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Digital cranial endocast of Pseudoplohophorusabsolutus (Xenarthra, Cingulata) and its systematic andevolutionary implicationsP Sebastián Tambussoa & Richard A. Fariñaa

a Sección Paleontología, Facultad de Ciencias, Universidad de la República, Iguá 4225, 11400Montevideo, Uruguay, ;Published online: 20 Jul 2015.

To cite this article: P Sebastián Tambusso & Richard A. Fariña (2015): Digital cranial endocast of Pseudoplohophorusabsolutus (Xenarthra, Cingulata) and its systematic and evolutionary implications, Journal of Vertebrate Paleontology, DOI:10.1080/02724634.2015.967853

To link to this article: http://dx.doi.org/10.1080/02724634.2015.967853

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ARTICLE

DIGITAL CRANIAL ENDOCAST OF PSEUDOPLOHOPHORUS ABSOLUTUS (XENARTHRA,CINGULATA) AND ITS SYSTEMATIC AND EVOLUTIONARY IMPLICATIONS

P. SEBASTI �AN TAMBUSSO* and RICHARDA. FARIeNASecci�on Paleontolog�ıa, Facultad de Ciencias, Universidad de la Rep�ublica, Igu�a 4225, 11400 Montevideo, Uruguay,

pasebita@gmail.com; fari~a@fcien.edu.uy

ABSTRACT—Glyptodonts are a group of extinct xenarthrans with several anatomical features that make them one of themost bizarre groups of mammals. By the late 19th century, some authors began to analyze the brain of Pleistoceneglyptodonts using natural endocranial casts. These studies revealed the small size of the brain of the large Pleistocene forms.However, the evolution of the brain in glyptodonts and how it fits in a phylogenetic context has not been analyzed. In orderto evaluate the evolution of the brain in this group, we described the first digital endocranial cast of the late Mioceneglyptodont Pseudoplohophorus absolutus and compared it with digital endocranial casts of the Pleistocene glyptodontsGlyptodon, Doedicurus, and Panochthus and the extant armadillos Dasypus, Euphractus, Chaetophractus, and Zaedyus. Theendocast morphology of P. absolutus is similar to that of Pleistocene glyptodonts: large olfactory bulbs, a small cerebrum witha single neocortical sulcus, and a large cerebellum. However, the relative brain size is larger than in the Pleistocene forms,with values of the encephalization quotient (EQ) close to that of extant armadillos. A comparison between xenarthransorders shows that Cingulata (glyptodonts and armadillos) have lower EQ values than Pilosa (sloths and vermilinguas). Thiscould possibly be related to certain restrictions and benefits imposed by the presence of the carapace in cingulates.Furthermore, because the carapace restricts the development of the cervical musculature that supports the skull, the smallsize of the brain in glyptodonts could be a trade-off (along with others) to reduce the weight of the skull.

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

INTRODUCTION

The order Cingulata is divided into Dasypodoidea, consistingof living and extinct armadillos, and Glyptodontoidea, a mono-phyletic group that includes glyptodonts and pampatheres, bothextinct (McKenna and Bell, 1997). More recent phylogenies con-sider armadillos a paraphyletic group and the clade of glypto-donts and pampatheres the most derived group (Gaudin andWible, 2006; Fernicola, 2008; Fernicola et al., 2008; Gaudin andMcDonald, 2008).Glyptodonts have several anatomical features that make them

one of the most bizarre groups of mammals (Burmeister, 1874;Carlini and Zurita, 2010; Fari~na et al., 2013). Like all cingulates,they bear a carapace composed of a mosaic of dermal scutes.Another anatomical peculiarity is the complete fusion of the tho-racic and lumbar vertebrae to form tough dorsal tubes (Lydek-ker, 1894; Gillette and Ray, 1981). Also, the presence of a caudaltube is characteristic of glyptodonts (with the exception of theclades Propalaehoplophoridae and Glyptodontinae [Fernicolaand Porpino, 2012]); in some species (i.e., Doedicurus clavicau-datus), it forms a large tail club that may have been adapted forantagonistic behavior (Fari~na, 1995; Alexander et al., 1999;Blanco et al., 2009).The singular position of the masticatory apparatus in large

glyptodonts, situated almost completely underneath the brain-case, is a unique feature among mammals (Fari~na and Parietti,1983; Fari~na, 1985, 1988; Fari~na and Vizca�ıno, 2001). It could

have evolved as a consequence of an increase in body size andthe presence of a carapace. Telescoping the masticatory appara-tus underneath the braincase reduces the moment arm of theskull and allows for a reduced cervical musculature to fulfill itsrole. The evolution of this pattern can be observed in older andsmaller forms such as the 80-kg early Miocene genus Propalae-hoplophorus, in which the trend of telescoping is less developedthan in larger Pleistocene forms such as Glyptodon (Fari~na andParietti, 1983; Fari~na and Vizca�ıno, 2001). The external mor-phology of the skull of glyptodonts has been widely studied(Huxley, 1865; Burmeister; 1874; Lydekker, 1894; Vinacci Thul,1945; Gillette and Ray, 1981); however, the internal anatomy isless understood because of the difficulty of its visualization(Macrini et al., 2007b).In fossil vertebrates, the brain can be studied through endocra-

nial casts, either natural or artificial. In most birds and mammals,the brain fills the entire cranial cavity; therefore, the endocranialcasts largely reproduce the external morphology of the brain(Jerison, 1973).Regarding the Cenozoic mammals of South America, a con-

siderable number of paleoneurological studies have been carriedout. They include marsupials, xenarthrans (Gervais, 1869;Dechaseaux, 1958, 1962; Quiroga, 1980, 1988; Dozo, 1987, 1989a,1989b, 1994a, 1994b, 1998; Quiroga and Dozo, 1988; Macriniet al., 2007b), notoungulates, litopterns, rodents, and carnivorans(Simpson, 1933a, 1933b; Dechaseaux, 1962; Jerison, 1973; Radin-sky, 1981; Dozo, 1997a, 1997b; Dozo et al., 2004). Withinxenarthrans, glyptodonts are the group in which the fewest pale-oneurological studies have been carried out. The few analyses ofPleistocene glyptodonts have not been updated by recent work(Serres, 1865; Gervais, 1869; Dechaseaux, 1958). They show thatthe brain was rather lissencephalic and, in absolute terms, quite

*Corresponding author.Color versions of one or more of the figures in this article can be found

online at www.tandfonline.com/ujvp.

Journal of Vertebrate Paleontology e967853 (12 pages)� by the Society of Vertebrate PaleontologyDOI: 10.1080/02724634.2015.967853

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small for the large body size of these animals. However, the evo-lution of the brain in glyptodonts and how it fits in a phylogeneticcontext have not been analyzed.Several glyptodonts from the Oligocene to Pleistocene

reached large size, with some genera exceeding 1000 kg in adultbody mass (Scillato-Yan�e, 1977; Fari~na et al., 1998, 2013; Viz-ca�ıno et al., 2012b). Nevertheless, not all glyptodonts reachedsuch a large body size; several genera did not exceed a bodymass of 100 kg (e.g., Vizca�ıno et al., 2012a). The descriptions ofthe brain have been focused on the very large Pleistocene gen-era, with no analyses so far conducted of more basal or smallerglyptodonts.Here we describe the first endocranial cast of a glyptodont

from the late Miocene of Uruguay, Pseudoplohophorus absolu-tus Perea, 2005, and compare it with endocasts of Pleistoceneglyptodonts and extant armadillos in order to evaluate the maincharacteristics and evolutionary patterns in these xenarthrans,including quantitative features such as relative brain size.

Institutional Abbreviations—FC-DPV, Departamento dePaleontolog�ıa de Vertebrados, Facultad de Ciencias, Universi-dad de la Rep�ublica, Montevideo, Uruguay; MACN-Pv,Colecci�on Nacional de Paleontolog�ıa de Vertebrados, MuseoArgentino de Ciencias Naturales ‘Bernardino Rivadavia,’ Bue-nos Aires, Argentina; MMBR, Museo Municipal ‘BautistaRebuffo,’ Colonia, Uruguay; MPAC, Museo paleontol�ogico‘Armando Calcaterra,’ Colonia, Uruguay; TMM M, Recentmammal collections of the Vertebrate Paleontology Laboratory,Texas Memorial Museum, Austin, Texas, U.S.A; ZVC-M,Colecci�on de Vertebrados, Mam�ıferos, de Facultad de Ciencias,Universidad de la Rep�ublica, Montevideo, Uruguay.

MATERIALS ANDMETHODS

Specimens

The digital endocast of Pseudoplohophorus absolutus (FC-DPV 595) was extracted from a specimen collected in the coastalcliffs of Rio de la Plata at Arazat�ı, Department of San Jos�e, Uru-guay, from late Miocene deposits assigned to the Camacho For-mation (Perea, 2005). The skull is complete and undistorted,with partial damage in the squamosal portion of the left zygo-matic arch (Fig. 1). The endocast of P. absolutus was comparedwith Pleistocene glyptodont digital endocasts extracted fromskulls of Doedicurus clavicaudatus (FC-DPV no number), Glyp-todon sp. (MPAC 11-04), Glyptodon sp. (MACN-Pv 15152), andPanochthus tuberculatus (MMBR 1103a), and with extant arma-dillo digital endocasts from Chaetophractus villosus (ZVC-M nonumber), Dasypus novemcinctus (TMM M-7417), Dasypushybridus (ZVC-M no number), Euphractus sexcinctus (ZVC-M105), and Zaedyus pichiy (TMM no number).The endocast anatomical terms are based on Dozo (1987,

1998) and Butler and Hodos (1996).

CT Scanning and Endocast Extraction

The specimens P. absolutus, Glyptodon sp. MPAC 11-04, D.clavicaudatus, and P. tuberculatus were computed tomographi-cally (CT) scanned in the year 2011 at Hospital Mautone, Maldo-nado, Uruguay, using a General Electric (GE) 16 slice BrightSpeed CT scanner. The skulls were scanned in the coronal planeat 120 kV and 200 mA; the resulting slices have a thickness of0.625 mm. The specimens Glyptodon sp. MACN-Pv 15152, D.hybridus, E. sexcinctus, and C. villosus were scanned in 2004 atHospital Mautone, Maldonado, Uruguay, using a General Elec-tric CT/E scanner. The skulls were scanned in the coronal planeat 120 kV and 200 mA, which yielded 2-mm-thick slices. The CTscans of D. novemcinctus and Z. pichiy were obtained from theWeb site ‘digital morphology’ of the University of Texas (http://www.digimorph.org). The digital endocasts were extracted from

the CT slices using the software BioVis3D 3.0 and Amira 5.2(2008; Visage Imaging), which allows three-dimensional recon-struction of structures from a series of two-dimensional images.

Endocast Volume and Body Mass Relationship

Relative brain size analyses have been used to assess theencephalization grade and the evolution of the brain among andwithin different taxonomic groups (Jerison, 1973; Finarelli andFlynn, 2007). Here we analyze the relative brain size of glypto-donts and armadillos in order to compare the brain-body sizerelationship within cingulates and between these and the rest ofmammals through the encephalization quotient (EQ); this quo-tient is the ratio of actual brain size to expected brain size (Jeri-son, 1973). The actual brain size (Ei) is the measured volume ofthe brain (or endocast), and the expected brain size (Ee) is the

FIGURE 1. Semitransparent digital render of the skull of Pseudoploho-phorus absolutus to show the endocast in situ.A, left lateral view; B, dor-sal view. Scale bar equals 10 cm.

Tambusso and Fari~na—Digital endocast of Pseudoplohophorus (e967853-2)

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expected volume of the brain (or endocast) in a mammal of thesame body mass (m). The latter is obtained from the equation ofa linear regression of brain volume versus body mass in a sampleof extant mammals.The total volume of the digital endocast of the specimens ana-

lyzed was calculated with Amira. The endocast was divided intothree regions: olfactory bulbs, cerebrum, and cerebellum. Theseregions were sectioned with the software netfabb Studio. Theanterior limit of the cerebrum was located at the anterior-mostexpansion of the frontal lobe, which coincides with the beginningof the peduncle of olfactory bulbs. The posterior limit of the

cerebrum was located at the transverse sulcus, which separatesthe cerebellum (Fig. 2D). The volume of the three regions wasalso calculated and expressed as percentages of the total endo-cast volume; each region was compared in the different taxathrough an analysis of variance. The body mass of glyptodontswas estimated from skull measurements following the best esti-mators among the equations in Fari~na et al. (1998). For armadil-los, body mass was estimated assuming geometric similarity inthe skull size and body size taken from the literature. The brainvolume and body mass of 796 living mammals included in 26orders were obtained from the literature. Data on five fossil

FIGURE 2. Digital endocast of Pseudoplohophorus absolutus in A, dorsal view; B, left lateral view; C, ventral view;D, schematic lateral view show-ing the divisions of the three regions of the endocast and the lobes of the cerebrum. Abbreviations: cbl, cerebellum; cblh, cerebellar hemisphere; cer,cerebrum; hr, hypophyseal region; ic, internal carotid; ob, olfactory bulb; pl, pyriform lobe; rf, rhinal fissure; sls, superior longitudinal sulcus; ss, supra-sylvian sulcus; trs, transverse sinus; ts, transverse sulcus; v, vermis; II–XII, cranial nerves. Scale bar equals 5 cm.

Tambusso and Fari~na—Digital endocast of Pseudoplohophorus (e967853-3)

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xenarthrans were obtained and included in the analyses (Supple-mentary Data 1).The expected brain size for the EQ was obtained from a linear

regression on the data of the total sample of extant mammals. Toanalyze whether the allometric relationship between brain sizeand body mass in xenarthrans is equal or different from the othermammalian orders, those orders with five or more species werecompared by analysis of covariance.

RESULTS

Digital Endocasts

In all 10 specimens analyzed a complete digital endocast wasobtained, in which all major regions (olfactory bulbs, cerebrum,and cerebellum) can be identified. In addition, the majority ofthe cranial nerves and some vascular elements werereconstructed.The endocast of P. absolutus has large, oval, and pedunculate

olfactory bulbs, slightly anterolaterally divergent at an angle of37.5� measured in ventral aspect (Appendix 1). The olfactorypeduncles are elongated and not covered by the neocortex(Fig. 2A, B). The volume of the olfactory bulbs represents 5.7%of the total endocast volume. In the Pleistocene glyptodontsGlyptodon sp. MACN-Pv 15152, D. clavicaudatus, and P. tuber-culatus, the olfactory bulbs are oval, pedunculated, and larger,with a relative volume of 7.4%, 8.4%, and 9.7%, respectively; inGlyptodon sp. MPAC 11-04, the volume is slightly smaller, 4.8%(Table 1). With the exception of Glyptodon sp. MACN-Pv15152, the olfactory bulbs of Pleistocene glyptodonts are moreanterolateral divergent, with angles of 46.5–73� (Appendix 1).The olfactory peduncles are not covered by the neocortex either(Figs. 3A–D, S1–S4). In the extant armadillos, the olfactorybulbs are triangular, sessile, and less divergent than in glypto-donts (Appendix 1, Figs. 3E–I, S5–S9), although the size is com-parable and even larger: 7.3–10.7% (Table 1, Fig. 4). However,the analysis of variance (ANOVA) between glyptodonts andarmadillos does not show significant differences in the volume ofthe olfactory bulbs (ANOVA, F1,8 D 4.065, P > 0.05).The cerebrum of P. absolutus is subtriangular in dorsal view, wid-

ening towards the caudal region and with a maximum transversewidth of 54.1 mm at the posterior end of the cerebral hemispheres.In lateral view, the dorsal surface is convex (Fig. 2B). It has a maxi-mum anteroposterior length of 46.5 mm and does not cover theolfactory bulbs or the cerebellum; the length/width ratio is 0.86. Themaximum height is 40.8 mm, and the length/height ratio is 1.14(Appendices 1, 2). In the region of the interhemispheric sulcus liesthe superior sagittal sinus. The rhinal fissure is observed in lateraland dorsal views and extends continuously and horizontally alongthe hemispheres, ventrally delimiting a large pyriform lobe. Thesuprasylvian sulcus is located in the temporal lobe of the cerebralhemispheres and extends posterodorsally. The volume of the

cerebral hemispheres represents 65.2% of the endocast (Table 1).Except forGlyptodon sp. MACN-Pv 15152, in the Pleistocene glyp-todonts the shape of the cerebrum is less triangular in dorsal view(Figs. 3A–D, S1–S4). The length/width and length/height ratios haveranges of 0.92–1.11 and 1.30–1.53, respectively (Appendices 1, 2).These higher ratios in Pleistocene glyptodonts mean that the cere-brum is more anteroposteriorly elongated and more dorsoventrallycompressed, although the dorsal surface is as convex as in P. absolu-tus. In all of them, the cerebral hemispheres do not cover the olfac-tory bulbs nor the cerebellum. The superior sagittal sinus is present.The rhinal fissure has the same characteristics as in P. absolutus. Inboth specimens of Glyptodon sp., the suprasylvian sulcus is locatedin the temporal lobe of the cerebral hemispheres as in P. absolutus;in D. clavicaudatus and P. tuberculatus, it is more displaced to thefrontal lobe. The proportion of the cerebrum in the endocast is63.8% inD. clavicaudatus, 63.8% in P. tuberculatus, 64.8% inGlyp-todon sp. MACN-Pv 15152, and 65.1% inGlyptodon sp. MPAC 11-04 (Table 1). In the extant armadillos D. hybridus and D. novem-cinctus, the cerebrum is ovoid, whereas in C. villosus, E. sexcinctus,and Z. pichiy it is more triangular (Figs. 3E–I, S5–S9). In the lastthree, in lateral view the dorsal surface of the frontal lobe slopedown to the olfactory bulbs. The length/width and length/heightratios have ranges of 0.74–0.93 and 0.93–1.11, respectively(Appendix 2); therefore, the cerebrum is less anteroposteriorly elon-gated and dorsoventrally compressed than in glyptodonts. The rhinalfissure has an anterior and a posterior branch (Dozo, 1998), ventrallydelimiting a very large pyriform lobe. There are two sulci in the cere-bral hemispheres: the suprasylvian sulcus in the temporal lobe andthe presylvian sulcus, which extends anterodorsally, in the frontallobe. The superior longitudinal sinus is not observed. The proportionof the cerebrum in the endocast is 65.4% inD. novemcinctus, 67.8%inD. hybridus, 70.3% inE. sexcinctus, 70.7% inZ. pichiy, and 72.1%inC. villosus (Table 1). The analysis of variance shows that the cere-brum is significantly larger in extant armadillos than in glyptodonts(ANOVA, F1,8D 14.221, P< 0.01) (Fig. 4).The cerebellum of P. absolutus is large; its volume represents

29.2% of the digital endocast. The cerebellar hemispheres arevisible. In lateral view, the vermis is dorsally projected abovethem (Fig. 2B). The maximum width of the cerebellum,47.7 mm, is less than the maximum width of the cerebrum. Themaximum length is 18.5 mm, and the length/width ratio is 0.39(Appendices 1, 2). In the Pleistocene glyptodonts, the cerebel-lum also occupies a large proportion of the endocast (26.5–30%;Table 1). The cerebellar hemispheres and the vermis are visible,although in P. tuberculatus the separation between them is lessclear (Figs. 3D, S4). The length/width ratio range is 0.48–0.55,indicating that in P. absolutus the cerebellum is slightly shorterthan in Pleistocene glyptodonts. In the extant armadillos, the cer-ebellum is separated from the cerebrum by a posteromedial ossi-fied tentorium cerebelli; this structure is not observed inglyptodonts. The cerebellar hemispheres are separated from thevermis by two deep paramedian sulci (Figs. 3E–I, S5–S9). The

TABLE 1. Body mass, total endocast volume, and relative size of olfactory bulbs, cerebrum, and cerebellum expressed as percentage of total endo-cast volume in glyptodonts and extant armadillos.

Taxon Body mass (g) Total endocast volume (cm3) % Olfactory bulbs % Cerebrum % Cerebellum

Glyptodon sp. MACN-Pv 15152 2,012,000 234.12 7.4 64.8 27.8Glyptodon sp. MPAC 11-04 946,000 213.38 4.8 65.1 30.0Panochthus tuberculatus 1,453,000 212.61 9.7 63.8 26.5Doedicurus clavicaudatus 1,229,000 233.81 8.4 63.8 27.8Pseudohoplophorus absolutus 209,000 100.98 5.7 65.2 29.2Dasypus novemcinctus 3500 10.17 10.7 65.4 23.9Dasypus hybridus 4900 13.07 7.3 67.8 24.9Zaedyus pichiy 1300 6.05 10.6 70.7 18.7Chaetophractus villosus 3700 14.6 9.5 72.1 18.4Euphractus sexcinctus 6800 20.65 10.1 70.3 19.7

Tambusso and Fari~na—Digital endocast of Pseudoplohophorus (e967853-4)

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FIGURE 3. Digital endocast ofGlyptodon sp. MACN-Pv 15152 inA, dorsal view;A’, left lateral view;Glyptodon sp. MPAC 11-04 in B, dorsal view;B’, left lateral view; Doedicurus clavicaudatus in C, dorsal view; C’, left lateral view; Panochthus tuberculatus in D, dorsal view; D’, left lateral view;Dasypus novemcinctus in E, dorsal view; E’, left lateral view; Dasypus hybridus in F, dorsal view; F’, left lateral view; Chaetophractus villosus in G,dorsal view; G’, left lateral view; Euphractus sexcinctus in H, dorsal view; H’, left lateral view; Zaedyus pichiy in I, dorsal view; I’, left lateral view.Abbreviations: arf, anterior rhinal fissure; cblh, cerebellar hemisphere; cer, cerebrum; ihs, interhemispheric sulcus; ob, olfactory bulb; otc, ossified ten-torium cerebelli; pl, pyriform lobe; pms, paramedian sulcus; prf, posterior rhinal fissure; ps, presylvian sulcus; rf, rhinal fissure; sls, superior longitudinalsulcus; ss, suprasylvian sulcus; trs, transverse sinus; v, vermis; II–XII, cranial nerves. All scale bars equal 5 cm.

Tambusso and Fari~na—Digital endocast of Pseudoplohophorus (e967853-5)

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cerebellum represents 18.4–24.9% of the endocast (Table 1);although in the armadillos the cerebellum is large, the propor-tions are smaller than in the glyptodonts (Fig. 4) and the analysisof variance shows that the cerebellum is larger in glyptodonts(ANOVA, F1,8 D 21.843, P < 0.005). Both D. novemcinctus andD. hybridus have greater length/width ratios (0.52 and 0.63,respectively) than P. absolutus, whereas Z. pichiy, E. sexcinctus,and C. villosus have lower length/width ratios (Appendix 2).Most cranial nerves (CNs) and some vascular elements were

reconstructed in the digital endocasts of glyptodonts and arma-dillos. In the ventral surface of the endocast of P. absolutus(Fig. 2C), towards the anterior third, lies the canal for the opticnerve (CN II). In the Pleistocene glyptodonts and extant arma-dillos, this nerve has a similar location (Figs. S1–S9). The hypo-physeal fossa is located in the center of the endocast posterior to

the optic nerve. Lateral to this one, the canal for the oculomotornerve (CN III), trochlear nerve (CN IV), ophthalmic and maxil-lary branches of the trigeminal nerve (CN V1, 2), and abducensnerve (CN VI). In P. absolutus, Glyptodon, andD. clavicaudatus,this canal has an anteroposterior horizontal direction (Figs. 2C,S1–S3), whereas in P. tuberculatus it is more anteroventrally dis-placed (Fig. S4). In extant armadillos, the canal has an antero-posterior horizontal course, except in D. novemcinctus and D.hybridus in which the canal has an anterolateral course (Figs. S5,S6). The CNs III, IV, V1, 2, and VI exit the skull through thesphenorbital fissure/foramen rotundum (Gaudin and Wible,2006). The canal for the mandibular branch of the trigeminalnerve (CN V3) is located posterior and lateral to the sphenorbitalfissure/foramen rotundum. In P. absolutus, this nerve was recon-structed only on one side of the endocast because on the otherside the canal was not preserved. The size and location of CN V3

is comparable in all glyptodonts (Figs. S1–S4), although in P.tuberculatus and Glyptodon sp. MPAC 11-04 the cast of the tri-geminal ganglion is more evident. In the armadillos Z. pichiy, E.sexcinctus, and C. villosus, CN V3 is located more posteriorlythan in D. novemcinctus and D. hybridus, although in the latterthe trigeminal ganglion is less evident (Figs. S5–S9). Medial toCN V3 and posterolateral to the hypophyseal fossa, the canal forthe internal carotid artery is observed. In glyptodonts, this canalis seen next to the CN V3, whereas in armadillos it lies next tothe hypophyseal fossa (Figs. S1–S9). Posterior to CN V3 lies thecast of the internal acoustic meatus (IAM), which transmits thefacial nerve (CN VII) and the vestibulocochlear nerve (CNVIII). In P. absolutus, Glyptodon sp. MPAC 11-04, D. novem-cinctus, and P. tuberculatus, it is possible to observe a lateralbifurcation in the IAM that corresponds to the canals for eachnerve (Figs. 3, S2–S4). Posteroventral to the IAM is the cast ofthe jugular foramen, which transmits the glossopharyngeal (CNIX), vagus (CN X), and spinal accessory (CN XI) nerves and thejugular vein. At the level of the medulla is the cast of the hypo-glossal nerve (CN XII). In both specimens ofGlyptodon, the castof the CN XII is much greater than in the other glyptodonts,which is congruent with the observations of Burmeister (1874).

Relative Brain Size

Results of body mass estimates (Table 1) are congruent withother body mass estimations of extinct xenarthrans (Bargo et al.,2000; Vizca�ıno et al., 2006, De Esteban-Trivigno et al., 2008)and data reported in the literature of extant xenarthrans (Crileand Quiring, 1940; Biknevicius, 1999; Smith et al., 2003; De Este-ban-Trivigno et al., 2008).The allometric relationship between log brain volume versus

log body mass analyzed in the full data set of mammals(Table S1) results in a slope of 0.751 (r2 D 0.954, P < 0.0001) andan intercept of ¡1.295, which is congruent with results of otherauthors (Isler, 2011; Boddy et al., 2012). The result of this allo-metric relationship was used in the encephalization quotient(EQ) equation, Ee D 0.050 m0.751. Two groups have higher val-ues of EQ, primates and cetaceans (Fig. 5), although, as Boddyet al. (2012) pointed out, both groups have a high variance in thevalues of EQ. Carnivorans and proboscideans also have high EQvalues. Extant armadillos have EQs (0.44–1.06) that do not differfrom the remaining mammalian orders, whereas glyptodontshave the lowest values (0.12–0.40). P. absolutus has the highestEQ (0.40) among glyptodonts, whereas the maximum value inthe Pleistocene glyptodonts is 0.23 for Glyptodon sp. MPAC 11-04 (Appendix 3).In orders with five or more species (Afrosoricida, Artiodac-

tyla, Carnivora, Cetacea, Chiroptera, Erinaceomorpha, Lago-morpha, Macroscelidea, Perissodactyla, Primates, Rodentia,Soricomorpha, and Xenarthra), the slope of the linear regres-sion has a range of 0.51–0.84 (Table S2) and the analysis of

FIGURE 4. Size proportions of the olfactory bulbs, cerebrum, and cere-bellum related to total endocast size in extant armadillos andglyptodonts.

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covariance shows that four orders have significant differencesin their slope: Artiodactyla, Cetacea, Chiroptera, and Pri-mates. The remaining orders have a slope range of 0.56–0.72.The analysis of covariance (ANCOVA) shows no significantdifferences in the value of the slope (ANCOVA, F D 1.303, PD 0.240) but significant differences in the intercept(ANCOVA, F D 35.415, P < 0.0001).Due to the differences in the allometric relationship of brain

volume and body mass in the different orders of mammals, ananalysis of the EQ of glyptodonts and armadillos was performedusing the regression values of the order Xenarthra, Ee D0.123 m0.606. Within xenarthrans, extant armadillos have a rangeof values of EQ from 0.59 to 1.44 and glyptodonts have a rangeof 0.39–0.84.If the EQs of extant armadillos and glyptodonts are compared

with the EQs of sloths (extant and fossils) and vermilinguas cal-culated from the regression of the total data set of mammals, thefossil forms (glyptodonts and ground sloths) have lower valuesthan the extant ones (armadillos, sloths, and vermilinguas). How-ever, when the EQ is calculated from the regression of xenar-thrans, armadillos and glyptodonts have the lowest values,whereas the sloths (extant and fossils) and vermilinguas do notdiffer (Appendix 3).

DISCUSSION

Endocast Morphology

The different species of extant armadillos have some variationin the encephalic morphology (Dozo, 1989a, 1998), and the digi-tal endocasts of the specimens analyzed in the present work arecongruent with that variation, although some traits are commonto all of them. The olfactory bulbs are large. The cerebrum has asimple pattern of cortical sulcus, represented by two sulci: thesuprasylvian sulcus and the presylvian sulcus. The pyriform lobe

is very large, evidenced by a very dorsal position of the rhinal fis-sure, which has divided in an anterior and a posterior ramus. Thecerebellum is also large, and the size proportions are among thelargest in relation to the total size of the brain in mammals(Clark et al., 2001). Large olfactory bulbs and small cerebrumare plesiomorphic features within mammals (Macrini et al.,2007a, 2007b; O’Leary et al., 2013).Some differences in the endocast morphology of extant arma-

dillos could be related to their phylogenetic affinities. Moreclosely related species have a more similar endocasts. Dozo(1998) shows that Chaetophractus and Euphractus have the samepattern of cortical sulcus. These genera together with Zaedyusform the tribe Euphractini, which is phylogenetically supportedby craniodental and molecular traits, although the hypotheses ofthe relationship between them still have some discrepancies(Gaudin and Wible, 2006; Delsuc and Douzery, 2008). From thedigital endocasts of C. villosus, E. sexcinctus, and Z. pichiy, it ispossible to observe that C. villosus and E. sexcinctus are verysimilar in general morphology and not only in the pattern of cor-tical sulcus. Moreover, Z. pichiy has an endocast in which themorphology and sulci pattern are very similar to those of C. vil-losus and E. sexcinctus and different from the endocasts of thetwo species of Dasypus (Fig. 3). In fact, the digital endocasts ofD. novemcinctus and D. hybridus show very little difference,which is congruent with the very close phylogenetic relationshipof these species.The three genera of Pleistocene glyptodonts present some dif-

ferences, although, as in the extant armadillos, some general fea-tures are common to all. The olfactory bulbs are large, but theirvolume proportion relative to the total volume endocast issmaller than in the armadillos. The cerebellum forms a very largeproportion of the endocast (26–30%), being relatively largerthan in armadillos, although the cerebrum is smaller and lesscomplex than in this group. This is congruent with the

FIGURE 5. Encephalization quotient (EQ) ofA, extant mammalian orders; B, extant and fossil xenarthrans.

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observations of Gervais (1869) on the small size of the cerebrumand the large size of the cerebellum in glyptodonts.As mentioned above, the cerebrum of glyptodonts shows a sin-

gle neocortical sulcus, which, according to location and orienta-tion, is homologized with the suprasylvian sulcus. This sulcus wasdescribed by Gervais (1869:45) and, according to him, delimitsthe sylvian gyrus: “. . .montre une sorte de circonvolution rappe-lant la circonvolution sylvienne, et qui est elle-meme labour�eeant�erieurement par un ou deux sillons obliques assez �evidents.”Although the author mentions a possible second oblique sulcusin G. clavipes, in the digital endocast analyzed the presence ofother sulci is not evident.The endocast of P. tuberculatus differs more from the general

morphology of the other genera, mainly in the size and orienta-tion of the olfactory bulbs (Fig. 3A–D). Among Pleistoceneglyptodonts, P. tuberculatus has the largest proportion of olfac-tory bulbs and they are more laterally and ventrally oriented.This could be related to the great development of the paranasalsinuses, which may have pushed the olfactory bulbs to a moreventral region of the skull. In both Glyptodon sp. and D. clavi-caudatus, the paranasal sinuses do not show the great develop-ment observed in P. tuberculatus (Fig. 6) and the olfactory bulbsare less ventrally expanded. For that reason, it might be assumedthat the paranasal sinuses have an effect on the orientation ofthe bulbs in P. tuberculatus.Interestingly, the endocasts ofGlyptodon sp. MACN-Pv 15152

andGlyptodon sp. MPAC 11-04 tend to show greater differencesthan would be expected in species belonging to a single genus.As mentioned above for extant armadillos, although intraspecificand intrageneric variation has not been quantified, and samplesize is small, the two species ofDasypus show very little variationwith regard to each other, whereas in the other three genera thevariation is greater. It could be expected that being part of thesame genus, the two specimens of Glyptodon would have lessvariation between them. One reason for these differences couldbe that the brains of glyptodonts had greater individual variabil-ity. However, the endocast of Glyptodon clavipes illustrated byGervais (1869: pl. 3, fig. 2) is very similar to the endocast ofGlyptodon sp. MACN-Pv 15152. This similarity could supporttheir assignment to a single species and allows us to assume thatthe different species of the genusGlyptodon have some variationin their brain, unlike what is observed in the extant armadillos ofthe genus Dasypus. On the other hand, the species of the genusGlyptodon have a very similar skull, and the identification hasbeen based mainly on the morphology of the dorsal carapaceosteoderms (Zurita et al., 2009, 2011, 2012). If it were possible tocorrelate the similarity (or difference) of the endocast with thespecific assignment in this genus, it would be important for iden-tification of the species based on skull features, without the needfor associated osteoderms. Currently it is not possible to deter-mine whether the differences between the endocasts of Glypto-don sp. MACN-Pv 15152 and Glyptodon sp. MPAC 11-04 aredue to individual variation, to their belonging to distinct species,or to ontogenetic variation.The morphology of the endocast of P. absolutus is similar

to that of Pleistocene glyptodonts, although in quantitativeaspect (see below) it is closer to that of armadillos. Thiscould be due to the fact that P. absolutus is a smaller andmore basal species than the Pleistocene glyptodonts analyzed(Perea, 2005; Fernicola, 2008). Considering only the cere-brum, this is similar to Utaetus buccatus, an early Eocenearmadillo (Dozo, 1998), which has a cerebrum that is lessdeveloped than that of extant armadillos. This is evidencedby the presence of a single neocortical sulcus (although itcould be the result of the fusion of the presylvian and supra-sylvian sulci) a continuous rhinal fissure, and a low develop-ment of the frontoparietal lobe (Dozo, 1998). The presenceof a single neocortical sulcus and a continuous rhinal fissure

could represent the brain morphology in the common ances-tor of armadillos and glyptodonts.

Relative Brain Size

The EQ evaluated from the general equation of mammalsreveals that glyptodonts and ground sloths have smaller brainsthan most extant mammals, including extant xenarthrans. How-ever, when the EQ is calculated from the equation of xenar-thrans, a different result is obtained. In this case, glyptodontsand extant armadillos present the lowest EQ values withinxenarthrans. Because the regression of xenarthrans has a lowerslope than that of the total mammal regression, it is expectedthat specimens with large body masses (such as glyptodonts andground sloths) will have higher EQs. On the other hand, it isinteresting to note that both extant and fossil cingulates have thelower EQ values within xenarthrans.Several hypotheses have been developed to explain the varia-

tion of relative brain size in mammals, including the ‘maternalenergy hypothesis’ (Martin, 1981, 1996), the ‘expensive tissuehypothesis’ (Aiello and Wheeler, 1995; Isler and van Schaik,2009), and the ‘social brain hypothesis’ (Dunbar, 1998). In pla-centals, brain size is partially correlated to weaning age, littersize, and basal metabolic rate (Weisbecker and Goswami, 2010),and a combination of these factors could account for the brainsize in xenarthrans. This kind of analysis is beyond the scope ofthis work, but we can mention some aspects related to these andother factors.In extant sloths, weaning age can be 6 months, although this

time is variable (Gilmore et al., 2008). If the weaning age of allextant Pilosa were greater than in Cingulata, it may be a possiblecause of the difference in brain size between them. If a shortweaning age were a characteristic feature in cingulates, the smallbrain size of glyptodonts could be related to this feature.The presence of the carapace in cingulates could also account

for their smaller brain size. The carapace imposes certain restric-tions on the biology and ecology of armored mammals, such asin locomotor aspects (Lovegrove, 2001) and thermoregulation(Superina and Loughry, 2012). On the other hand, a possiblebenefit of the carapace is the protection against predators(Superina and Loughry, 2012). Extant xenarthrans are among

FIGURE 6. Sagittal slices of A, Glyptodon sp. MACN-Pv 15152; B,Glyptodon sp. MPAC 11-04; C,Doedicurus clavicaudatus;D, Panochthustuberculatus. Abbreviations: ec, endocranial cavity; nc, nasal cavity; ps,paranasal sinus. All scale bars equal 10 cm.

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the mammals with the lowest basal metabolic rates (McNab,1986, 2008). It is possible that cingulates spend less energy on anexpensive organ such as the brain by certain relief that the cara-pace could allow. In glyptodonts, the carapace and the largebody size could have been a passive defense, and they would nothave required high neuronal processing for the development ofescape or defense strategies against predators. A small relativebrain size associated with passive defense strategies is alsoobserved in some ornithischian dinosaurs, such as the armoredankylosaurs, which had a low EQ in comparison with non-armored dinosaurs (except sauropods [Hopson, 1977]). More-over, according to an analysis of the dental occlusal surface area(Vizca�ıno et al., 2006), glyptodonts could have had low meta-bolic rates; therefore, it would be of great importance to knowthe metabolic status of glyptodonts and its relation to energyrequirements.Although inferences about the metabolic rates of fossil species

are complex and often speculative because few osteological fea-tures are clearly related to metabolic requirements, the analysisof Ruben et al. (1996) showed a relationship between the cross-sectional area of the nasal cavity, body mass, and metabolic sta-tus in vertebrates. Similar analyses including glyptodonts andother xenarthrans could improve the inferences on the metabo-lism in these fossil mammals. Also, analysis of dental growthlines, as suggested by Fari~na et al. (2013), and a more extensiveand quantitative examination of palaeohistological data on glyp-todonts, given previous work on xenarthrans (Straehl et al.,2013), could potentially reveal information on physiology andmetabolism in these animals.In island mammals, brain size reduction may be associated

with dwarfism through a reduction in the duration of earlypostnatal brain growth (Weston and Lister, 2009). A case ofreduction of the brain size was observed by K€ohler and Moy�a-Sol�a (2004) in the Plio-Pleistocene bovid Myotragus from theisland of Majorca. They found that the relative brain size ofthis bovid was small compared with extant bovids and withfossil bovids of comparable stratigraphic age and body size.They postulated that the reduction was an adaptive strategyfor more efficient energy use in an island environment (whichlimits the amount of available resources and therefore energyabsorption) and, on the other hand, facilitated by the absenceof predators. The escape strategies, both locomotor and thoseassociated with cognitive development, can be reduced in anenvironment free of predators, and the energy could be reas-signed to other organs or feeding strategies to maximize theenergy absorption (Alexander, 1999; K€ohler and Moy�a-Sol�a,2004).Glyptodonts would not be affected by a restriction in the avail-

ability of resources; their dietary habits could have been anadvantage in the acquisition of resources compared with arma-dillos. The grazer diet of glyptodonts, inferred from the analysesof the masticatory apparatus (Fari~na and Vizca�ıno, 2001; Viz-ca�ıno et al., 2004, 2011), would have allowed them to exploit amore available resource, which in turn would have allowed allo-cating more energy to increased body size.As mentioned before, the carapace restricts the development

of the cervical musculature that supports the skull; because thesize of the skull accompanies the increase in body size, theincrease in the cervical musculature must have been restrictedby the carapace. Telescoping the masticatory apparatus under-neath the braincase reduces the moment arm of the skull, andthe same is true for the reduced brain size observed. Pseudoplo-hophorus had a lower body mass and a less telescoped skull thanthe large Pleistocene glyptodonts, and its relative brain size isthe largest among the glyptodonts. This could imply that there isa trade-off in large Pleistocene glyptodonts between brain andbody size (the larger the body, the relatively smaller the brain),to compensate for the limitations imposed by increased skull

weight versus the restrictions in supportive musculature causedby a large carapace.The small size of the brain in glyptodonts could be the result of

a combination of factors that include life history, low metabolicrate, a passive defense against predators, and the need to reducethe skull weight.

ACKNOWLEDGMENTS

We are grateful to M. E. Castell�o and S. F. Vizca�ıno for valu-able suggestions. Thanks to reviewers G. Billet and K. Porpinoand the editor M. S�anchez-Villagra for comments and correc-tions that improved the manuscript. Thanks to S. Olivieri andthe technical staff of Hospital Mautone for their assistance in theCT scans of the skulls. Thanks to S. Pati~no for improving theEnglish text. ANII (Agencia Nacional de Investigaci�on eInnovaci�on) grant BE_POS_2010_1_2195 to PST partially sup-ported this research.

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Submitted June 13, 2014; revisions received August 27, 2014;accepted August 27, 2014.Handling editor: Marcelo Sanchez-Villagra.

Citation for this article: Tambusso, P. S., and R. A. Fari~na. 2015. Digitalcranial endocast of Pseudoplohophorus absolutus (Xenarthra, Cingulata)and its systematic and evolutionary implications. Journal of VertebratePaleontology. DOI: 10.1080/02724634.2015.967853.

APPENDIX 1. Linear measurements (in mm) of the digital endocasts of glyptodonts and extant armadillos.

Cerebrum Cerebellum

TaxonAngle betweenolfactory bulbs

Maximumlength

Maximumwidth

Maximumheight

Maximumlength

Maximumwidth

Glyptodon sp. MACN-Pv 15152 33.8 60.3 65.4 44.9 26.8 49.1Glyptodon sp. MPAC 11-04 46.5 65.2 63.6 42.6 27.6 53.4Panochthus tuberculatus 73 57.8 60.3 44.5 26 50.9Doedicurus clavicaudatus 64 66.6 59.9 51.1 26.7 55.3Pseudohoplophorus absolutus 37.5 46.5 54.1 40.8 18.5 47.7Dasypus novemcinctus 14 19 25.8 20.5 10 19.2Dasypus hybridus 14.5 22 29.7 22.7 12.3 19.5Zaedyus pichiy 12 19.9 23.9 18 6 19.7Chaetophractus villosus 12.2 26.9 28.8 24.4 9.1 24.7Euphractus sexcinctus 11.8 29.8 33.2 27.6 7.4 22.9

APPENDIX 2. Ratios of the linear measurements in the cerebrum and cerebellum of glyptodonts and extant armadillos.

Cerebrum

Taxon Length/width ratio Length/height ratio Cerebellum Length/width ratio

Glyptodon sp. MACN-Pv 15152 0.92 1.34 0.55Glyptodon sp. MPAC 11-04 1.03 1.53 0.52Panochthus tuberculatus 0.96 1.30 0.51Doedicurus clavicaudatus 1.11 1.30 0.48Pseudohoplophorus absolutus 0.86 1.14 0.39Dasypus novemcinctus 0.74 0.93 0.52Dasypus hybridus 0.74 0.97 0.63Zaedyus pichiy 0.83 1.11 0.30Chaetophractus villosus 0.93 1.10 0.37Euphractus sexcinctus 0.90 1.08 0.32

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APPENDIX 3. Encephalization quotients of fossil and extant xenarthrans, calculated using the regression values of the total data set of mammals(EQT) and using the regression values of xenarthrans (EQX).

Taxon EQT EQX Order

Glyptodon sp. MACN-Pv 15152 0.16 0.47 CingulataGlyptodon sp. MPAC 11-04 0.23 0.61 CingulataPanochthus tuberculatus 0.22 0.60 CingulataDoedicurus clavicaudatus 0.12 0.39 CingulataPseudohoplophorus absolutus 0.40 0.84 CingulataHapalops 0.73 1.36 PilosaMegalonyx 0.45 1.17 PilosaParamylodon harlani 0.32 0.98 PilosaNothrotherium shastensis 0.41 1.05 PilosaVassallia maxima 0.17 0.44 CingulataDasypus novemcinctus 0.44 0.59 CingulataDasypus hybridus 0.44 0.62 CingulataZaedyus pichiy 0.55 0.64 CingulataChaetophractus villosus 0.61 0.82 CingulataEuphractus sexcinctus 0.55 0.80 CingulataChaetophractus vallerosus 0.82 0.94 CingulataTolypeutes mataco 0.77 0.92 CingulataChlamyphorus truncatus 1.02 0.91 CingulataCabassous 1.07 1.44 CingulataMyrmecophaga 0.84 1.47 PilosaTamandua 1.05 1.40 PilosaCyclopes 2.90 2.25 PilosaBradypus variegatus 1.29 1.70 PilosaCholoepus hoffmanni 0.56 0.85 Pilosa

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