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PE Article Number: 15.3.27ACopyright: Palaeontological Association October 2012Submission: 21 June 2012. Acceptance: 19 September 2012

Fernicola, Juan Carlos, Toledo, Néstor, Bargo, M. Susana, and Vizcaíno, Sergio F. 2012. A neomorphic ossification of the nasal cartilages and the structure of paranasal sinus system of the glyptodont Neosclerocalyptus Paula Couto 1957 (Mammalia, Xenarthra). Palaeontologia Electronica Vol. 15, Issue 3;27A,22p; palaeo-electronica.org/content/2012-issue-3-articles/305-glyptodont-nasal-anatomy

A neomorphic ossification of the nasal cartilages and the structure of paranasal sinus system of the glyptodont

Neosclerocalyptus Paula Couto 1957 (Mammalia, Xenarthra)

Juan Carlos Fernicola, Néstor Toledo, M. Susana Bargo, and Sergio F. Vizcaíno

ABSTRACT

Glyptodonts together with armadillos, pampatheres and peltephilines constitutethe Cingulata, one of the three clades of the Xenarthra. The most remarkable feature ofthis group is the presence of an armored exoskeleton along the head, body and tail.Only a few contributions have described in detail the endoskeleton. In the case of theskull, almost no attention has been focused on the narial region. The objective of thisstudy is to provide a description of the narial anatomy of the glyptodont Neoscleroca-lyptus. This genus has the most expanded and globular narial region among glypt-odonts and was recently described as part of the fronto-nasal sinuses system. Ouranalysis based on CT scanning shows that this region includes an independent ossifi-cation of the nasal cartilage that housed the maxillo-atrioturbinates. This ossificationwould represent a neomorphic feature produced by a terminal addition of an ossifiedstage via peramorphosis. Other remarkable anatomical features are the presence ofan expanded paranasal sinuses system that involves the nasal, frontal, parietal andsquamosal bones, and the wide separation between the maxillo-atrioturbinates andethmoturbinates. Functional consequences of this rearrangement are not readily pre-dicted or inferred. Thus, this neomorphic ossification would constitute a morphologicalnovelty, but not necessarily a functional one.

Juan Carlos Fernicola. CONICET - División Paleontología, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Av. Ángel Gallardo 470, C1450DJR Ciudad Autónoma de Buenos Aires, Argentina. [email protected], [email protected] Universidad Nacional de Luján, Departamento de Ciencias Básicas, Ruta Nacional 5 y Av. Constitución, 6700 Luján, ArgentinaNéstor Toledo. División Paleontología Vertebrados, Museo de La Plata, Paseo del Bosque s/n, B1900FWA, La Plata, Argentina. CONICET. [email protected]. Susana Bargo. División Paleontología Vertebrados, Museo de La Plata, Paseo del Bosque s/n, B1900FWA, La Plata, Argentina. CIC. [email protected] F. Vizcaíno. División Paleontología Vertebrados, Museo de La Plata, Paseo del Bosque s/n, B1900FWA, La Plata, Argentina. CONICET. [email protected]

Key words: cingulates; glyptodonts; nasal cavity; narial ossification; neomorphic; function

FERNICOLA, ET AL.: GLYPTODONT NASAL ANATOMY

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INTRODUCTION

The glyptodonts (Xenarthra, Cingulata), com-prising one of the most important groups ofarmored mammals that evolved in the Americas,are known from the middle Eocene to the Pleisto-cene-Holocene boundary (see Fernicola et al.,2008). During the Pleistocene, these herbivorousmammals attained their largest morphologic diver-sity and a high taxonomic richness (22 generaaccording to McKenna and Bell, 1997). All werelarge forms, ranging in body mass from severalhundred kilograms to two tons (Fariña et al., 1998;De Esteban-Trivigno et al., 2008; Vizcaíno et al.,2011a, 2012), and possessed remarkable anatomi-cal features with no functional analogues amongliving mammals that made glyptodonts a peculiargroup. Such features include the presence of anessentially immobile dorsal carapace; hypselodontand mostly lobate teeth consisting of an externallayer of cementum, a matrix of orthodentine and araised central axis of harder osteodentine (Hoff-stetter, 1958; Gillette and Ray, 1981; Fariña andVizcaíno, 2001; Vizcaíno et al., 2004, 2011a,2011b; Fernicola et al., 2008; Vizcaíno, 2009;Kalthoff, 2011); and a unique skull.

The skull morphology (Figure 1) is very differ-ent when compared with that of their extinct andliving relatives, the armadillos (Figure 2.1): the cra-nium is dorsoventrally tall and anteroposteriorlyshort; the rostrum and the masticatory apparatusare positioned below the braincase, producing avery marked angle between the mandibular too-

FIGURE 1. Skull of Pleistocene glyptodonts: 1- Neoscle-rocalyptus paskoensis (MACN-Pv 18107); 2- Neosclero-calyptus sp. (MACN-Pv 8091); 3- Glyptodon reticulatus(MACN-Pv 10153); 4- Panochthus tuberculatus (MLP16-38); 5- Doedicurus sp. (MACN Pv. 2762). Scale barequals 5 cm.

FIGURE 2. Skull of cingulates in dorsal view: 1- Chae-tophractus sp.; 2- Glyptodon reticulatus (MACN-Pv10153); 3- Neosclerocalyptus paskoensis (MACN-Pv18107). Scale bar equals 5 cm.

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throw and the coronoid process; the zygomaticarch posseses a huge descending process thatprojects ventrally beyond the toothrow and is par-ticularly important as an origin site of the masse-teric musculature (Fariña and Vizcaíno, 2001;Vizcaíno et al., 2004).

Among glyptodonts, a particularly remarkablefeature is the expanded and globular narial region

(Figures 1.1-1.2, 3) present only among specimensassigned to Neosclerocalyptus Paula Couto, 1957.The degree of expansion of the narial region is somarked that the orbits are directed almost entirelylaterally, and probably precluded the animal’scapacity for frontal vision.

Studies on the skull anatomy of glyptodontsare scarce, and those on the morphology of the

FIGURE 3. Skulls of Neosclerocalyptus in lateral view (nasal region to the left), showing different morphotypes: 1-Neosclerocalyptus paskoensis (MLP 16-384); 2- Neosclerocalyptus pseudornatus (MACN-Pv 8579); 3- Neosclero-calyptus paskoensis (MACN-Pv 18107); 4- Nesoclerocalyptus sp. (MACN-Pv 8091); 5- Neosclerocalyptus ornatus(MLP 16-28); 6- Neosclerocalyptus pseudornatus (MACN-Pv 8773). Scale bar equals 5 cm.


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nasal cavity even more so. Among them, we maynote the descriptions of Huxley (1864) on Glypt-odon Owen, 1839; Burmeister (1870-1874) onGlyptodon, Panochthus Burmeister, 1866, andNeosclerocalyptus; Scott (1903) on Propalaehoplo-phorus Ameghino, 1887, and Cochlops Ameghino1889; and Gillete and Ray (1981) on GlyptotheriumOsborn, 1903. Huxley (1864) provided a briefdescription of the posterior part of the nasal cavity.Burmeister (1870-1874) published a detaileddescription of the nasal cavity of Glyptodon basedon at least two longitudinally and transversely sec-tioned skulls and considered also the skulls of Neo-sclerocalyptus and Panochthus, in which thepresence of frontal and parietal sinuses were veri-fied. Huxley (1864) and Burmeister (1870-1874)recognized in Glyptodon the presence of frontalsinuses communicating with the nasal cavity. Bur-meister (1870-1874) also identified the presence ofseveral chambers in the skull roof of Neoscleoca-lyptus and Panochthus (although not illustrated inthe latter) that he recognized as sinuses, butbecause of the fragmentary nature of the specimenhe did not provide functional or other interpreta-tions. Despite this singular morphology, this subjectwas completely abandoned as a course of studyduring the 20th century. Recently, Zurita and collab-orators revisited the topic of the nasal morphologyof Neosclerocalyptus and attempted to explain itsbiological meaning (Zurita, 2002; Zurita et al.,2005, 2008, 2009, 2011). Based on their work andBurmeister’s (1870-1874) descriptions, theseauthors interpreted the most anterior part of thenarial bony expansion as sinuses within the nasalbone and its morphologic variation (Figure 3) asreflecting specific differences among the four spe-cies recognized by Zurita et al. (2011): N. pseudor-natus (Ameghino, 1889), N. ornatus (Owen, 1845),N. gouldi Zurita et al., 2008, and N. paskoensis(Zurita, 2002). Conversely, preliminary studies byFernicola et al. (2007), Toledo et al. (2007), andFernicola et al. (2010) interpreted the most anteriorpart of the narial bony expansions in Neoscleroca-lyptus as the result of ossification of the nasal carti-lages. The form of the external surface of theossified nasal cartilage allows recognition of twomain morphotypes: one a single globular structureand the other with at least two protuberances sepa-rated by grooves.

From the phylogenetic perspective, Zurita etal. (2011) suggested that narial ossification,despite the morphologic variation and the differentinterpretations on the anatomical parts involved, isa possible synapomorphy uniting the four species

in a single clade, currently considered as Neoscle-rocalyptus. This genus was considered by Ferni-cola (2008), Porpino et al. (2010), and Fernicolaand Porpino (2012) as the sister taxon of Hoplo-phorus Lund, 1839 plus Panochthus (Figure 4).

Zurita et al. (2011) also made some ecologicalassessments, suggesting a correlation betweenthe degree of pneumatization of the skull and thecold arid Pleistocene cycles of South America(Clapperton, 1993).

The different interpretations of the anatomicalparts of the narial expansions of Neosclerocalyptusindicate that more detailed research on the anat-omy of the nasal cavity is needed. On this basisand proceeding along similar studies performed onliving mammals by Witmer et al. (1999) and Cliffordand Witmer (2004a, 2004b), we undertake exten-sive comparative anatomical analyses of the nasalcavity of the skulls of Neosclerocalyptus, as well asother glyptodont genera (Glyptodon, Panochthusand Doedicurus Burmeister, 1874), and evaluateits paleobiological significance. As specimensbelonging to N. paskoensis are the best preserved,we initiate the series of planned contributions byproviding a detailed anatomical description of theskull roof and nasal cavity of this species and dis-cussing its functional implications.

MATERIAL AND METHODS

Materials

Institutional acronyms. AGM: Archivo Gráfico yMuseo Histórico de la Ciudad de San Francisco yalrededores, Córdoba Province, Argentina; MCA:Museo de Ciencias Naturales “Carlos Ameghino”,Mercedes, Buenos Aires Province, Argentina;MLP: Museo de La Plata, La Plata, Buenos AiresProvince, Argentina; MACN-Pv: Colección Nacio-nal de Paleontología de Vertebrados del MuseoArgentino de Ciencias Naturales “BernardinoRivadavia”, Ciudad Autónoma de Buenos Aires,Argentina.

Neosclerocalyptus gouldi

MCA 2010. Skull and cephalic shield, humerus andfragmentary dorsal carapace. Horizon: BuenosAires Formation / Bonaerian Stage (Zurita et al.,2009). Locality: San Andrés de Giles, BuenosAires Province, Argentina.

Neosclerocalyptus ornatus

AGM 006. Partial skull, fragment of dorsal cara-pace, vertebrae and scapula. Horizon: Level 2 /Ensenadan Stage (Cruz et al., in press). Locality:


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Cava de Carobolante, San Francisco, CórdobaProvince, Argentina.

MLP 16-28. Complete skeleton. Horizon: MiramarFormation / Ensenadan Stage (Zurita et al., 2009).Locality: Mar del Plata, Buenos Aires Province,Argentina.

Neosclerocalyptus paskoensis

MLP 16-384. Skull and mandible. Horizon:Unknown. Locality: Unknown.

MACN-Pv 18107. Skull, mandible, fragment of dor-sal carapace, cephalic shield, forelimbs and hindlimbs. Horizon: Unknown. Locality: Carhué, Bue-nos Aires Province.

Neosclerocalyptus pseudornatus

MACN-Pv 8579. Skull without the most anteriorpart of the ossified nasal cartilages and mandible.Horizon: “Toscas del Río de La Plata” / EnsenadanStage. Locality: Río de La Plata, Olivos, BuenosAires Province, Argentina.

MACN-Pv 8773. Skull without the most anteriorpart of the nasal cavity, cephalic shield and frag-ment of dorsal carapace. Horizon: “Toscas del Ríode La Plata” / Ensenadan Stage. Locality: Río deLa Plata, Olivos, Buenos Aires Province, Argen-tina.

Neosclerocalyptus sp.

MACN-Pv 15151. Skull. Horizon: Unknown. Local-ity: Unknown.

MACN-Pv 8091. Skull. Horizon: Miramar Forma-tion / Ensenadan Stage (Zurita et al., 2011). Local-ity: Mar del Plata, Buenos Aires Province,Argentina. Zurita et al. (2011) considered this fossilas a deformed specimen of N. ornatus. However,the bilaterally symmetric position of the anatomicalelements indicates that it is not a heavily distortedspecimen (Figure 1.2).

Methods

For the purposes of this work, we describemainly the skull roof and the osseous elements that

FIGURE 4. Cladogram depicting phylogenetic hypothesis used in this work. Modified from Fernicola (2008), Porpinoet al. (2010), and Fernicola and Porpino (2012).


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contribute to the formation of the nasal cavity of N.paskoensis. In doing so, we first analyze the skullmorphology of different Pleistocene glyptodonts:Glyptodon, Panochthus and Doedicurus and theother specimens of Neosclerocalyptus. The exter-nal cranial anatomical terminology used herein foradult individual follows Gillete and Ray (1981) andWible and Gaudin (2004), who described the skullof the glyptodont Glyptotherium and the armadilloEuphractus sexcinctus (Linnaeus, 1758), respec-tively. For recognition of paranasal sinuses we fol-low the terminology provided by Farke (2010). Thisauthor considered a sinus as an air-filled cavitywithin the bone, generated by the removal of tra-becular bone by the activity of soft tissues of thenasal cavity. Therefore, this space is positionedbetween two layers of cortical bone. In contrast, arecess is a concavity of the surface of the bone.With respect to the identification of features of thenasal cavity, we follow Reinbach (1952a, 1952b,1955), Wegner (1960) and Zeller et al. (1993) (see“Discussion”).

To evaluate the internal anatomical structuresof the nasal cavity, MACN-Pv 18107 was subjectedto X-ray computered tomographic (CT) scanning atthe Hospital “Dr. Diego Paroissien” in La Matanza,Buenos Aires, Argentina. Slice thickness forMACN-Pv 18107 was 1 mm. CT scanning providedgood resolution between bone and rock matrix.

RESULTS

Skull Roof and Nasal Cavity Morphology of Neosclerocalyptus paskoensis

In contrast to the condition in most adult spec-imens of other glyptodonts, in which many suturesof the skull are obliterated during ontogeneticdevelopment (hindering recognition of the differentbony elements), in specimens of N. paskoensis(MACN-Pv 18107) and N. pseudornatus (MACN8579) the sutural boundaries are preserved in theadult stage, allowing recognition of bone limits.This peculiar condition allows us to delimit theextension of the supraoccipital, parietal, frontal andnasal bones, as well as a fifth osseous element,the posterior border of which is overlapped dorsallyby the nasal bones (Figure 2.3). The premaxillaeand maxillae overlap this fifth element ventrally andlaterally. The walls of this latter element are com-posed of external and internal compact layers anda middle trabecular layer. As described later, thisossification housed the maxilla maxilloturbinatesand atrioturbinates. We interpret this fifth elementas an independent bone formed by the ossification

of the nasal cartilages. This structure is not anexceptionally preserved artifact of taphonomic pro-cesses, but a bony element formed during the ani-mal’s life. In order to avoid the introduction of anew term for this element, we will refer to it as“ossified nasal cartilages” throughout the text.

Skull in Dorsal View (Figure 2)

Supraoccipital. In dorsal view this bone is repre-sented by a narrow, transverse surface of approxi-mately 10 mm width. Anteriorly it contacts both theparietals bones along a V-shaped suture, while lat-erally it contacts the mastoid exposure of the parscanalicularis of the petrosal bone.

Parietals. In dorsal view each parietal is Γ-shaped(Greek uppercase letter gamma). Laterally, its pos-terior narrow transverse arm contacts posteriorlythe mastoid surface of the pars canalicularis of thepetrosal bone and anteriorly it does the same withthe posterior edge of the squamosal bone, bothalong straight sutures. Medially, the broad longitu-dinal arm contacts the contralateral parietal and lat-erally the medial edge of the squamosal, bothalong straight sutures, whereas its anterior edgecontacts the frontal along an anteriorly convexsuture. Most of the sutures are more or less hori-zontal, but those with the squamosal and petrosalare at right angles, as these bones are restricted tothe side wall of the skull. Internally, each parietalbone contains a large parietal sinus, which is con-tinuous with both the squamosal and frontalsinuses (see below).

Frontals. In dorsal view each frontal is rectangular,with the long axis oriented transversely. The short,medial margin contacts the contralateral frontal,and, similarly to the parietal, its lateral margin con-tacts the squamosal. Anterolaterally, the frontalcontacts the lacrimal along a short, straight suture,while anteriorly it does the same with the nasalbone, though along a long and posteriorly concavesuture. Internally, each frontal contains foursinuses, which are continuous with the sinuses ofthe parietals, squamosals and nasals (see below).

Lacrimals. In dorsal view each lacrimal is verysmall and rectangular. Posteriorly it contacts thefrontal and medially the nasal. Its anterior marginoverlaps the ossified nasal cartilages (see below).In the orbital side there is a wide lacrimal foramenand a lacrimal sinus is absent.

Nasals. In dorsal view each nasal is triangular, witha straight medial base and convex anterior andposterior edges. Medially, its longitudinal edge con-tacts the contralateral nasal. Together, the bones


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outline an oval, with the major axis transverse tothe sagital plane. Posteriorly each nasal contactsthe frontal bones and laterally a lacrimal. Anteriorly,the nasals overlap the ossified nasal cartilages(Figures 5, 6). Each nasal contains three sinuses,of which one appears to be independent whereasthe other two sinuses are continuous with the fron-tal sinuses (see below).

Ossified nasal cartilages. In dorsal view this ele-ment is globular in form and represents nearly onequarter of total skull length. Its osseous walls, lack-ing air cavities, are formed by a trabecular middlelayer between inner and outer layers of corticalbone. Posteriorly it is overlapped by the nasals anddorsolaterally by the lacrimals. Ventrally and later-ally to these latter contacts (Figure 5), the contribu-tion of the maxillae and premaxillae could not bedetermined because their sutural contacts areobliterated. Each region of overlap is indicated by anarrow space, possibly occupied in life by connec-tive tissue. The anterior border of the ossified nasalcartilages is acute and forms the osseous dorsaland lateral rim of the fenestra narina, which isdelimited ventrally by the lamina transversalis ante-rior. Thus, the apertura piriformis is in fact the

fenestra narina. The external surface is smoothand globular, without discontinuities (such as thefenestra lateralis), allowing recognition of the pos-terior limit of the cupula nasi anterior as defined inprenatal individuals of Cingulata (Fawcett, 1919,1921; Reinbach, 1952a, 1952b, 1955; Wegner,1960; Zeller et al., 1993). The only structure thatwe could differentiate is the processus alaris supe-rior, positioned on the ventrolateral corner of theparies nasi.

Paranasal Sinuses

The paranasal sinuses (Figures 6-11), housedwithin the parietals, squamosals, frontals andnasals, are extensively interconnected by severalapertures (following Márquez et al., 2008). Consid-ered as a whole, the air space conformed delimitedby these bones roughly resembles an invertedtruncated pyramid. Topographically, it may beinferred that the anterior plane of this pyramid, con-tiguous with the posterior portion of the ossifiednasal cartilages, would be formed entirely by thenasals. The ventral plane, in fact the roof of thenasopharyngeal duct, is formed by the internal cor-tical layer of the nasals and frontals. The posteriorplane, coinciding with the roof of the ethmoid

FIGURE 5. Skull of Neosclerocalyptus paskoensis (MACN-Pv 18107) depicting ossified nasal cartilages conformingthe rostral most region (light orange) and turbinates (red).


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FIGURE 6. Neosclerocalyptus paskoensis (MACN-Pv 18107). Parasagittal CT slice (above) and diagram depictingstructures explained in the text (below). Scale bar equals 5 cm.


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chamber and braincase and adjoining the anteriorwall of occipitals, is formed by the internal corticallayer of the frontals and parietals. Laterally, the pyr-amid is formed by the internal layer of the lacri-mals, frontals and squamosals. The internalcortical layer of the squamosal delimits the cranialcavity laterally. Finally, the dorsal plane of the pyra-mid is formed by the nasals, frontals and parietals,plus a small medial fringe of the squamosal regionof the temporal.

The median longitudinal walls of both nasals,frontals and parietals divide the paranasal sinuses(the truncated pyramid) into symmetric right andleft halves. Each half is subdivided by four mainosseous walls that delimit the anterolateral nasal,frontolateral, frontonasal and frontoparietosquamo-sal sinuses. As occurs in several mammals (e.g.,bovids, see Farke, 2010), the limits of the parana-sal sinuses and the external boundaries of the cra-nial bones do not match precisely.

FIGURE 7. Neosclerocalyptus paskoensis (MACN-Pv 18107). Frontal CT slice (above) and diagram depicting para-nasal sinuses explained in the text (below). Scale bar equals 5 cm.


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The dorsal part of the nasopharyngeal ductcontains a very dense mass of sediment: its poorresolution in the CT scans precludes recognition ofthe openings through which the paranasal sinusescommunicate with the nasopharyngeal duct.

Anterolateral nasal sinus. This kidney-shaped aircavity occupies most of the anterior and lateral por-tion of the nasal (Figures 7, 8). It is delimited dor-sally by the external cortical layer of the nasal,anteriorly by the nasal’s anterior wall (contactingthe posterior surface of the ossified nasal carti-lages), laterodorsally by the inner wall of the lacri-mal bone and lateroventrally by the lateral wall ofthe maxilla. The posterior wall is formed by ananteriorly concave septum that is 55 mm thick. Thelength of the sinus from the anterior to the posteriorwall is about 35 mm. This posterior wall extendsfrom the lateral wall of the skull to the median wallof the nasal approximately 25 mm from the skullmidline. Ventrally, about 40 mm from the skull roof

and aligned with the dorsal surface of the septotur-binates (see below), the posterior wall bendstoward the anterior wall of the nasal bone, thusclosing the anterolateral nasal sinus. However, awide aperture located on its posteromedial portioncommunicates with the frontonasal paranasalsinus.

Frontolateral sinus. This oblong air cavity ishoused within the anterior and lateral portions ofthe frontal (Figures 7, 8). Its dorsal boundary isformed by the ventral surface of the endocraniallayer of the frontal. Anteromedially and posterome-dially, the sinus is delimited by two walls that sepa-rate it, respectively, from the anterolateral nasaland the frontoparietosquamosal sinuses. About 22mm from the dorsal boundary of the frontolateralsinus, each wall is pierced by a wide aperture(approximately 14 mm in height) through which thefrontolateral sinus communicates with the frontona-sal and frontoparietosquamosal sinuses. Ventral to

FIGURE 8. Neosclerocalyptus paskoensis (MACN-Pv 18107). Block diagram depicting paranasal sinuses explainedin the text.


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these apertures the walls converge and enclosethe frontolateral sinus ventrally. The height of thesinus is approximately 45 mm.

Frontonasal sinus. This oblong shaped air cavityoccupies about two thirds of the inner space of thenasal and one quarter of the frontal bones (Figures7, 8). Its anterior surface rests on the posterior wall

of the ossified nasal cartilages, whereas its poste-rior surface is constituted by the anterior wall of thefrontoparietosquamosal sinus. It is delimited medi-ally by the longitudinal median wall and laterally bythe medial wall of the anterolateral nasal and fron-tolateral sinuses. Its ventral boundary is formed bythe roof of the nasopharyngeal duct. From between

FIGURE 9. Neosclerocalyptus paskoensis (MACN-Pv 18107). Transverse CT slice (above) and diagram depictingstructures explained in the text (below). Scale bar equals 5 cm.


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approximately 22 to 46 mm ventral to the skull roof,an extensive, though incomplete dorsally convex,partition is developed and extends horizontallyacross the sinus between the median longitudinalwall and the medial walls of the anterolateral nasal

and frontolateral sinuses. This partition subdividesthis sinus into dorsal and ventral intercommuni-cated vaults.

Frontoparietosquamosal sinus. This air cavityoccupies the dorsal third of the posterior half of the

FIGURE 10. Neosclerocalyptus paskoensis (MACN-Pv 18107). Frontal CT slice (above) and diagram depicting struc-tures explained in the text (below). Scale bar equals 5 cm.


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frontal, and the entire parietal and squamosal (Fig-ures 7, 8). It is delimited dorsally by the ventral sur-face of the external cortical layer of these threebones. Its lateral boundary is the inner surface ofthe external wall of squamosal. It is separatedanteriorly from the frontonasal sinus by an osseouswall, although an aperture is present ventrallybetween these sinuses. The posterior surface ofthis wall bears a globular, open chamber. The sinusis limited posteriorly by the inner layer of the pari-etal, the roof of the braincase and of the ethmoidchamber. Internally, a parasagital partition that iscontinuous dorsally with the parietosquamosalsuture and extends ventrally and obliquely to reachthe roof of the braincase. The partition separatesthe sinus into parietal and squamosal portions,which extend anteriorly into the frontal portion ofthis sinus.

Nasal Cavity

Anterior portion. This portion is formed entirely bythe ossification of the anterior part of the nasal car-tilages (Figure 5), which form an anteroturbinatechamber. The absence of the fenestra lateralis pre-vents recognition of the posterolateral limits of thecupula nasi anterior. Thus, we describe, among theossified nasal cartilages, the tectum nasi, solum

nasi and paries nasi, and the processus alarissuperior, positioned on the ventrolateral corner ofthe paries nasi. The apertura nasi externa islocated between the processus and the cupulanasi anterior (Figure 5) (Göbbel, 2000 and refer-ences therein).

Ossified tectum nasi. The roof of the nasal cap-sule or tectum nasi (Figure 5) is convex in form andexhibits a deep groove along the midline that Faw-cett (1919) termed the sulcus dorsalis nasi (= sul-cus supraseptalis of Reinbach, 1952a, 1952b,1955; Wegner, 1960). Dorsally, this groove sepa-rates the ossified nasal cartilages into symmetricleft and right halves and extends about 15 mmanteroventrally, reaching the dorsal border of theossified septum nasi. On the surface of the tectumnasi, approximately 40 mm from the sulcus, lies anobliquely oriented depression that is 25 mm inlength and 10 mm in width. The anterior margin ofthe depression is about 25 mm from the anteriorborder of the ossified nasal cartilages, while itsposterior margin reaches the anterior border of thenasal (Figure 5). The depression demarcates theposition of an internal air space positionedbetween two posterior partitions of the maxillo-atri-oturbinates (see below), but it is not possible to dis-cern the presence of an internal partition in this

FIGURE 11. Neosclerocalyptus paskoensis (MACN-Pv 18107). Block diagram depicting nasal meatuses explainedin the text.


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space. A narrow space for air circulation is presentbetween the inner surface of the tectum nasi andthe maxillo-atrioturbinate. The boundary betweentectum and paries nasi is indistinguishable. Wethus consider, for descriptive purposes, the above-mentioned depression as the limit between them. Anotable feature is the absence of nasoturbinates,scroll-like bony structures that hang from the roofof the nasal cavity in most mammals, includingother glyptodont genera (Gaudin and Wible, 2006;Gavrilov, 1959).

Ossified paries nasi. This corresponds to the lat-eral wall of the nasal (Figure 5). Its external surfaceis convex and bears on its ventroanteromedial cor-ner a projection that plausibly represents a proces-sus alaris superior, as defined by Göbbel (2000).This laminar process is triangular in form; its ven-tral half is directed upwards and extends dorsally,and its dorsal end extends toward the septum nasi.Its most distal border is about 5 mm from the sep-tum nasi. The process almost completely dividesthe fenestra narina into dorsal and ventral portions,the functional interpretation of which is discussedin the next section. The inner surface of the pariesnasi bears an extended osseous lamina that rep-resents the anchorage of the maxilloturbinate. Thisturbinate is continuous medially with the atrioturbi-nate (see below), forming the maxillo-atrioturbi-nates and occupying almost the anterior part of thenasal capsule (Figures 5-11). The dorsolaterallysituated maxillo-atrioturbinates and the posteriorlysituated ethmoturbinates (see below) are sepa-rated by a gap of 55 mm.

Ossified solum nasi. The solum nasi, forming oneach side the primary floor of the anterior region ofthe nasal capsule, is formed by a horizontal laminaextending laterally from the ventral border of theosseous septum nasi. The lateral end of the laminabends dorsally to meet the paries nasi, formingthere the osseous root of the atrioturbinate. Thislamina possibly represents the processus lateralisventralis and the lamina transversalis anterior ofprenatal armadillos. According to Fawcett (1919,1921), Reinbach (1952a, 1952b, 1955), Wegner(1960) and Zeller et al. (1993) the lamina transver-salis anterior is united with the ventral border of theparies nasi and, at this contact, with the base ofatrioturbinate.

Ossified septum nasi. The ossified nasal capsuleis subdivided into right and left chambers by theseptum nasi (Figure 5). In anterior view, the sep-tum nasi is triangular, with its dorsal third groovedby a narrow depression (sulcus dorsalis: see Tec-

tum nasi, above). Its ventral two thirds exhibit arough surface, which served for attachment of thecartilaginous anterior part of the septum nasi. Theseptum rest on the vomer, but these elements arecompletely fused. As described for Zaedyus pichiy(Desmarest, 1804) and Dasypus novemcinctusLinnaeus, 1758 (Fawcett, 1919; Reinbach, 1955;Wegner, 1960), two lateral expansions are discern-ible from the middle portion of the septum that rep-resent the septoturbinates (Figures 6, 9, 10).These turbinates are medially and slightly posteri-orly disposed with respect to the maxillo-atrioturbi-nates and are separated from the ethmoturbinatesby a gap of 50 mm. The surface of the anteriormargins of the ossified septum nasi and processusalaris superior is rough, suggesting that a consider-able amount of soft tissues (connective and mus-cular) arose from these areas and formed thefleshy nostrils and the upper lip.

Nasal meatuses. The nasal meatuses (Figure 11)are air-flow passages within the nasal cavity(Evans, 1993). The meatus nasi dorsalis is locatedbetween the ventral surface of the ossified tectumnasi and the dorsal surface of the maxillo-atriotur-binates. This meatus is continuous laterally withthe meatus nasi lateralis that is located betweenthe lateral surface of the maxillo-atrioturbinatesand the ossified paries nasi. This lateral air spaceis continuous with the meatus nasi ventralis, whichis located between the ventral surface of the max-illo-atrioturbinates and the nasal cavity floor (dorsalsurface of the hard palate). The meatus nasi dorsa-lis and ventralis are continuous with the meatusnasi communis, which is positioned between theossified septum nasi and the medial-most surfaceof the maxillo-atrioturbinates. Finally, the meatuscommunis empties into the nasopharyngeal duct(see below).

Posterior portion. The posterior portion of thenasal cavity is delimited dorsally by the ventral sur-faces of the nasals and frontals, anteriorly by theposteroventral border of the septoturbinates, pos-teriorly by the anterior surface of the cribriformplate, and ventrally and laterally by the palatineand maxillary (Figures 6, 10). The participation ofthe horizontal processes of the palatines to thefloor of the nasal cavity could not be determinedbecause the sutural contact with the maxilla isobliterated. Moreover, Gillette and Ray (1981)mentioned that this process is absent in the glypt-odont Glyptotherium. Internally, the posterior nasalcavity is partitioned into an undivided anterior half,whereas the posterior half is divided by the pneu-matized horizontal lamina transversalis. The latter


15

forms the floor of the ethmoturbinal chamber andthe roof of the posterior part of the nasopharyngealduct that bears in its medial line two continuousgrooves separated by a low septum. The fan-shaped ethmoturbinates are continuous with thecribriform plate. This latter shows on the middleline of its encephalic surface a prominent andanterodorsally-posteroventrally sloped crista galli.

DISCUSSION

Ossified Nasal Cartilages

Despite the variation observed in the morphol-ogy of the ossified nasal cartilages among the dif-ferent species assigned to Neosclerocalyptus(Figure 3), the presence of this structure in theadult stage is a feature not known for any otherglyptodont, and not described for any extant terres-trial mammal.

The ossified nasal cartilages have been inter-preted by Zurita (2002) and Zurita et al. (2005,2008, 2009, 2011) as the most anterior part of thefronto-nasal sinuses system, and the entire systemof paranasal sinuses was described as an autapo-morphy of the genus. However, the clear osseousdiscontinuity between the most anterior portion ofthe narial region and the nasals, premaxillae andmaxillae, and the triple nature of the osseous wallsof this anterior narial region (a trabecular layerbetween two cortical layers), allows it to be consid-ered as the independent ossification of the anteriorportion of the nasal capsule. As mentioned above,the shape of the external surface of the ossifiednasal cartilages allows recognition of two morpho-types: I, a single globular structure, and II, a globu-lar structure with at least two protuberancesseparated by grooves. Among the species recog-nized by Zurita et al. (2011) the first morphotype ispresent in those specimens assigned to N. ornatus(MLP 16-28, AGM 006), N. gouldi (MCA 2010) andN. paskoensis (MLP 16-384, MACN-Pv 18107) andthe second morphotype in specimens assigned toN. pseudornatus (MACN-Pv 8579) and Neosclero-calyptus sp. (MACN-Pv 8091).

Regarding the fact that the nasal capsule ofextant cingulates remains cartilaginous at the adultstage (Starck, 1967; Wegner, 1922), the ossifica-tion of the nasal cartilages in Neosclerocalyptuswould represent a neomorphic feature produced bya terminal addition of an ossified stage via per-amorphosis (sensu Alberch et al., 1979). However,the absence of a fenestra lateralis in N. paskoensisdoes not allow us to assert that it is exclusively aterminal addition. Indeed, the absence of this fea-

ture could be explained by two developmentalhypotheses: 1) the nasal capsule of N. paskoensisdeveloped as in modern cingulates, forming afenestra lateralis, and this fenestra was obliteratedduring the process of ossification, and 2) the nasalcapsule of N. paskoensis retained the condition ofan earlier embryonic stage, prior to the formation ofthe fenestra lateralis, and this feature of the foetalnasal capsule in the adult was preserved by thesubsequent ossification. The first hypothesis wouldcorroborate the ossified condition as a terminaladdition, whereas the second would imply anotherheterochronic process (paedomorphosis) in addi-tion to the neomorphic ossification. Either of thesetwo hypotheses requires an ontogenetic series tobe tested.

The Processus Alaris of the Nasal Cartilages

One of the problems we faced during thedevelopment of this work was to establish anunequivocal nomenclature to designate differentparts of the nasal cavity. This difficulty was particu-larly marked with respect to the number and posi-tion of the processus alaris, the interpretations ofwhich vary considerably among the severalauthors who have studied the nasal region ofarmadillos.

Fuchs (1911) recognized the existence of twoprocesses located at the anterior and posterior partof the lateral border of the fenestra narina in prena-tal specimens of Dasypus novemcinctus. He couldnot decide whether these structures were homolo-gous to the processus alaris superior and inferiorobserved in the lizard Lacerta (Gaupp, 1900) andthe monotreme Echidna (Gaupp, 1908) because,in contrast to the condition in these taxa, Dasypusnovemcinctus shows the processus superior andinferior in a lower and upper position, respectively,therefore he preferred to label them as anticus andposticus (Fuchs, 1911, p. 38). Later, Fawcett(1921) named Fuchs’ cartilage alaris posticus andcartilage alaris antica as the processus alaris infe-rior and superior, respectively. This opinion was notshared by Reinbach (1952a, 1952b) and Wegner(1960), who recognized that the cartilage alarisantica of Fuchs (1911) and the processus alarissuperior of Fawcett (1921) correspond to the fold-ing of the lateral portion of the fenestra narina, andtherefore, it is not a true process. Therefore, Rein-bach (1952a, 1952b) and Wegner (1960), as wellas Zeller et al. (1993) and Göbbel (2000), consid-ered the processus alaris inferior of Fawcett as theprocessus alaris superior because it is continuouswith the paries nasi. Thus, in this and future contri-


16

butions, we follow Reinbach (1952a, 1952, 1955),Wegner (1960) and Zeller et al. (1993) with respectto the identification of prenatal structures of theanterior part of the nasal cartilage in consideringthe bony process arising from the ossified pariesnasi in N. paskoensis as the processus alaris supe-rior. This structure is also present in N. gouldi(MCA 2010), but absent in N. ornatus (MLP 16-28)and Neosclerocalyptus sp. (MACN-Pv 8091). In theremaining specimens this part of the skull is miss-ing.

Turbinates

In relation to the identification of the turbi-nates, N. paskoensis had septoturbinates butlacked nasoturbinates. This absence was associ-ated with the clear retraction of the nasal boneswith respect to the nasal aperture, and concomi-tantly with the greater separation between anteriorand posterior (ethmo) turbinates. Septoturbinateswere described in prenatal individuals of the extantarmadillo Zaedyus, but not in adults by Reinbach(1955). Wegner (1922) described osseous septo-turbinates in adult specimens of the extant Cabas-sous. Adult specimens of both armadillos have acartilaginous nasal capsule. Considering the caseof Zaedyus, the presence of septoturbinates in N.paskoensis, could be related also to heterochronicprocesses, but regarding the presence of osseousseptoturbinates in adults of Cabassous this hypoth-esis should be further explored. In any case, it isclear that retention of septoturbinates in the adultforms of both Neosclerocalyptus and Cabassous isindependent of the presence or absence of neo-morphic ossification of the nasal capsule. Theextension of these conclusions to the other speciesof the genus implies particular descriptive studiesfor each morphotype (I and II), currently in prog-ress.

Nasal Cavity of Neosclerocalyptus and Function

With regard to the function of the nasal cavity,we follow conceptualizations provided by Bock andvon Wahlert (1965) and Plotnick and Baumiller(2000), who considered function as “what a featuredoes” (including both physical and chemical emer-gent properties of its form). The four main functionsdescribed for the nasal cavity in mammals corre-spond to chemoreception, hydric and thermal regu-lation, and the passage of air to the lungs (Cravenet al., 2010).

Among extant terrestrial mammals, in the pig(Sus scrofa) the ventral and anterior end of the

septum nasi usually ossifies, forming an “os naria-lis” (Getty, 1982) of unknown function. In somespecimens of the Pleistocene sloth Megatheriumamericanum Cuvier, 1796, the septum nasi is ossi-fied along its entire length (Bargo et al., 2006, fig-ure 2.A), a pattern also present in glyptodonts suchas Glyptodon, Panochthus, and Doedicurus (Fig-ure 1.3, 1.4, 1.5, respectively). However, besidethese particular cases, the degree of ossification ofthe nasal cartilages as seen in Neosclerocalyptusspp. has no homologues among other terrestrialmammals, even among those with more bizarrenarial anatomy (Witmer et al., 1999; Clifford andWitmer 2004a, 2004b). Functional consequencesof the neomorphic ossification of the nasal capsuledescribed above are not readily predicted orinferred. Indeed, as we discuss below, the inferredfunctions of the internal structures of the nasal cav-ity are the same or similar to those of extant mam-mals. In this context, it is possible that the functionsof the ossified nasal cartilage were similar to thenasal and maxillary bones in other mammals: thatis, supporting and covering the inner structures ofthe nasal cavity (turbinates). Thus, although furtherresearch is needed, this neomorphic ossificationwould constitute a morphological novelty, but not afunctional one.

In mammals, the ethmoturbinates areinvolved in chemoreception while the maxillo- andatrioturbinates are related to thermal and hydricregulation and air passage. As mentioned above,in N. paskoensis the maxillo-atrioturbinates arewidely separated from the ethmoturbinates. Theyare housed in wide, globulose, anterior chambers(“turbinate chambers”) formed by the ossified nasalcartilages. The incurrent airflow (Figure 12) movedto surround the maxillo-atrioturbinates inside thedorsolateral meatuses before being channeled intothe nasopharyngeal duct. This pattern seems to beconcordant with those described for other mam-mals (Craven et al., 2010) and it allows us to inferthat the maxillo-atrioturbinates had the same func-tion in N. paskoensis as in other mammals: tohumidify and warm the incoming air. Outgoing air(Figure 13) also passed around the turbinates, inthis case being dehumidified. As well, the incomingand outgoing air flowed through the septoturbi-nates: if the septoturbinates also had humidifyingand warming functions, they surely would haveparticipated with the maxillo-atrioturbinates in con-ditioning the air. The expanded rostral area of themaxillo-atrioturbinates of Neosclerocalyptus sug-gest increased capabilities for air conditioningwhen compared with other coetaneous glyptodonts


17

as Glyptodon, Panochthus and Doedicurus, atleast in absence of ad hoc physiological hypothe-ses. These functional hypotheses have to beaddressed by further, specific analysis such asmorphometric approaches, to test allometric pat-terns, for instance.

Although the biological role of these functionalproperties are difficult to address, they suggest thatNeosclerocalyptus would breathe more efficientlyin coldest and/or dryer conditions than other glypt-odonts. Despite its speculative nature, the behav-ioral explanatory hypothesis that in areas where itwas sympatric with other glyptodonts Neoscleroca-lyptus expend more time grazing during momentsof the day with lower temperatures (i.e., at night ordawn), can be proposed. Increased capabilities forair conditioning can also be related to metabolicrequirements derived from higher activity patterns,e.g., a more cursorial or a more digging behavior,or a larger home-range than other glyptodonts.

The morphology of the ethmoid chamber of N.paskoensis allowed isolation of part of the airflow.Such a condition is termed macrosmatic, definedby Craven et al. (2010) as the condition where alamina transversalis of the sphenoid bone preventsmost of this air from being delivered to the lungsvia the nasopharynx, and remaining quiescent, sur-

rounding the ethmoturbinates even during the expi-ration, and optimizing chemoreception. Thus, theethmoid chamber constitutes an “olfactory recess,”which houses chemoreceptory turbinates andreceives part of the airflow. This condition is alsopresent in the modern relatives of glyptodonts, thearmadillos. Morphometric studies are needed toassess differences in olfactory capabilities of N.paskoensis in comparison with other glyptodonts.

The paranasal sinus system has severalhypothetical functions discussed largely by Witmer(1997, see references therein). These functionsinclude not only increasing area for olfaction,humidification and warming of the inspired air, butalso thermal insulation, vocal resonation, weightreduction, flotation and shock absorption, amongothers. The absence of wide fenestration allowingcommunication of the paranasal sinuses with thenasal cavity in N. paskoensis weakens the func-tional hypothesis for vocal resonation, olfaction andair conditioning. The possibility of thermal insula-tion requires more detailed research on extant cin-gulates in order to be evaluated. Farke’s (2008,2010) work on bovids and ceratopsians suggestedthat paranasal sinuses would be functionless struc-tures resulting from removal of unnecessary bone(opportunistic pneumatization). Fariña and Viz-

FIGURE 12. Neosclerocalyptus paskoensis (MACN-Pv 18107). Block diagram depicting structures explained in thetext and inferred entering airflow (light blue arrows).


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caíno (2001) addressed that the telescoping pro-cess that displaced the masticatory apparatus ofglyptodonts beneath the cranium could reduce themoment of the weight of head, compensating therelatively small space left by the dorsal carapacefor neck muscles supporting and counterbalancingthe head. In agreement with this, the extensivepneumatization of the skull roof in N. paskoensiscould help to reduce the density of the skull roof.However, more testing of the proposed functionson weight reduction in N. paskoensis is needed forfurther and more detailed studies. Zurita et al.(2011) suggested a correlation between the degreeof development of the paranasal sinus system inNeosclerocalyptus and the cold arid Pleistocenecycles of South America (Clapperton, 1993), butthe structures they identified as paranasal sinusesare in fact ossified nasal cartilages (see above).Nevertheless, following Witmer’s (1997) andFarke’s (2010) discussion of several of these func-tional hypotheses, it is clear that the function of theparanasal sinuses in the terrestrial vertebratesremains enigmatic, hindering making predictionsabout their biological role in the ecology of Neo-sclerocalyptus until more detailed studies are per-formed, particularly on extant cingulates.

In summary, the inferred functions of the vari-ous structures forming the nasal cavity of N.paskoensis are broadly similar to those of extantmammals: support and protection of the nasal cav-ity, conditioning of inspired and expired air, andchemoreception. However, this strict actualistic cri-terion may be of restricted use when phylogeneticaffinity is not very close or fossil lineages possessmorphologies not represented in extant species,what is clearly the case for xenarthans in generaland glyptodonts in particular. Due to the historicalcontingency of evolutionary constraint, if a lineagedevelops a phenotype that is adapted to a certainenvironmental condition, its species will not neces-sarily be identical to the current models. This cir-cumstance is particularly applicable to thosemammalian faunas that evolved in isolation inSouth America during the Cenozoic. Among them,xenarthrans show important dental, skeletal, andmuscular peculiarities that make them differ greatlyfrom other mammals (Vizcaíno and De Iuliis, 2003;Vizcaíno et al., 2004; Vizcaíno et al., 2008).

CONCLUDING REMARKS

The skull of Neosclerocalyptus (and particu-larly the species N. paskoensis) described herepossesses a markedly different nasal cavity com-

FIGURE 13. Neosclerocalyptus paskoensis (MACN-Pv 18107). Block diagram depicting structures explained in thetext and inferred leaving airflow (light blue arrows).


19

pared to that of other glyptodont genera. Theunusual organization of the nasal cavity of N.paskoensis includes a wide separation betweenanterior (maxillo-atrio) turbinates and posterior(ethmo) turbinates, the absence of nasoturbinates,the development of a highly pneumatized skull,and the independent and derived condition of ossi-fication of the nasal cartilages. The maxilla-atriotur-binates are circumscribed medially, dorsally andlaterally by the ossified anterior nasal capsule, theexternal borders of which are not covered by thenasals, premaxillae or maxillae.

The following summarizes the most importantconclusions of this study:

A detailed revision of a number of skullsassigned to different glyptodonts drew attention toseveral skulls with well-marked bony limits thatpermit the identification of previously undescribedbony elements.

The most notable differences between Neo-sclerocalyptus and the remaining glyptodonts is theexistence of an anterior ossification, which corre-sponds to the anterior portion of the cartilaginousnasal capsule. The macroscopic analysis of thiselement reveals that its structure is composed ofthree bony layers. The external and internal arecompact, and the middle layer is trabecular inaspect. Together with the clear discontinuity withthe nasals, premaxillae and maxillae, these fea-tures indicate that this element is an independent,possibly endochondral, ossification. This ossifica-tion houses the maxillo-atrioturbinals.

The shape of the external surface of the ossi-fied nasal cartilages exhibits two morphotypes: I, asingle globular structure, and II, a globular struc-ture with at least two protuberances separated bygrooves.

Marked pneumatization is present in almostall cranial bones, which modifies to a great extentthe internal structure of the nasal cavity. However,the function of these inner air cavities remainsenigmatic, although it could be related to weightreduction.

Analysis of the morphology of the nasal cavitysuggests that functions of its elements were verysimilar to those described for extant terrestrialmammals. Functional hypotheses concerning theparanasal sinuses could not be assessed; theirevaluation requires further studies. A paleobiologi-cal hypothesis, albeit requiring further studies, isthat N. paskoensis could have breathed more effi-ciently than other coetaneous glyptodonts in cold-est and/or dryer conditions.

ACKNOWLEDGMENTS

We are especially grateful to R.A. Alvarez delRivero and O. Salvador of the Unidad TomografíaComputada at the Hospital Interzonal de Agudosde la Matanza “Dr. Diego Pairoissien” (La Matanza,Argentina) for providing access to CT facilities andassistance with CT scanning. We thank M.Reguero (MLP), and A. Kramarz (MACN) whokindly gave us access to the specimens under theircare; G. De Iuliis for valuable suggestions thatimproved the manuscript and to the two anony-mous reviewers that helped to enhance our work.This is a contribution to the grants, PICT 0143,UNLP N 647 and PIP-CONICET 1054 to Sergio F.Vizcaíno and UNLu CDD-CD 281-09 to Juan Car-los Fernicola.

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