugular foramen; lch, left cerebellar
hemisphere; lf, longitudinal fissure; lg, lateral gyrus; ls, lateral sulcus;
ob, olfactory bulb; obr, olfactory bulb ramifications; og, occipital gyrus;
olg, olfactory gyrus; op, olfactory peduncle; opt, optic foramen; org,
orbital gyrus; p, paraflocculus; pl, pyriform lobe; pnc, petrosal nerve
complex; prf, posterior rhinal fissure; ps, presylvian sulcus; pss,
pseudosylvian sulcus; rch, right cerebellar hemisphere; sg, suprasylvian
gyrus; ss, suprasylvian sulcus; tf, transverse fissure; tl, temporal lobe; ve,
vermis. Colors indicate: grey, cerebrum; blue, olfactory bulbs; turquoise,
cerebellum; orange, neurovascular connections. Roman numeral
designations indicate cranial nerves. Scale bars equal 2 cm
Fig. 3 Digital reconstruction of (a-c) the right side endocasts in
ventrolateral view, with the petrosal represented in decreasing degrees
of opacity, and (d) the right side braincase in ventrolateral view, of
Glossotherium robustum (MACN Pv 13553). Abbreviations: cf, carotid
foramen; fn, facial nerve; fov, foramen ovale; fsph, sphenorbital fissure;
gga, geniculate ganglion area; gpn, greater petrosal nerve; iam, internal
acoustic meatus; ica, internal carotid artery; jf, jugular foramen; lpn, lesser
petrosal nerve; ob, olfactory bulb; prp, promontorium of petrosal; pt(lp),
pterygoid (lateral portion); pt(mp), pterygoid (medial portion); shf,
stylohyal fossa; stmf, stylomastoid foramen; vn, vidian nerve. Colors
indicate: blue, olfactory bulbs; green, bony labyrinth; orange,
neurovascular connections; red, arterial vessels. Darker tones of red and
orange indicate inferred structures on the outer surface of the skull.
Roman numeral designations indicate cranial nerves. Scale bars equal
2cm
R
JMammalEvol
turns medially and, after passing through the hiatus Fallopii,
extends in a distinct sulcus on the epitympanic wing of the
petrosal, before turning ventrally at the level of the trigeminal
ganglion (Fig. 3). The greater petrosal nerve then enters in the
foramen located in the anterior wall of the carotid foramen,
piercing the ventral surface of the medial portion of the pter-
ygoid and emerging anteriorly in the groove of the vidian
nerve (Fig. 3). The lesser petrosal nerve is an anterior exten-
sion of the tympanic nerve (a branch of the glossopharyngeal
nerve, cranial nerve IX, that forms a sensory tympanic plexus
on the ventral surface of the promontorium; Clemente 1985;
Evans 1993; Wible 2010). The tympanic nerve leaves no trace
on the petrosal surface, but the lesser petrosal nerve enters a
canal that extends parallel with but dorsal to the greater petro-
sal nerve (Fig. 3). The lesser petrosal nerve then follows the
mandibular branch of the trigeminal nerve, and leaves the
cranium through the foramen ovale.
More posteriorly, cranial nerves IX, X, and XI leave the
braincase through the jugular foramen (Figs. 2and 3).
The hypoglossal nerve (XII) is the most posterior cranial
nerve, and is extremely well developed in Glossotherium (Fig.
2ac), but very reduced in the extant sloths (Fig. 2el).
In general, Glossotherium exhibits great enlargement of the
sphenorbital fissure, the foramen ovale, and the hypoglossal
foramen, in comparison with all the other nerve-transmitting
foramina (Fig. 2ad). On the contrary, more homogeneity in
the size of the foramina is observed in the extant sloths
Choloepus (Fig. 2eh) and Bradypus (Fig. 2il).
Blood Vessels
As already observed, the surface of the brain endocast of
Glossotherium is more rugose and convoluted than in the
extant sloths. Not only are sulci and gyri more evident in
Glossotherium than in the extant genera, but grooves for the
blood vessels are also more clearly marked. In fact, some
vessels have left marks that we attribute to both arteries and
veins (Fig. 4).
Arteries The main arterial vessel leading to the brain is the
internal carotid artery, entering in the cranial cavity though
the carotid foramen, located at the anteromedial corner of
the petrosal. In Glossotherium, the track of the internal carotid
artery is particularly enlarged at the base of the trigeminal
ganglion, and is visible on both sides of the ventral surface
of the endocast, at the level of the hypophyseal reagion (Fig.
4bd). Thisvessel is partially visible in the ventral endocast of
Choloepus (Fig. 4f) but not detectable in Bradypus.Inboth
Glossotherium and Choloepus, the internal carotid artery
shows a strong posterolateral to anteromedial trajectory, fol-
lowing a detached sulcus on the internal side of the petrosal
(Patterson et al. 1992;Boscainietal.2018). In Glossotherium
(Fig. 4a, b, d), two paired arteries diverge toward the olfactory
bulbs (= internal ethmoidal arteries, according to Evans 1993:
626). These are partially preserved in Glossotherium MACN
Pv 13553 along the medial margin of the olfactory bulbs, and
are oriented largely dorsoventrally (Fig. 4a, b, d).
These vessels are attributed to arteries on the basis of their
large size, which is more compatible with the anteriormost
termination of the ventral arterial system of the brain than
any vein draining the region. Moreover, this pattern is typical
in mammals and appears to be plesiomorphic in xenarthrans,
as it is observed in the extant armadillos, anteaters, and sloths
(Hyrtl 1854; Tandler 1901; Bugge 1979).
Veins The venous circulation is partially preserved in MACN
Pv 13553. In dorsal view, some tiny vessels, the branches of the
frontal meningeal veins, depart from the olfactory bulbs and are
posteriorly directed (Fig. 4a, c, d). More posteriorly, the
branches of the parietal meningeal vein are thicker than the
frontal meningeal veins and are irregularly distributed. All these
veins are confluent with the dorsal sagittal sinus, the
posteriormost portion of which is represented in MACN Pv
13553 (Fig. 4a). This latter sinus is observable along nearly
its entire length in Oreomylodon (Dechaseaux 1971). The dor-
sal sagittal sinus connects posteriorly to the paired transverse
sinuses at the level of their median divergence (Fig. 4; Evans
1993: 709). The grooves for these latter vessels, located at the
boundary between the cerebral hemispheres and the cerebellum
(and thus along the transverse fissure), are the deepest on the
dorsal surface of the endocast, a condition that is also observed
in other extinct sloths such as Megatherium,Mylodon,
Oreomylodon,Scelidotherium,andEucholoeops (Gervais
1869; Dechaseaux 1958,1962a,1971;Dozo1994).
In lateral view, the transverse sinus gives rise laterally into
two anteriorly directed lesser veins: the ventral cerebral vein
and the dorsal petrosal sinus (Fig. 4c). The former has a wider
diameter than the latter, and extends partially in the caudal
suprasylvian sulcus, whereas the latter is narrower, lies in a
more ventral position (on the pyriform lobe), and projects
farther anteriorly (Fig. 4c).
The greater part of the transverse sinus flows laterally and
ventrally into the sigmoid sinus, which leaves the cranium
through the jugular foramen (Fig. 4b, c). The sigmoid sinus is
the only vein that is recognizable on the endocasts of the extant
sloths Choloepus (Fig. 4e, h) and Bradypus (Fig. 4g, i). In its
most ventral portion, the sigmoid sinus of Glossotherium
MACN Pv 13553 is joined by two veins, the inferior petrosal
sinus and the basilar sinus (Fig. 4b, c). In ventral view (Fig. 4b),
the inferior petrosal sinus extends anteroposteriorly through a
fissure that lies between the petrosal and the basioccipital. In its
anteriormost portion the inferior petrosal sinus passes through a
second opening in the posterior wall of the carotid foramen,
whereas posteriorly it emerges in the anterior wall of the jugular
foramen, where it joins the sigmoid sinus (Fig. 4b, c). There is a
large branch of the inferior petrosal sinus that extends
J Mammal Evol
posteroventromedially, the left and right sides converging to-
ward the floor of the foramen magnum. We are unaware of a
large vein that would occupy such a position in xenarthrans, or
indeed in other mammals, so we have, for the time being, sim-
ply labeled this branch as an unknown vessel (Fig. 4b). The
basilar sinus merges with the sigmoid sinus more dorsally than
the inferior petrosal sinus, and extends through the condyloid
canal (Fig. 4ac). At its posterior end, the basilar sinus turns into
the internal vertebral venous plexus as it leaves the foramen
magnum (Evans 1993: 711). This condition was previously
observed in the genus Mylodon by Patterson et al. (1992),
who suggested that the very large groove running from the
inside of the foramen lacerum posterium to the foramen mag-
numwas pierced by an unidentified venous sinus(Patterson
et al. 1992: 6). In accordance with the CT scans performed in
the present study and the available literature (Clemente 1985;
Evans 1993), this vein is likely the basilar sinus. The groove
that housed this vessel is absent in all living xenarthrans
(Patterson et al. 1992).
The condyloid canal, which connects the jugular foramen
with the foramen magnum, has a dorsoposteriorly directed
branch near its caudal end (Fig. 4ac). This branch emerges pos-
teriorly at the mastoid foramen, located just dorsal to the occipital
condyle. This latter canal accommodated the occipital emissary
vein, draining the external surface of the occipital bone.
Paranasal Pneumaticity
The paranasal sinuses, a characteristic feature of placental mam-
mals (e.g., Moore 1981; Novacek 1993), are air-filled chambers
Fig. 4 Brain endocasts of Glossotherium (MACN Pv 13553) (a-d),
Choloepus (AMNH 30765) (e, f, h), and Bradypus (AMNH 95105) (g,
i), in dorsal (a,e,g), ventral (b,f), lateral (c,h,i), and anterior (d) views,
showing the arterial vessels (red) and venous vessels (blue).
Abbreviations: bs, basilar sinus; dps, dorsal petrosal sinus; dss, dorsal
sagittal sinus; fmv, branches of the frontal meningeal vein; ica, internal
carotid artery; iea, internal ethmoidal artery; ips, inferior petrosal sinus;
oev, occipital emissary vein; pmv, branches of the parietal meningeal
vein; ss, sigmoid sinus; ts, transverse sinus; unv, unknown vessel; vcv,
ventral cerebral vein. Scale bars equal 2 cm
JMammalEvol
that form within a variety of cranial bones and are connected to
the nasal cavity. They are commonly divided into maxillary,
frontal, and sphenoidal sinuses, of which the maxillary sinuses
are the most basal and widespread among eutherian mammals
(Moore 1981). The maxillary sinuses are also invariably present
in xenarthrans (Moore 1981). Unfortunately, due to breakage of
the anterior portion of MACN Pv 13553 (Fig. 1), the maxillary
sinuses cannot be observed. Thus, the description and compar-
ison that follow will be limited to the frontal and sphenoidal
sinuses. These sinuses are so named because they are typically
found within the frontal and sphenoidal bones (specifically the
presphenoid; Evans 1993), but sometimes they extend into other
cranial bones (Moore 1981). For this reason, and following this
scheme, our description of the cranial pneumatization pattern in
Glossotherium and the extant sloth genera will be based on the
bony elements directly involved (thus, for example, we refer to
the orbitosphenoid sinus). In mammals, the number and extent
of the chambers differ among species, but their development
also varies greatly during ontogeny, producing intraspecific var-
iation among individuals of different ages, particularly during
the later stages of growth and in adult life (Moore 1981;Farke
2008). Moreover, minor differences occur between the right and
left sides of a single individual (Moore 1981). Therefore, our
descriptions are limited to symmetrically observed aspects of
sinus morphology, and our inter-taxon comparison is made only
among adult specimens, in order to avoid differences related to
different ontogenetic stages.
The three genera considered in this work (i.e.,
Glossotherium,Choloepus,andBradypus) possess both fron-
tal and orbitosphenoid sinuses. In Bradypus, the frontal si-
nuses are smooth walled and shallow in lateral view
(Fig. 5gi). These sinuses are approximately rectangular in
Fig. 5 Paranasal pneumaticity in the skulls of Glossotherium (MACN Pv
13553) (a-c), Choloepus (AMNH 30765) (d-f), and Bradypus (AMNH
95105) (g-i), in lateral (a,d,g), dorsal (b,e,h), and anterior (c,f,i) views.
Abbreviations: bbs, basisphenoid-basioccipital sinuses; eps, epitympanic
sinuses; fps, fronto-parietal sinuses; fs, frontal sinuses; ors,
orbitosphenoid sinuses; ps, palatine sinuses; pts, pterygoid sinuses.
Scale bars equal 2 cm
J Mammal Evol
dorsal view and more elongated anteroposteriorly than
mediolaterally. They are composed of a single chamber that
covers the olfactory bulbs dorsally and is limited posteriorly
by the fronto-parietal suture (Fig. 5g, h). Ventral to, and sep-
arate from the frontal sinuses, some small sinuses open into
the orbitosphenoid. These orbitosphenoid sinuses are located
just ventral to the olfactory bulbs and posterior to the ethmoid.
Their most lateral portions project anteriorly towards the na-
sopharynx (Fig. 5g). Another highly pneumatized part of the
skull is the zygomatic process of the squamosal, which con-
tains the epitympanic sinus, passing dorsally from its posterior
connection to the tympanic cavity into the squamosal, and
then extending anteriorly to the level of the glenoid fossa
(Fig. 5g, h). Also, large pterygoid sinuses have been described
in the maned sloth, B. torquatus (e.g., Guth 1961), but are not
evident in our specimen of B. variegatus, and are not known to
be developed in other Bradypus species (Patterson et al. 1992;
Hayssen 2008,2010). The frontal, orbitosphenoid, and zygo-
matic sinuses are distinct and well separated in lateral, dorsal,
and anterior views (Fig. 5gi).
In Choloepus (Fig. 5df), the frontal sinuses are much larg-
er, more complex, more convoluted, and display more bilater-
al asymmetry than those of Bradypus (Fig. 5gi). In the two-
toed sloth, these sinuses are composed of several chambers
extending dorsally over the olfactory bulbs (Fig. 5df). In dor-
sal view (Fig. 5e), they extend posterior to the fronto-parietal
suture into the parietal, following an irregular pattern that is
not observed in Bradypus (Fig. 5h).
Choloepus has small orbitosphenoid sinuses that are visible
in lateral and anterior views, just ventral to the olfactory bulbs
(Fig. 5d, f). These are separated from the frontal sinuses, as in
Bradypus. In their most lateral parts they project anteriorly, but
are quite asymmetric (Fig. 5d, f). In contrast with Bradypus,the
frontal sinuses of Choloepus project markedly posteroventrally
in lateral and anterior views. This extension merges with the
palatine sinuses (Fig. 5d, f). On the right side of Choloepus
AMNH 30765, the pneumatization is continuous, whereas it
is separated by a thin septum on the left side (Fig. 5d, f).
More ventrally, the pneumatization of the palatine is in contact
with the pterygoid sinuses in both the right and the left sides.
The inflation of the pterygoid is more pronounced in Choloepus
than in Bradypus (except in B. torquatus, see preceding para-
graph) or Glossotherium (Gaudin 2004:char137).The
basicranial pneumatization extends posteriorly into the
basisphenoid and the basioccipital, again with a sinuous and
irregular pattern comparable to the irregularities observed in
the other sinuses of Choloepus.AsinBradypus, the zygomatic
process of the squamosal is also well pneumatized, housing an
extensive epitympanic sinus (Fig. 5df). The pneumatized re-
gion extends from the tympanic cavity dorsally into the squa-
mosal and anteriorly to the level of the glenoid fossa, but it
tapers in width posteriorly, terminating before reaching the pos-
terior end of the zygomatic process. Therefore, the epitympanic
sinus is somewhat smaller and more anteriorly restricted than
that of Bradypus (Fig. 5d-e, g-h). Choloepus displays more
pneumatized areas than Bradypus, as well as more communi-
cation among them (Fig. 5d-f, g-i).
In Glossotherium (MACN Pv 13553; Fig. 5ac) the
pneumatization is so pervasive that the sinuses mirror the ex-
ternal morphology of the cranium and are not separable into
well-defined areas as in Choloepus (Fig. 5df) and Bradypus
(Fig. 5gi). Pneumatization in Glossotherium affects the whole
braincase, from the occipital to the parietals and frontals, ex-
tending ventrally into the side walls of the braincase and the
basicranium, and supported throughout by internal struts
(Figs. 1a, 5ac). This condition is comparable to the extent
of pneumatization in other extinct giant sloths in which this
feature has been observed, such as the mylodontid
Oreomylodon and the megalonychids Megalocnus and
Megistonyx (Dechaseaux 1971; Patterson et al. 1992;
McDonald et al. 2013). However, such pneumatization may
not be universal in giant extinct sloths, as suggested by the
genus Eremotherium (see sectioned skull in Patterson et al.
1992: 35). Inlateral view, air-filled chambers are missing from
only a few areas of the skull of Glossotherium. These include
the paraoccipital process of the petrosal and the exoccipital
crest, both involved in the formation of the stylohyal fossa
(Fig. 5a, b). Also, the bones surrounding the foramen magnum
are not pneumatized, including the most distal portion of the
basioccipital and the most ventral limit of the occipital, along
with the occipital condyles (Fig. 5a, b). This is probably relat-
ed to the robustness necessary in these areas that articulate
with the hyoid apparatus and the vertebral column,respective-
ly. A reduction of the sinuses in the vicinity of the foramen
magnum is also observed in modern elephants, the cranium of
which is otherwise highly pneumatized (Van der Merwe et al.
1995). Left and right portions of the cranium in Glossotherium
display similar pneumatization, but there is considerable
shape variation. Some tubular structures are detectable among
the rounded air-filled spaces, both on the internal and external
sides of the pneumatized layer. These structures are
neurovascular in nature, but their limits frequently cannot be
traced because of breakage or structural discontinuities.
Discussion
The recent increase in paleoneurological studies of extant and
fossil vertebrates reflects the fact that brain endocasts repre-
sent an important source of anatomical, morpho-functional,
and, in particular cases, ethological information, which help
researchers in their attempt to better understand the paleobiol-
ogy of fossil mammals (e.g., Sakai et al. 2011; Cunningham et
al. 2014; Thiery and Ducrocq 2015; Dozo and Martínez 2016;
Vinuesa et al. 2016;Bertrandetal.2017). Unfortunately, our
knowledge offossil sloth brain morphology and its functional
JMammalEvol
implications are based on only a very few, dated studies (e.g.,
Gervais 1869;Dechaseaux1971;Dozo1987,1994). In addi-
tion, endocasts from this group of fossil mammals have been
obtained from only a limited number of genera, almost always
represented by very few specimens. Despite these limitations,
the descriptions and comparisons of the endocast features in
the present study allow for some preliminary analysis.
Brain Endocast According to Dechaseaux (1971) and Dozo
(1987), all the fossil sloth taxa discussed above show a very
similar brain morphology, and this similarity involves not only
the general shape of the brain, but also the pattern of convo-
lutions, which are highly conservative in both extinct and
extant sloth species. However, the apparent roughness of the
external surface is shared exclusively among the large-bodied
extinct sloths, suggesting that this feature might be related to
allometric factors. The pattern of convolutions apparently
remained fairly stable during the evolutionary history of sloths
and the number, and arrangement, of the identified convolu-
tions is almost the same (Fig. 2). In both Glossotherium
MACN Pv 13553 and A10.263, the entolateral sulcus is clear-
ly visible, but this is also true in the extinct genera Lestodon,
Megatherium, Mylodon, Oreomylodon, and Scelidotherium
(Gervais 1869;Dechaseaux1958,1962a,1971), and in the
extant two-toed sloth Choloepus.However,thissulcusisab-
sent in the extant three-toed sloth Bradypus and in the middle
Miocene forms Hapalops and Eucholoeops (Dozo 1987,
1994). The distribution of this feature accords with the most
recent phylogenetic scenarios based on morphological evi-
dence (Gaudin 1995,2004), which propose that Choloepus
and Glossotherium are more closely related to one another
than either is to Bradypus. However, the condition in
Bradypus is present in Hapalops and Eucholoeops,even
though the latter two are more closely related to Choloepus
than Glossotherium according to Gaudin (2004). The simpli-
fied pattern of Bradypus,Hapalops,andEucholoeops,along
with the phylogenetic position of Bradypus as the putative
sister-taxon to all other sloths, suggests that Bradypus has
maintained the plesiomorphic condition probably since the
Oligocene (Dozo 1987,1994; Gaudin and Croft 2015), but it
may also imply that the similarity between Glossotherium and
Choloepus evolved convergently.
The complexity of convolutions is generally higher in large-
sized mammals than in medium- to small-sized mammals, be-
cause the convolutions increase the amount of cortical surface
area, compensating for reductions in surface area to volume
ratio for brains of increasing size (e.g., Prothero and Sundsten
1984; Roth and Dicke 2005; Macrini et al. 2007b). Folivorans
seemingly do not follow this rule. In fact, the apparent com-
plexity of the telencephalic surface in Glossotherium and other
large-sized species is related to the presence of several surface
irregularities, consisting of a high number of recesses and pro-
trusions (Fig. 2). Their irregular shape, small size, and,
especially, uniform distribution on the brain surface (they are
even observed on surfaces of the blood vessels) allow us to
exclude the possibility that these structures are convolutions.
They are more likely interpreted as traces of meninges. In large
extant mammals of similar size (e.g., pachyderms and ceta-
ceans), meninges, cisterns, and other soft-tissue structures tend
to fill the spaces in the sulci of the brain, obscuring the pattern
of sulci and gyri (Macrini et al. 2007b and references therein)
and this phenomenon can be partially responsible for the re-
duced sulcation in Glossotherium. In any case, in extant and
extinct sloths the basic pattern of convolutions is always ob-
servable, independent of body size. This basic pattern closely
resembles that of carnivorans, which display the simplest ar-
rangement of convolutions among gyrencephalic mammals
(Barone and Bortolami 2004). This similarity is particularly
strong for the dorsal surface of the telencephalon, and has been
previously reported by Gervais (1869), Elliot-Smith (1898),
and Anthony (1953).
The olfactory bulbs in Glossotherium strongly project dorsal-
ly (Fig. 2ad), with an enlarged anterior surface covered by the
many ramifications of the olfactory nerve. In the specimens of
Oreomylodon and Glossotherium figured by Dechaseaux (1958,
1971), the olfactory bulbs are also directed and enlarged dorsal-
ly. Even though the splanchnocranial portion is missing in
Glossotherium MACN Pv 13553, a fragment of the ethmoid
bone is preserved, and in it the cribriform plate appears vertical,
exceeding in height the dorsal portion of the olfactory pedun-
cles. This condition is also observed in Oreomylodon
(Dechaseaux 1971:fig.5),butitdoesnotoccurintheextant
sloth taxa, where the cribriform plate ends at the dorsal limit of
the olfactory peduncles, thus conferring a horizontal dorsal pro-
file to the bulbs in lateral view. In Glossotherium, the dorsal
projection of the olfactory bulbs can be related to the dorsoven-
tral expansion of the nasal cavities, which can affect the hori-
zontal development of the cribriform plate and, consequently,
the vertical profile of the bulbs. It is currently difficult to assess
if, and how, this peculiar morphology of the olfactory bulbs
relates to the olfactory sensitivity in this extinct sloth. For exam-
ple, the expansion of the nasal cavities may represent an adap-
tation to particular environmental conditions, or may be related
to thermoregulation, water balance, or even sound production
(or a combination of them). A larger set of cranial and
paleoneurological data is needed to better understand the corre-
lation between morphology and function of the olfactory bulbs
in these taxa. A dorsal projection of the olfactory bulbs is not
present in Choloepus, but like Glossotherium,ithas
anteroposteriorly short bulbs that are deep dorsoventrally and
narrow transversely. The olfactory bulbs of Bradypus are shal-
low dorsoventrally, elongated anteroposteriorly, and pointed at
their anterior tip, with a broad olfactory peduncule, imparting a
morphology quite different from that observed in Glossotherium
and Choloepus. The shape of the olfactory bulbs in Bradypus
does resemble that of Hapalops (Dozo 1987),andtoalesser
J Mammal Evol
extent of Eucholoeops (Dozo, 1994), which again likely repre-
sents the retention of a plesiomorphic condition in these taxa.
If the telencephalon shows a fairly uniform pattern of convo-
lutions in both extinct and extant sloths, the cerebellum (together
with the olfactory bulbs) represents the most variable portion of
the sloth endocasts. In dorsal view, Glossotherium has a sub-
triangular cerebellum with the apex formed by the posterior por-
tion of the vermis. This shape is the result of a lateral expansion
of the two cerebellar hemispheres, which reach a maximum
transverse width equivalent to that of the posterior portions of
the cerebral hemispheres. This latter is a common feature in
large-bodied extinct sloths, and is generally accompanied by
the presence of a well-developed paraflocculus. The presence
of large paraflocculi is considered a plesiomorphic character
within therian mammals (Kielan-Jaworowska 1986;Macriniet
al. 2007b). In Glossotherium, the parafloccular areas are propor-
tionally wider than in the small-bodied extant sloths Bradypus
and Choloepus, in which they appear as tiny swellings just dorsal
to the jugular foramen (Fig. 2). The former condition was previ-
ously illustrated by Dechaseaux (1971)forbothGlossotherium
and Oreomylodon. The latter condition is here reported for the
two extant genera Choloepus and Bradypus, but was also recog-
nized in the late early Miocene sloths Hapalops and Eucholeops
(Dozo 1987,1994). Further studies should investigate the possi-
ble allometric and functional significance of this feature.
Cranial Nerves The main trajectories of the cranial nerves have
been reconstructed for Glossotherium robustum MACN Pv
13553 (Figs. 2and 3) and the extant sloths Bradypus and
Choloepus (Fig. 2). The cranial nerve pathways through the
sphenorbital fissure, foramen rotundum, and foramen ovale
are similar in Glossotherium and Choloepus, and differ signif-
icantly from the pattern in Bradypus, consistent with their pro-
posed closer phylogenetic affinity (Gaudin 1995,2004). In
Glossotherium, we observed that the grooves for the
sphenorbital fissure, the foramen ovale, and the hypoglossal
foramen are enlarged relative to other foramina transmitting
cranial nerves, confirming initial observations by Owen
(1839,1842). The presence of these deep furrows is probably
related to a greater development of the trigeminal and hypo-
glossal nerves, compared to other nerves, in the extinct sloth
Glossotherium,t
haninBradypus and Choloepus, where the
nerve-transmitting foramina are more uniform in size. This
probably can be related to larger relative sizes of tongue and
jaw muscles in the extinct genus Glossotherium than the extant
forms, in accordance with their different dietary habits (Bargo et
al. 2006b; Pujos et al. 2012). The large sphenorbital fissure and
foramen ovale also could be partially related to an increased
sensory innervation coming from the elongated rostrum and
enlarged nasal cavity of Glossotherium.
Blood Vessels Blood vessels are more difficult to observe in the
small-sized extant sloths than the large-sized Glossotherium
(Fig. 4). In the latter (Fig. 4ad) many blood vessels are discern-
ible, and the general pattern is similar to that observed in other
extinct sloths (Gervais 1869; Dechaseaux 1958,1962a,1971;
Dozo 1994) and comparable with the plesiomorphic condition
in xenarthrans (Hyrtl 1854;Tandler1901; Bugge 1979). This
suggests a conservative conformation of the blood circulation.
The sigmoid sinus is the only vessel that is invariably observed
in Glossotherium,Choloepus,andBradypus,whereastheim-
pression of the internal carotid artery is another feature only
found in Glossotherium and Choloepus (Fig. 4).
Paranasal Pneumatization Many hypotheses concerning the
function of the paranasal sinuses have been proposed
(exhaustive reviews are available in Blanton and Biggs 1969;
Moore 1981;Blaney1990).Theideathatcranial
pneumatization is basically functionless (Weidenreich 1924,
1941;Edinger1950; Witmer 1997) has become the most wide-
ly accepted hypothesis over the last decade (Farke 2008,2010).
The possible existence of opportunistic pneumatization,
which implies that the sinuses do not have any apparent
function and are merely the result of the removal of
structurally unnecessary bone, has been gaining support over
the last few years and was recently advocated by Farke (2007,
2008,2010) who conducted the broadest and most compre-
hensive quantitative analysis of sinus morphology ever
attempted(Farke 2010: 1010). The same author demonstrated
that the size and complexity of paranasal sinuses in bovids are
not related with their ramming behavior, as previously thought
(Farke 2010). On the contrary, they seem to be partially related
to the size of the frontals (and consequently the whole skull),
and consistent with a role for the sinuses in weight reduction
(Farke 2010). However, this is true only in those groups that
already possess pneumatized frontal bones, suggesting both a
positive allometry with skull size and a strong phylogenetic
component. In this sense, Farke (2010) recognized that the
presence of a frontal sinus is the ancestral condition in
Bovidae and has been lost several times during the evolution
of the clade. In different bovid taxa, Farke (2010)alsodetected
several pneumaticity patterns, which include: i) sinuses extend-
ing up to the fronto-parietal suture (i.e., sinuses that do not cross
the suture and even conform to its morphology), ii) sinuses
extending beyond the fronto-parietal suture to pneumatize the
parietal, and occasionally also the occipital bone, and iii) si-
nuses widely extended and pneumatizing large regions of the
cranium (e.g., including the entirety of the horn cores).
Our preliminary data suggest that similarities between bo-
vids and sloths can be recognized regarding the development
of the sinuses. Generally, sinus morphology in Xenarthra
seems to have a strong phylogenetic component, given that
frontal sinuses have been demonstrated to be diagnostic even
at the subspecific level for different morphotypes of the nine-
banded armadillo Dasypus novemcinctus (Billet et al. 2017).
In contrast, frontal sinuses are lacking in anteaters, in which
JMammalEvol
only some basicranial pneumatizations are observed, mainly
in the alisphenoid, palatine, and the pterygoid bones, along
with an epitympanic sinus in the squamosal (Moore 1981;
Storch and Habersetzer 1991; Patterson et al. 1992;Gaudin
1995,2004).
In the three sloth genera described in the present study, the
frontal sinuses are invariably present. Bradypus, the putative
sister group to all the other extant and extinct sloths (e.g.,
Gaudin 2004) presents the simplest observed pattern, with the
fronto-parietal suture limiting the extent of the frontal sinuses
posteriorly (Fig. 5gi). On the other hand, Glossotherium and
Choloepus, which are more closely related phylogenetically
according to Gaudin (2004), also show similarities exclusive
of Bradypus in the morphology of their cranial sinuses. For
example, both exhibit a continuous pneumatization, from the
frontals to the basicranium (Fig. 5af). This pneumatization is
extremely exaggerated in Glossotherium, so that it involves a
series of interconnected chambers invading nearly every poste-
rior cranial bone. Total body size must be taken into account,
andwenotethatBradypus is the smallest of the three genera,
followed closely by Choloepus, whereas Glossotherium is
much larger, approaching the size of the largest modern
bovids. This suggests the presence of a corresponding
positive allometry in sinus size relative to skull size. As Farke
(2010) observed in bovids, it appears that in the sloth clade, the
different patterns observed are likely related to both phyloge-
netic effects and the influence of body size.
Conclusions
The digital cranial endocasts of G. robustum have been de-
scribed and compared with representative specimens of extant
sloths, providing an anatomical characterization of the main
features of the brain cavity, cranial nerves, blood vessels, and
paranasal sinuses.
Among these structures, we detected features that could
have a phylogenetic signal, such as the general shape of the
brain endocast, the presence/absence of the entolateral sulcus,
and the shape of the olfactory bulbs and the vermis. However,
the general pattern of sulci and gyri on the brain endocast
appeared to be extremely conservative in the folivoran clade
and we confirmed its simple organization, independent of
body size, if compared with other mammals. Similarly, the
arterial and venous circulation appeared to be conservative
in sloths, even if blood vessel features are more difficult to
observe in smaller- rather than larger-sized sloths. Other char-
acters, such as the apparent roughness of the external surface
of the brain endocast and the mediolaterally expanded cere-
bellum, may be related, instead, to allometric factors. In con-
trast, the relative size of the foramina through which the tri-
geminal and hypoglossal nerves passed suggests a probable
physiological influence, related with food processing and sen-
sory information.
Finally, paranasal pneumatization shows evidence of
mixed signals, i.e., it is mainly affected by phylogenetic and
allometric factors, even if a functional influence related to
body size increase cannot be currently refuted.
The anatomical regions of the extinct sloth G. robustum
analyzed in this work under 3D imaging techniques show
the great potential of these methodologies for elucidating the
evolutionary history of this peculiar mammalian clade.
Acknowledgments We are grateful to the FUESMEN for access to CT-
scanning facilities, and in particular we are indebted to Sergio Mosconi
and collaborators for assistance with image processing. We thank A.
Kramarz, S.M. Alvarez, and L. Chornogubsky (MACN) who kindlygave
access to the specimens under their care. This work was possible thanks to
the facilities offered by the PaleoFactory Lab (Sapienza Università di
Roma, Rome, Italy) and the free digital database available at http://
digimorph.org.WealsowanttothankG.Billet,L.Hautier,M.
Fernández-Monescillo, S. Hernández del Pino, and A. Forasiepi for
their useful suggestions. This paper greatly benefited from the careful
reading and thoughtful comments by the Editor J.R. Wible and two
anonymous reviewers. This work was partially funded by ECOS-
FonCyT (A14U01).
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... Nomenclature. Endocast descriptive terminology follows Boscaini et al. (2020aBoscaini et al. ( , 2020bBoscaini et al. ( , 2023 ...
... 1). By contrast, the lateral sulcus is simple and nonbifurcating in the Bradypus specimen studied by Boscaini et al. (2020b). ...
... The cerebellum is clearly demarcated from the cerebral hemispheres by a distinct transverse fissure ( Fig. 4.1-4) and is similar in breadth to the anterior cerebrum. A vermis is present and well-developed (Fig. 4.3), as in Choloepus Linnaeus, 1758, Glossotherium Owen, 1839 and Catonyx Ameghino, 1891b but unlike in Bradypus, where it is absent (Pohlenz-Kleffner, 1969;Boscaini et al., 2020aBoscaini et al., , 2020bBoscaini et al., , 2023Freitas et al., 2020). The vermis is bordered laterally by deep paramedian fissures, as described by Dozo (1987) for H. indifferens. ...
... The applications of these new techniques to extant and extinct Folivora started less than a decade ago, and are now undergoing a rapid increase (e.g. Billet et al. 2012Billet et al. , 2013Billet et al. , 2015Coutier et al. 2017;Amson et al. 2018;Boscaini et al. 2018Boscaini et al. , 2020a. In these works, the sloth endocranial cavities that have been more intensively analyzed are: (i) the brain cavity and cranial nerves, (ii) the bony labyrinth of the inner ear, and (iii) the cranial sinuses. ...
... Like the early brain endocasts produced in the nineteenth century, the first extinct sloth species whose neuroanatomy was studied in detail using digital methods was Glossotherium robustum (Boscaini et al. 2020a;Fig. 19.3a-c). ...
... The brain endocast of this species was compared to that of the modern arboreal forms Bradypus variegatus and Choloepus hoffmanni (Boscaini et al. 2020a;Fig. 19.3g-i), and subsequently, to that of another extinct mylodontid sloth, the scelidotheriine Catonyx tarijensis (Boscaini et al. 2020b;Fig. ...
Chapter
Folivora (sloths) constitutes a taxonomically rich group comprised of many extinct representatives and a few living forms. The clade also shows remarkable skeletal disparity that has been studied by paleontologists for more than two centuries. Accordingly, the first published information on endocranial morphology in fossil sloths, recovered though natural or reconstructed internal casts or broken specimens, date to the nineteenth century. Today, new computed tomography (CT) and three-dimensional digital reconstruction techniques allow observation in great detail of many endocranial structures, such as the brain endocast and cranial nerve trajectories, as well as the bony labyrinth of the inner ear and patterns of cranial pneumatization. These analyses have been recently applied to modern (Bradypus and Choloepus) and extinct (Catonyx, Glossotherium, and Megatherium) sloth skulls. General patterns include a conservative brain anatomy among sloths, a strong phylogenetic imprint on the bony labyrinth, and the presence of extensive cranial pneumatization in some extinct mylodontids. The present work comprises a synthesis of both historical and recently published data on endocranial structures in Folivora. Further studies of the endocranial cavities in other extinct sloths have the potential to enhance understanding of several aspects of the clade’s evolutionary history, including phylogeny and paleobiology.
... We reconstructed several endocranial elements of the neurocranium (Fig. 2) for three specimens: Doedicurus clavicaudatus (PIMUZ A/V 4148); Glyptodon munizi (PIMUZ A/V 461), and Neosclerocalyptus pseudornatus (PIMUZ A/V 439). We reconstructed the braincase while delineating the olfactory bulbs, cerebrum, and cerebellum in accordance with the work of Boscaini et al. (2020a) on Catonyx tarijensis Gervais & Ameghino, 1880, an extinct ground sloth. All the canals connecting with the braincase were reconstructed and identified following Le Verger et al. (2021), which allowed us to make the link with the analysis of the external anatomy through the opening of the canals by the cranial foramina (Fig. 2). ...
... (2021) (see below). The rami temporales observed in all species open in the cranial roof in various foramina (e.g., Gaudin & Wible, 2006), marking auxilliary canals from the main braincase canals for the vascularization of temporalis muscles, here, emerging mainly from the orbitotemporal canal ( Fig. 11 (Boscaini et al., 2020a;Le Verger et al., 2021;Wible & Gaudin, 2004). Moreover, in Doedicurus clavicaudatus (PIMUZ A/V 4148), the oval canal, which transmits the mandibular division of the trigeminal nerve (see for sloths Boscaini et al., 2020b), is directed more laterally in anterior view than in the remaining specimens. ...
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With their odd cranial features, glyptodonts, closely related to extant armadillos, are a highly diverse group of the South American megafauna. Doedicurus, Glyptodon, Panochthus, and Neosclerocalyptus were present in the “Pampean Formation” during the Pleistocene, and they are all exceptionally preserved in the Santiago Roth Collection, thus ofering the possibility of investigating these four well-diversifed genera. A total of 13 specimens (seven species) were analysed and compared in a qualitative/quantitative study of external cranial remains and endocranial reconstructions (i.e., braincase and associated cranial canals, and inner ears). We report on anatomical features that contribute to existing phylogenetic matrices; many of them are new potential synapomorphies supporting the current hypotheses regarding the evolutionary history of the Pleistocene glyptodonts. These include the anterior cranial shape, the position of the basicranium in respect to the whole cranium, the shape of the cranial roof, the position of the largest semicircular canal, and the inclination of the cerebrum. They may represent new shared-derived features among Glyptodon, Doedicurus, Neosclerocalyptus, and Panochthus. We also provide detailed comparative descriptions highlighting new potential convergences in respect to current phylogenies, concerning, for instance, the shape of the foramen magnum, the global shape of the cranium, orbital shape, cochlear position, and a strong protrusion of the zygomatic process of the squamosal. In light of these results, we discuss morphological transformations across phylogeny. The endocranial comparison brought insights on the phylogenetic patterns of cranial canal evolution.
... In their work on the brain of Glossotherium, Boscaini et al. (2018) observed that there are many similarities between the endocranial cast of this ground sloth and the extant sloth Choloepus, particularly regarding the pattern of sulci and convolutions, whereas the extant sloth Bradypus has more similarities with the Miocene sloths Hapalops and Eucholoeops. Boscaini et al. (2020) interpreted these similarities based on the phylogenetic scenarios with the best evidence up to that time (Gaudin 2004), which placed Bradypus as the most basally diverging sloth, and Choloepus within the clade Megalonychidae. However, the most recent molecular analyses (Delsuc et al. 2019;Presslee et al. 2019) ally Choloepus with the mylodont clade, so it would be more closely related to Glossotherium, whereas Bradypus is placed within the megatherioid clade, and is therefore possibly more closely related to Hapalops and Eucholoeops. ...
... However, the most recent molecular analyses (Delsuc et al. 2019;Presslee et al. 2019) ally Choloepus with the mylodont clade, so it would be more closely related to Glossotherium, whereas Bradypus is placed within the megatherioid clade, and is therefore possibly more closely related to Hapalops and Eucholoeops. These new phylogenetic analyzes are congruent with the observations on the endocast morphology of sloths studied by Boscaini et al. (2020). ...
Chapter
Xenarthrans, a largely endemic group originating in South America, constitute one of the four major clades of placental mammals. The order Cingulata is composed of extant and extinct xenarthrans that possess a carapace formed by dermal ossicles, i.e. armadillos, pampatheres and glyptodonts. Towards the end of the nineteenth century the study of natural endocasts showed that the brain of glyptodonts was small relative to their body size, with an unusual external neuroanatomy, particularly due to the large size of the olfactory bulbs and cerebellum, and the lissencephalic neocortex. Recently, CT scans allowed us to increase our knowledge of cingulate paleoneurology, including glyptodonts and pampatheres. These new analyses largely corroborate early observations of the glyptodont brain, and show that the pampathere brain presents differences with both glyptodonts and armadillos. Furthermore, it has allowed to reconstruct their inner ear anatomy. Some functional aspects of cingulate paleobiology has also been inferred from the anatomy of the semicircular canals. These analyses have allowed us to obtain a more complete picture of the paleoneurological evolution in this group of mammals. However, more specimens and new species are still needed to better understand their intraspecific variation, as well as their evolutionary patterns and functional implications.
... As stated in ref. 109, living Xenarthra show many cortical architectural traits in common with the stem eutherian mammal, including the motor cortex. We followed the sulcal pattern in Xenarthra described in ref. 110. ...
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Although intense research effort is seeking to address which brain areas fire and connect to each other to produce complex behaviors in a few living primates, little is known about their evolution, and which brain areas or facets of cognition were favored by natural selection. By developing statistical tools to study the evolution of the brain cortex at the fine scale, we found that rapid cortical expansion in the prefrontal region took place early on during the evolution of primates. In anthropoids, fast-expanding cortical areas extended to the posterior parietal cortex. In Homo, further expansion affected the medial temporal lobe and the posteroinferior region of the parietal lobe. Collectively, the fast-expanding cortical areas in anthropoids are known to form a brain network producing mind reading abilities and other higher-order cognitive functions. These results indicate that pursuing complex cognition drove the evolution of Primate brains.
... Virtual endocranial reconstructions and geometric morphometric techniques have proved useful for studying the diversification of brain shape and size in different vertebrate groups (e.g. Bertrand et al., 2019;Boscaini et al., 2020;Early et al., 2020;Weisbecker et al., 2021). Virtual reconstructions provide a basis for brain morphological comparisons between living and fossil organisms. ...
Article
Brain morphological variation is analysed through virtual endocasts in a highly diversified clade of caviomorph rodents belonging to the family Echimyidae. Diversification in brain size and shape is explored through geometric morphometrics and comparative phylogenetic analyses. The results indicate that brain shape is largely independent of general size and reveal different trends in brain size and shape. Fossorial Euryzygomatominae, arboreal Echimyini and the semi-aquatic Myocastorini Myocastor show high encephalization; the former with a greater contribution from the olfactory bulb and petrosal lobe, and the latter two with a larger surface area of neocortex. The Euryzygomatomyinae and Myocastorini of terrestrial habits show low encephalization with a low contribution of the neocortex. Phylogenetic comparative analyses suggest that endocranial morphological evolution would have been influenced by both phylogeny and locomotor habits. The concurrence of the best fit of the Ornstein–Uhlenbeck model and the significant phylogenetic signal in the datasets suggests the involvement of constraints on morphological diversification within the major clades, as expected under phylogenetic conservatism. This could be explained by an early establishment of a particular endocranial morphology in each major clade, which would have been maintained with relatively little change.
... Although the cranial anatomy is relatively well known in xenarthrans, their internal cranial anatomy remains poorly studied. Yet, several studies have shown that their exploration provides systematic interest on their past and present diversity (Zurita et al., 2011;Fernicola et al., 2012;Billet et al., 2015;Tambusso & Fariña, 2015a;Tambusso & Fariña, 2015b;Billet et al., 2017;Boscaini et al., 2018;Boscaini et al., 2020;Tambusso et al., 2021). In a recent study (Le Verger et al., 2021), we describe and compare 8 cranial canals (involved in the vascularization and innervation of the cranium) and alveolar cavities ( Figure 1) of 30 specimens belonging to the Cingulata. ...
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The present 3D Dataset contains the 3D models analyzed in the following publication: Le Verger K., González Ruiz L.R., Billet G. 2021. Comparative anatomy and phylogenetic contribution of intracranial osseous canals and cavities in armadillos and glyptodonts (Xenarthra, Cingulata). Journal of Anatomy 00: 1-30 p. https://doi.org/10.1111/joa.13512
... Glossotherium robustum (Owen, 1842) Boscaini et al., 2020b;Brambilla & Ibarra, 2018a;McAfee, 2009McAfee, , 2016Pitana et al., 2013). Initial diagnoses to distinguish mylodont species were based primarily on cranial characters including teeth (Brambilla & Ibarra, 2018a;McAfee, 2009). ...
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Unlabelled: The present work concerns xenarthrans from the collection of Santiago (Kaspar Jakob) Roth (1850-1924) hou