THE ORDER Litopterna is represented in the São José de

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1 J. Paleont., 84(5), 2010, pp Copyright 2010, The Paleontological Society /10/ $03.00 DECIDUOUS PREMOLARS OF PALEOCENE LITOPTERNS OF SÃO JOSÉ DE ITABORAÍ BASIN, RIO DE JANEIRO, BRASIL LÍLIAN PAGLARELLI BERGQVIST Avenida Athos da Silveira Ramos, 274, bloco G, Centro de Ciências Matemáticas e da Natureza, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brasil, ,,bergqvist@geologia.ufrj.br. ABSTRACT The order Litopterna is represented in the São José de Itaboraí basin by four species belonging to the families Protolipternidae (Protolipterna ellipsodontoides, Miguelsoria parayirunhor and Asmithwoodwardia scotti) and Proterotheriidae (Paranisolambda prodromus). Only the deciduous teeth of P. prodromus are known so far. Isolated milk premolars are described for P. ellipsodontoides and M. parayirunhor. The known specimens assigned to P. prodromus are redescribed. No milk teeth are known for A. scotti. The upper and lower milk teeth of Protolipternidae, especially dp3, are more molarized than their successors, resembling, in several features later Proterotheriidae. They provide new support for the placement of this family within the order Litopterna. The analysis of the wear level of dp2 4/dP2 4 and X-ray images of the lower jaw of P. prodromus suggests that the second teeth of the premolar series, in upper and lower jaw, are retained milk premolars. Some information on tooth replacement pattern of P. ellipsodontoides and P. prodromus are also provided. INTRODUCTION THE ORDER Litopterna is represented in the São José de Itaboraí basin by four species belonging to the families Protolipternidae (Protolipterna ellipsodontoides Cifelli, 1983a; Miguelsoria parayirunhor (Paula-Couto, 1952a) and Asmithwoodwardia scotti Paula-Couto, 1952a) and Proterotheriidae (Paranisolambda prodromus (Paula-Couto, 1952a)). The first family contains the smallest litopterns, with a generally primitive (bunodont) dentition and advanced postcranial structure, typical of derived litopterns (Cifelli, 1983a, 1983b; Bergqvist, 1996, 2005). The placement of A. scotti in this order, in spite of the absence of postcrania, followed Cifelli (1983b). However, recently recovered postcranial bones from the locality Paso del Sapo, Argentina, where teeth of Asmithwoodwardia subtrigona Ameghino, 1901 are very common, suggest that this species also had litoptern tarsals (J. Gelfo personal commun., 2006). The most primitive taxa with a typically litoptern dentition are placed in the family Proterotheriidae. Soria (2001) proposed a new family, Anisolambdidae, to group the Paleocene and Eocene taxa originally placed in the family Proterotheriidae. However, his proposition is not supported by any phylogenetical analysis, and for this reason, not followed here. The Protolipternidae are far more common in the basin than Proterotheriidae but deciduous teeth (few specimens, with upper and lower milk dentition in loci) are only known for P. prodromus (Paula-Couto, 1952a). Deciduous dentitions are also known for the Astrapotheria Tetragonostylops apthomasi (Price and Paula-Couto, 1950). The lower ones were described by Paula-Couto (1952a), and the upper by Bergqvist and Moreira (2002), who also presented several non-destructive criteria for recognizing isolated deciduous dentition. Paula-Couto described all Itaboraí ungulates in a series of contributions (e.g., 1952a, 1952b, 1963, 1970), but all the species were based on the best-preserved specimens only in spite of the presence of thousands of isolated teeth and maxilary/mandibulary fragments in the collection of Departamento Nacional da Produção Mineral and Museu Nacional. A large amount of dark-colored fossils, collected in 1968 from a single fissure, enriched the Itaboraí fossil collection of DNPM, but none of these fossils have ever been studied by 858 Paula-Couto. Cifelli (1983b) recognized a new species, Protolipterna ellipsodontoides, among the fossils collected in In contrast to what generally happens with other ungulate species of the Itaboraí basin, this one turned out to be preserved only in this fissure, in which all fossils bear a dark or light brown color. No fossil recovered outside this fissure exhibits a dark color; all are light colored (white to ocre; Bergqvist et al., 2009). The São José de Itaboraí Basin is a small graben adjacent to a transcurrent fault. It is one of the smallest basins in Brazil and the only one to preserve continental fossils of Paleocene age in this country. It is located in São José, a district of the town of Itaboraí, Rio de Janeiro state. Based on its faunal composition, it has been regarded of Paleocene (Itaborarian) age (Medeiros and Bergqvist, 1999), but Gelfo et al. (2009) propose an earlier age (Lower Eocene) for Itaboraian SALMA. The fossils derive from predominantly argillaceous marls, which fill fissures in a limestone, the Itaboraí Formation. Medeiros and Bergqvist (1999) provide more geological information for this area. In this paper the upper and lower milk dentition of Protolipternidae is described. The fossils were discovered after a careful review of isolated and fragmentary fossils recovered from the Itaboraí basin. A review of Proterotheriidae milk teeth is also furnished. MATERIAL AND METHODS Abbreviations used in the text. DGM: Divisão de Geologia e Mineralogia, DNPM, Rio de Janeiro, fossil mammal collection; DNPM: Departamento Nacional da Produção Mineral, Rio de Janeiro, Brazil; MCT: Museu de Ciência da Terra, Rio de Janeiro, fossil mammal collection (replaced the abreviation DGM in the 1990s decade); UFRJ-DGM: Universidade Federal do Rio de Janeiro, Departamento de Geologia, fossil mammal collection. Material. All the specimens were recovered from fissure fill deposits. The teeth of Miguelsoria parayirunhor and Paranisolambda prodromus were found in different fissures around the basin, but all specimens of Protolipterna ellipsodontoides came from the same fissure (known as 1968 fissure ), in which all fossils are brownish. Deciduous teeth are commonly found isolated, because they were either shed in

2 BERGQVIST DECIDUOUS TEETH OF ITABORAÍ BASIN LITOPTERN 859 the course of maturation or lost after the death of an immature individual (West, 1971). Among the Protolipternidae, only the deciduous p4 of Protolipterna ellipsodontoides was found in locus, associated with m1 (MCT 1600M), but in some cases, deciduous teeth were found in loci alone (MCT 1237M, 1255M, 1447M, 1577M, 2129M). However, due to their frequency, morphology and size, they could be unambiguously assigned to P. ellipsodontoides (the smaller and dark ones) or Miguelsoria parayirunhor (the larger and lighter ones). Apparently, no deciduous teeth of Asmithwoodwardia scotti are present in the sample, a very rare species in the basin (see Paula-Couto, 1952a; Bergqvist, 1996). New isolated upper and lower deciduous teeth of Proterotheriidae were added to the previously known material (Paula-Couto, 1952a). All litoptern milk dentition is low crowned. With the exception of the specimens assigned to P. ellipsodontoides, in which both permanent and milk teeth are brownish, in M. parayirunhor and P. prodromus the milk teeth are lighter colored than the permanent ones. The deciduous premolars of both Protolipternidae species present a similar structure, as it is true for permanent ones. Besides the color of the fossils and the size (the deciduous teeth of M. parayirunhor are slightly larger), they were assigned to each of the Protolipternidae species on the basis of the following feature: in P. ellipsodontoides the cusps are gracile and slender, while in M. parayirunhor they are somewhat more inflated. In contrast to what generally happens in milk dentition (see West, 1971), the majority of the milk teeth recovered in Itaboraí basin bear little or no wear. The criteria employed here to determine the wear level was based on comparisons of the development of the tooth wear facets in occlusal view. It is generally known that older animals bear well-developed wear facets, while in younger individuals these facets are less developed (Tuen et al., 1999). Although the development of the wear facets is influenced by diet and tooth structure (Fortelius and Solounias, 2000), I designated wear categories for this analysis based solely on morphology, and independent of consideration of diet or absolute differences in numerical age. I interpreted these categories to represent only generalized relative ages. Five wear stages were proposed for both bunodont and bunolophont teeth, based on lower dp4. They grade from no wear (stage 1) to cuspids completely worn out (stage 5). For bunodont teeth, the three intermediate wear stages are: little wear (stage 2), when only the tips of the cuspids bear wear facets; intermediate wear (stage 3), when the wear facets are larger although still rounded, but starting to extend over the crests/cristids; and heavy wear (stage 4), when the wear facets extend over crests/cristids and became continuous between cusps/cuspids. The wear levels of bunolophodont teeth are related to the development of the cristids. Little wear (stage 2) is defined here as when the tips of the cuspids are already worn but minute wear is present on the cristids of the trigonid and even on the cristid oblique; intermediate wear (stage 3), when both trigonid and talonid cristids bear some wear, but paraconid and entoconulid are independent; and heavy wear (stage 4), when the cristids are deeply worn out and joined the paraconid and entoconid; the wear over cristid oblique reaches the tip of metaconid. For assessing the percentage of tooth wear in each of the species considered here, the minimal number of individuals (MNI) was first calculated. Based on left dp4, at least twentytwo individuals of P. ellipsodontoides were preserved in the basin, and among them, 27.3% bear no wear facets (stage 1) and none is totally worn out (stage 5). Among the other stages of wear level, 45.5% belong to stage 2, 13.6% to stage 3 and 13.6% to stage 4. The MNI of right and left dp4 of M. parayrunhor (3/3) and P. prodromus (5/6) are about the same and less significant than in P. ellipsodontoides, and for this reason I considered both teeth in assessing the percentage of tooth wear levels. The stages 1 and 5 are not present in both species. Based on right dp4, the percentage of wear levels are 66.6% for stage 2 and 33.4% for stage 3 in Miguelsoria. When considering left dp4, the percentage for stages 2 and 3 are reversed. In Paranisolambda, on the basis of right dp4, 60% of the teeth belong to stage 2 and 40% to stage 3. When considering left dp4, the teeth seemed to belong to little older individuals, as stage 4 is present and represents 16.7% of the individuals. Stage 2 represents 33.3% of the amount and stage 3, 50% of the total. Shigehara (1980) noted that the eruption of the full permanent dentition may postdate sexual maturity in some recent mammals and Asher and Lehmann (2008) observed a delayed eruption of the permanent dentition in some extant afrotherians. Litopterns bear no living relatives and inference of sexual maturity in fossils is not easy (if possible). So, this analysis follows the traditional view of West (1971) and Tuen et al. (1999) in which isolated milk teeth with little or no wear belonged to individuals that died very early in life, while heavily worn teeth belonged to individuals that died later, but are still juveniles (as they still had milk teeth). The stages in between are indicative of the relative age of the animal at the time of death. The goal of this analysis was to picture the frequency of very young individuals (no wear facets) or older individuals (although still juveniles, but with cusps totally worn out) in the basin. The majority of the specimens here studied (96) belong to P. ellipsodontoides (see Appendix). It represents approximately 17% of the total tooth specimens assigned to the species. For the other two species, the percentages are: 8% for M. parayirunhor (9) and 36% for P. prodromus (37). SYSTEMATIC PALEONTOLOGY Order LITOPTERNA Ameghino, 1889 Family PROTOLIPTERNIDAE Cifelli, 1983b Genus PROTOLIPTERNA Cifelli, 1983b PROTOLIPTERNA ELLIPSODONTOIDES Cifelli, 1983b Description. The upper milk P3 (Fig. 1.1), like its permanent successor, presents a triangular outline and bears only two cusps: a larger labial cusp (paracone) and a smaller lingual one (protocone). But differently from P3, these cusps are not transversally aligned, as the protocone is more distally placed. In the permanent successor, the paracone is more bulbous, but in the milk tooth it is slightly more transversely elongated, with a sharp, mesial and distal crest that goes up to the styles. A low and oblique crest, present in some specimens, links both cusps. The parastyle and metastyle are far more developed than in P3, the former much larger and more labial than the later. Labial and distal cingula are developed. Lingual cingulum is short and weak. The upper deciduous P4 (Fig. 1.1) is subquadrangular in its occlusal view. It is very molariform, resembling M1, but is clearly distinct from it for being slightly longer than wide, and for the presence of a large parastyle, and a metastyle more prominent than in M1. All cusps are bunoid. The three main trigon cusps are about of the same height, but the paracone and metacone are less inflated than the protocone. The metacone is slightly more lingual than paracone. In occlusal

3 860 JOURNAL OF PALEONTOLOGY, V. 84, NO. 5, 2010 FIGURE 1 Upper milk dentition of Protolipterna ellipsodontoides. SEM image of: 1, left dp3 4 (MCT 1447M); 2, left dp4 (MCT 1661M); 3, left dp4 (MCT 2302M). view, parastyle, preparacrista, centrocrista, postmetacrista, and metastyle are perfectly aligned mesiodistally. The paraconule is larger than metaconule and both are closer to protocone and united to it by a low crest. According to Muizon and Cifelli (2000), a mesial position of the conules with respect to para- and metacone is typical of deciduos teeth, but in P. ellipsodontoides, it is true for the paraconule, while the metaconule can be placed at the same level or slightly distal (e.g., MCT 1580M, 1586M, 1661M). Preparaconular and postmetaconular cristae are always present, however, postparaconular and premetaconular cristae, like in permanent molars, may or may not be present. Preparaconular and postmetaconular cristae do not reach the parastyle and metastyle, as in the primitive Mioclaenidae (Muizon and Cifelli, 2000). The trigon basin is deep and smooth. The hypocone, which is part of the distal cingulum, is much smaller and more lingually placed than protocone and, in most cases, linked to protocone by its base. In some specimens (e.g., MCT 1661M, 1669M, 2226M, 2302M) both cusps are separated, and a low crest join then (Fig. 1.2). Marked mesial, labial, and distal cingula are present. A protostyle, in some cases very small (e.g., MCT 2302M; Fig. 1.3), is present in the mesial cingulum; labial cingulum is absent around paracone. Cifelli (1983b) described no permanent p2 in the original (and sole) description of P. ellipsodontoides, although they are present, isolated, in the DNPM collection, and in some mandibles not seen by this author. All deciduous teeth here studied were found isolated, but I assigned to dp2 due to: (1) their resemblance to p2, but much smaller size; (2) the presence of two roots and heavy wear. No lower p1 is known for Protolipternidae, but its presence is suggested by the single alveolus behind the canine (separated from it and from the alveolous of p2 by a diastema), in the specimen MCT 1,392gM. So, the presence of two roots excludes these specimens from being a p1. The lower dp2 (Fig. 2.1) is longer than wide, and larger in its distal half. It bears a single bulbous and inflated cusp somewhat mesially displaced. A strong crest along its distalmedian edge descends to a style, medially placed at the broad distal cingulum, which forms the heel of the tooth. A weak crest runs over its mesial-median edge, descending to a smaller and narrower cingulum at the mesial face. The dp3 (Fig. 2.2) is more molarized than p3, being proportionately longer and narrower than its successor. It bears a differentiated trigonid in the specimen MCT 1582M, while in the others no metaconid is present. A small and bunoid paraconid is placed at the mesial edge of the tooth; it is connected to protoconid by a sharp paracristid that turns lingually at its extremity, to reach the paraconid on its labial side. A small metaconid, when present, is conated and distal to the protoconid to it. A straight and sharp median ridge descends from the small and also sharp protocristid, terminating in a cusp (hypoconid) at the middle part of the heel, comparable in development with paraconid, but shorter than it. Directly lingual and labial to the main cusp there is a tiny cusp. The dp4 (Fig. 2.3) is a very molarized tooth, with complete and triangular trigonid and talonid. The tooth is longer and narrower than m1. The talonid is wider, little longer and lower than trigonid. The cusps are bunoid, but slender and gracile, and the cristae connecting them are moderately high and sharp. The protoconid is the largest cusp and the metaconid the highest, but in some specimens it is as large as protoconid. The paraconid is more developed than in molars, and is much more mesially placed, so the angle formed between paraconid, protoconid and metaconid is greater, and the trigonid is more opened lingually than on succeeding teeth. As a consequence, the paracristid is longer, obliquely oriented and broadly concave. In one specimen (MCT 1448M), the metaconid is somewhat lingual than the paraconid and is formed by two twin cusps (Fig. 2.5). An intermediate stage, in which the metaconid is mesiodistally elongated, is seen in the specimen MCT 1601M (Fig. 2.4). The well-marked cristida obliqua begins at the distolabial face of metaconid, and in contrast to molars, no cuspid (mesoconid) was observed on it. The three talonid cusps are almost equally high, being hipoconid the largest while hypoconulid is the smallest. These two are connected by the postcristid, but they are isolated from entoconid. Talonid basin is open lingually. A short and weak mesial cingula is present at the base of protoconid; a stronger distal cingulum is restricted to the side of hipoconulid. A labial cingulum is present under the ectoflexid. Genus MIGUELSORIA Cifelli, 1983b MIGUELSORIA PARAYIRUNHOR (Paula-Couto, 1952a) Description. According to Cifelli (1983b), one of the most diagnostic features distinguishing Miguelsoria from Protolipterna lies in the morphology of p4, but it is not true for lower and upper milk P4. These teeth are very similar in both taxa, but the lighter teeth (yellowish) were assigned to M.

4 BERGQVIST DECIDUOUS TEETH OF ITABORAI BASIN LITOPTERN 861 FIGURE 2 Lower milk dentition of Protolipterna ellipsodontoides. SEM image of: 1, left dp2 (MCT 1633M); 2, left dp3 (MCT 1582M); 3, left dp4 (MCT 1592M); 4, left dp4 (MCT 1601M); 5, left dp4 (MCT 1448M). Scale bar 5 500m. parayirunhor as no P. ellipsodontoides is known outside 1968 fissure (from where all dark specimens were recovered). The dp4 of M. parayirunhor (Fig. 3.1) can be differentiated from Protolipterna ellipsodontodes in a few features: it is more robust and as long as wide; the trigon cusps are arranged more obliquely to the mesiodistal axis; paracone is more labial than metacone and protocone is more aligned to paracone than in that species; the postparaconular crista is absent and the hypocone is more separate from the protocone and bears no crest uniting them. Considering that it is a variable feature in P. ellipsodontoides, and that the sample analyzed is composed of only two specimens, absence of a postparaconular crest cannot be surely asserted as a distinguishing feature. In dp4 (Figs. 3.2, 3.3), hypoconulid is clearly smaller than hypoconid and entoconid, while in P. ellipsodontoides hypoconulid is only slightly smaller than both cusps. Mesial and distal cingulids are longer and stronger than is this species. Family PROTEROTHERIIDAE Ameghino, 1885 Genus PARANISOLAMBDA Cifelli, 1983b PARANISOLAMBDA PRODROMUS (Paula-Couto, 1952a) Description. The upper and lower deciduous premolars were described by Paula-Couto (1952a). However, the discovery of new milk teeth and permanent premolars that time unknown to Paula-Couto brought new information to the original description. The deciduous premolars are redescribed here. Paula-Couto (1952a) considered the tooth at the second premolar locus, associated with third and fourth milk premolars, in both upper and lower jaws of P. prodromus, as permanent tooth. According to Luckett and Maier (1982), ontogentic series provides the best evidence for identification of deciduous or successional nature of individual teeth. However, this is impossible when dealing with fossil species lacking growth series, and external features must be used to support both stages of dental development.

5 862 JOURNAL OF PALEONTOLOGY, V. 84, NO. 5, 2010 FIGURE 3 Upper and lower milk dentition of Miguelsoria parayirunhor. SEM image of: 1, left dp4 (MCT 2132M); 2, right dp4 (MCT 2129M); 3, cracked right dp4 (MCT 2130M). One of the most typical feature of a deciduous teeth is its lighter color compared to permanent ones (Simpson, 1951; West, 1971; Bergqvist and Moreira, 2002). The teeth at the second upper and lower locus of P. prodromus present the same lighter color of dp/dp3 4. Enamel is significantly thinner in deciduous premolars than in their successors or permanent molars (Grine, 2005), and therefore, deciduous teeth present lower radiopacity than permanent ones (Bergqvist and Moreira, 2002 and references herein). This feature can be easily observed in Figure 5, where the first molar is strongly impressed in the X-ray (high radiopacity), while second premolar is almost indistinct (low radiopacity). Paula-Couto (1952a) did not take into account the above mentioned features, and ignored the wear level of the premolars. In DGM 307M, 2/3 of the occlusal face is worn out, about the same wear level as is observed in dp3 4. Considering the aforementioned features (color, radiopacity and wear), I consider the upper and lower second premolars of the specimens DGM 239M, 262M, 273M, 307M and MCT 1298M, as milk teeth. However, Figure 5 shows an intriguing situation: if the second upper and lower premolars are milk teeth, where are their successors, as is observed for dp3 4? (The observation of permanent P3 4 was compromised by fossilization and/or thickness of upper jaw, but their presence can be inferred by comparison with their occlusal counterparts in the jaw.) This condition poses four possibilities: (1) the absence of a successor is pathological for these specimens. (2) The absence of a successor is a strong support to Paula-Couto (1952a) proposal that these are permanent teeth. Ziegler (1971) suggested that litopterns (he did not mention which taxa he observed) possess a successor first premolar. If this is true, a successor for the second premolar would be expected. In a careful study of the ontogenetic development of deciduous and permanent dentition in Tarsius, Luckett and Maier (1982) observed that when primary teeth undergo an abnormal prenatal development and reabsorption, they do not erupt or become functional. If this is the case of P. prodromus, the tooth in the second alveolus would be the permanent second premolar. A figure of an eight-day-old juvenile tarsier shows the p/p2 in place at the same time as dp/p3 4. Unfortunately, the authors did not make any observation on the color of the permanent second premolar (if darker than dp/ P3 4), on the enamel thickness (if thicker than deciduous). In the case of P. prodromus, if the teeth in the second alveolus are really permanent teeth, the wear level (about the same as dp/ P3 4) would make them non-functional for most of this species life. (3) In P. prodromus there is a delay in the formation of the dp/p2 successor; nevertheless, such a long delay has never been reported in literature for fossil ungulates. Asher et al. (2009) noted that there is a delayed eruption of permanent teeth in atlantogenatans. If this is the case of P. prodromus, such delay would be regarded to just one tooth. (4) The second premolar of P. prodromus is a deciduous tooth with no successor. According to Luckett and Maier (1982), an abnormal prenatal development of a tooth can also cause a non-replacement by its successor. Although possibilities two and four are equally plausible, the enamel color and thickness favor hypothesis four, in which the second premolar of P. prodromus would be a deciduous teeth with no successor. Even though it has never been reported for any other Anisolambdinae taxa, as they are known mainly by isolated teeth (see Simpson, 1948; Soria, 2001), Van Nievelt and Smith (2005) observed that loss of teeth at various loci is common in therians, and loci that are being reduced in size and importance may possibly eliminate functional replacement as an intermediate stage on the way to full elimination of the locus. P. prodromus is one the most primitive species of Proterotheriidae, and derived species of this family do not show any tendency to premolar reduction; on the contrary, most Pliocene Proterotheriidae bear all four premolars and predecessors in the milk-series (Scott, 1910). In domestic dog, for instance, the functional tooth at the upper and lower P1 locus is usually considered to be a tooth [dp1] from the deciduous dentition that is retained with the permanent dentition. Van Nievelt and Smith (2005) listed as potential factors to explain the reduction of functional tooth replacement in mammals the loss of tooth loci, major modifications of the dentition and dental development, factors related to the particulars of life history and adaptations, functional demands during the normal replacement period, phylogenetic history, and growth. Presently it is not possible to point one of these reasons to explain the absence of second premolar replacement in P. prodromus. Upper dp2 is perfectly triangular in outline and slightly wider than long, with a low crescent lingual cusp (protocone) and a high and transversely compressed paracone. From it, a

6 BERGQVIST DECIDUOUS TEETH OF ITABORAI BASIN LITOPTERN 863 FIGURE 4 Upper and lower dentition of Paranisolambda prodromus. 1, fragment of upper jaw with left dp2 4, M1 erupting and right dp2 4 (DGM 273M); 2, incomplete right dentary with dp2 4, m1 (DGM 262M); 3, SEM image of left dp3 (MCT 1672M); and 4, right dp3 (MCT 1516M). mesial and distal crests run to strong parastyle and metastyle. No mesostyle is present. The paraconule is present as a small crest (probably preparaconular crest). There are narrow mesial and distal cingula. The upper dp3 is somewhat molariform, roughly triangular, with low, distinct, but coalescent protocone and hypocone, the first larger than the latter. Paracone and metacone are very distinct, nearly equal in size and obliquely aligned, metacone being slightly lingual to paracone. A strong parastyle, intermediate mesostyle, and small metastyle are present. Paula-Couto (1952a:369) described the conules as small and conical paraconule and metaconule. As can be observed in Figure 4, both paraconule and metaconule are reduced to oblique and thick crests, with mesiolabial-distolingual orientation. In permanent molars these crests correspond to the most developed part of paraconule and metaconule. Broad mesial and distal cingula and a slight labial one are present, as well as a small protostyle in some specimens (DGM 1248M, 1672M). The last upper milk tooth, dp4, is very similar to its successor (never described by previous authors). It is much larger than the anterior teeth, perfectly molariform, much broader than long, with well-defined protocone and hypocone but with their bases in contact. In permanent P4 a low but strong crest connects both cusps. Paraconule and metaconule are well-developed, the first with marked preparaconular crest and the later with pre and postmetaconular crest. Like molars, paracone and metacone are large, distinct and subequal in size. Parastyle is very strong and metastyle weak, mesostyle intermediately developed. Mesial and distal cingula are broad, labial cingulum is weak, but complete and lingual cingulum is absent. The deciduous p2 (Fig. 4.2) is a small and, to some degree, a cutting tooth, with much compressed trigonid, high protoconid, and a slightly smaller metaconid, connected to protoconid by a crest, which runs obliquely. No paraconid is present, but a marked paracristid. Another sharp crest runs down from the protoconid mesiolingually, limiting a deep depression with paracristid. The talonid is low, broader than long, with strong lingual declivity and a small distomedian cusp, from which a weak and depressed crest runs up to the metaconid. The lower dp3 is somewhat molariform, with complete talonid but lacking paraconid in the trigonid, as suggested by Paula-Couto (1952a). A paraconid is present in dp3 4 of Proterotheriidae, in different degrees of development (Soria, 2001), but it is absent in dp3 of Anisolambdinae. No permanent p3 is known so far, but, as the paraconid is absent in the permanent p4, it may also be absent in the permanent p3. The trigonid is slightly higher, narrower, and shorter than the talonid. Metaconid is the highest cusp of trigonid. With FIGURE 5 X-ray negative lower dentition of Paranisolambda prodromus showing the lower radiopacity of deciduous teeth in comparison with permanent teeth. 1, incomplete right dentary with dp2 4, m1 (DGM 262M); 2, incomplete left dentary with dp2 4, m1 (DGM 239M).

7 864 JOURNAL OF PALEONTOLOGY, V. 84, NO. 5, 2010 one exception (MCT 1368M), all dp3 bear a small accessory cuspule in the distal slope of metaconid, facing somewhat distally. The cristida obliqua begins at the distolabial face of metaconid, but in the specimens MCT 1516M and 1674M, it runs from this accessory cusp to hypoconid (Fig. 4.3). Talonid is broader than long, with well-developed cusps. Entoconid is separated from hypoconulid by a notch, but it is connected with hypoconid by a high postcristid. A distal crest runs from the apex of hypoconulid to the cingulum, as in permanent cheek teeth. Weak mesial and distal cingula are present. The last milk tooth, dp4, is molarized. The trigonid is broader than long, and little shorter than talonid. The trigonid basin, as in molars, is closed lingually by the high paraconid. However, differently from these teeth, the paraconid is more mesially displaced, with its apex mesial to the apex of protoconid, and consequently, more separated from metaconid than in molars. No paraconid is present in permanent p4. As in dp3, the cristid obliqua runs from the distolabial face of metaconid to hypoconid, the highest and largest cuspid of talonid. It is connected to the smaller hypoconulid by a high and somewhat concave postcristid. A notch separates hypoconulid from the conical entoconid. Paula-Couto (1952a, p. 369) described this cuspid as large conical entoconid, which attains nearly the same size as the hypoconid. Unworn teeth showed that entoconid is only little higher than hypoconulid, but more slender than this cusp. In the majority of the observed specimens, entoconid is connected to hypoconulid by a low and straight crest, but in some, no crest is present and both cuspids are separated. Mesial and distal cingula are feeble, and in some specimens, a weak labial cingulum is also present. DISCUSSION The first in observing the peculiarities of the deciduous dentition was Flower (1871, in Koenigswald, 1967), who concluded that the milk teeth of Eutheria invariably show a more primitive pattern and shape than their successors. Another important work on deciduos dentition was conducted by Leche (1907). Koenigswald (1967) challenged Flower s conclusion with a series of observation on recent primates and carnivorous. He recognized two patterns among deciduous teeth a conservative and a progressive one. In the first case, the milk teeth retain in its morphology features of the ancestral condition; on the opposite, in the progressive pattern, the milk teeth foreshadow features developed by latter forms. A good example of the conservative type is found in the lower dentition of extant Carnivora, in which the talonid of the first molar is reduced or even absent, although it is still present in the last deciduous premolar, as well as in permanent premolars of Upper Miocene forms, that retained an old and unspecialized condition. In upper dentition of carnivores and most primates, the deciduous premolars preserve a complete trigon (like in molars), no longer evident in permanent premolars of extant taxa, but present in permanent premolars of their ancestors (Koenigswald, 1967). Based on observations of teeth evolution in tapirs and horses, Koenigswald (1967) concluded that in the progressive type, the molarization process of the deciduous teeth precedes molarization of the premolars. He noticed that in the Upper Eocene tapir Lophialets Mathew and Granger, 1925, the premolars were still triangular, whereas the deciduous premolars predicted the condition finally reached in Miocene forms. The family Protolipternidae, the oldest and most primitive family of Litopterna, was placed in this order by Cifelli (1983b), based on its derived ankle morphology, regardless of its primitive bunodont dentition, which is similar to that of Didolodontidae taxa. This placement was challenged by some authors (e.g., Soria, 2001; Gelfo, 2004), but none of them considered the condition of the deciduous teeth in their appraisal. According to Koenigswald (1967), if the milk teeth of Protolipternidae are of progressive type, it will presage the condition reached by derived forms, and in this case, they will be a support to the placement of the family within the order Litopterna. However, if it is of conservative type, it will retain the condition of its most likely ancestor, the condylarths (Muizon and Cifelli, 2000), and the use of deciduous teeth in phylogeny will not be meaningful. In the lower milk dentition of the most primitive litoptern, the deciduous premolars are more molarized than their successors, and even than molars. In dp4, the trigonid presents a distinct and anteriorly placed paraconid and a welldeveloped metaconid distal to protoconid. Muizon and Cifelli (2000) interpreted this condition as primitive for the molars trigonid of ungulatomorphs; it is present in early Paleocene South American Mioclaenidae, which has been regarded by these authors as closely related to Litopterna, especially to Protolipternidae. Based on these similarities, the milk teeth of Protolipternidae can be said to be conservative. However, although similar in number of trigonid cusps, both families are clearly distinct in morphology, since in Protolipternidae the cusps are more gracile than in South American Mioclaenidae (Muizon and Cifelli, 2000) and, consequently, more separated and linked by far more distinct crests than in this family. Moreover, the level of molarization of dp4 of P. ellipsodontoides has never been achieved by any p4 of ungulatomorphs or Mioclaenidae. When compared to the morphology of dp4 and p4 of derived Litopterna, as in the Proterotheriidae Diadiaphorus Ameghino, 1887 (SALMA Santacrucian, Miocene), the dp4 of Protolipternidae could be regarded as progressive. The deciduous p4 is morphologically very close to the morphological pattern (bunolophodont) shared by more derived litopterns, having adapted first than its successor and molars, to the new condition of the order. However, the same pattern of the dp4 of Protolipternidae is also present in the dp4 of Phenacodontidae (West, 1971) and Paulacoutoia Cifelli, 1983a (undescribed), which are not related to Litopterna. Therefore, the milk p4 pattern of Protolipternidae seems to be the pattern of early Paleogene ungulates of bunodont teeth morphology. Nevertheless, this is not true for the milk p3 of P. ellipsodontoides that is more molarized than its successor. This state is distinct from the primitive (Torrejonian) Phenacodontidae Tetraclaenodon purcensis (Cope, 1881) that bears a dp3 simpler than p3 (West, 1971). It is not clear if a simpler dp3 is typical of Phenacodontidae, or if in later forms (Wasatchian Phenacodus and Ectocion), dp3 became more complex than p3, as West s (1971) images and descriptions prevent from any further conclusion. Concerning the upper dentition, a well-developed parastyle in dp4 (and a moderately developed in dp3), generally absent or reduced in their successors, is a common feature of different lineages with bunodont teeth, as Phenacodontidae (West, 1971), Leptictidae (West, 1972), and Ursidae (Soilbelzon and Carlini, 2004). According to Muizon and Cifelli (2000), in zhelestids the protocone of P4 is smaller than paracone and separated from this cusp by a distinct waist, lost in condylarths due to the better development of protocone. A

8 BERGQVIST DECIDUOUS TEETH OF ITABORAÍ BASIN LITOPTERN 865 molarized P3 P4 was never achieved by primitive ungulatomorphs or condylarths, but is typical of derived litopterns. It is not possible to claim with confidence that the deciduous teeth of Protolipternidae is of progressive type, but more detailed morphological features seems to support this condition. The paraconule and metaconule of deciduous premolars of South American Mioclaenidae are mesially placed regarding para- and metacone (Muizon and Cifelli, 2000), while in Protolipternidae the metaconule is distal to metacone, as in Proterotheriidae Litopterna. In the lower dentition of South American Mioclaenidae, the hypoconulid and entoconid are joined by a crest, while in Protolipternidae entoconid is isolated, as in later litopterns. DENTAL ERUPTION SEQUENCE Little can be said about dental eruption sequence of Itaboraí Litopterna because only few specimens preserve deciduous and/or permanent teeth associated or teeth in erupting process. However, the comparison of the wear level of deciduous and permanent teeth provide an idea of the sequence of teeth emplacement. Judging from the wear level of deciduos premolars in loci, the sequence of eruption is dp3/p3 slightly before dp4/p4 in Protolipterna ellipsodontoides. Modern ungulates display remarkable diversity in their deciduous dentition eruption sequence, but in all extant ungulate species cited by West (1971), dp/p3 erupts before dp/p4. However, this seems to be not the case of phenacondonts, in which dp/p4 is frequently heavily worn. For West (1971) it may indicate that dp/p4 was emplaced in the jaw and functioning prior to the eruption of dp/p3. Judging from the wear level present in upper and lower deciduous dp/p3 dp/p4 of the hyopsodontid Hyopsodus lepidus Matthew, 1909, it seems to be also the case of this species (Gazin, 1968). Concerning the permanent teeth, it can only be said that a non-worn p4 and a little worn m1 are already in place by the time of eruption of p3 (Fig. 6), indicating that m1erupts before p4 and this before p3, and the absence of delayed eruption (p4 erupting after m3, sensu Holroyd, 2008). Although no m3 is present associated, the rule of molar eruption in mammals is in a front to back sequence (Smith, 2000). The eruption sequence of the premolars of P. ellipsodontoides is distinct from almost all extant ungulates (Smith, 2000), in which premolars erupts in a front to back order. Phenacodonts permanent premolars also erupt in a front to back sequence, as long as the arctocyonid Loxolophus kimbetovius (Matthew, 1937) (West, 1971). According to the FIGURE 6 Mandible (MCT 1301-M) of Protolipterna ellipsodontoides showing p3 erupting. wear levels observed in the excellent illustrations of permanent p/p3 p/p4 of Hyopsodus (Gazin, 1968), this taxon also presents a front to back sequence of eruption. No data about the permanent premolars eruption sequence is available for litopterns, and no confident information could be taken from the drawings of Scott (1910) and Soria (2001) due to the advanced wear level of the specimens. Based on available information, it is only possible to say that P. ellipsodontoides does not present the eruption sequence of condylarths. Judging by the level of tooth wear, dp4 of Paranisolambda prodromus may have been emplaced simultaneously with, or shortly after the anterior milk premolars, with the excessive wear resulting from the more extensive occlusal abrasion on that tooth. Little can be said after comparing the wear level of lower milk premolars (dp2 4) and first molars (m1 2). Permanent first and second molars precede the eruption of permanent premolars. When m1 is emerging, dp2 4 bear little wear. This is an indication of a short temporal gap between the eruption of dp4 and m1. When m1 is totally erupted and already bear little wear, milk premolars bear intermediate wear and m2 has not erupted yet. Unfortunately no adult individuals, with all molars erupted are known for P. prodromus. In all specimens with milk premolars associated, their wear level is the same. This is suggestive that they erupt almost at the same time, maybe in a reversed order. Unfortunately nothing can be said about the eruption sequence of permanent premolars of P. prodromus, but according to the X-ray of Figure 6, the bud of p4 is the first to calcify and the p3 the second. The same was observed in phenacodonts (West, 1971), in which the permanent premolars emplace in a front to back order. This differential eruption and calcification sequences may be the responsible for the great complexity of p4, as it requires more development time within the jaw. Based on the wear level of the known milk teeth, it is possible to suppose that p4 will erupt slightly before or together with m3. Although it represents a delayed eruption in comparison with P. ellipsodontoides, P. prodromus does not fit in the definition of delayed eruption proposed by Holroyd (2008). Simpson (1967) commented that eruption of permanent teeth is commonly much delayed in notoungulates. Asher et al. (2009) suggested that the pattern of notoungulates would resemble bovids and hippopotamids, which reach sexual maturity or adult size before complete eruption of the permanent dentition. These authors observed that delayed eruption is widely distributed among extant afrotherian mammals, and that it optimizes this feature as a synapomorphy at the afrotherian base. Although it is pending its status in xenathran, Asher et al. (2009) suggested that this feature could be a synapomorphy for southern placentals (Atlantogenata). Asher and Lehmann (2008) developed a methodology to identify the existence of delayed eruption of permanent dentition. They compared the proportion of erupted permanent cheek teeth with jaw length and/or condylobasal length in several species of different groups and observed if considerable skull growth takes place prior to the complete eruption of the permanent cheek teeth. In taxa that show delayed eruption of the permanent dentition, some or all of their permanent teeth finish erupting after the completion of growth, leading to specimens at or near adult size without a full complement of permanent teeth. Unfortunately, no complete mandible or skull were preserved for P. prodromus and P. ellipsodontoides

9 866 JOURNAL OF PALEONTOLOGY, V. 84, NO. 5, 2010 to evaluate if delayed eruption could be a synapomorphy for fossil southern placentals. CONCLUSIONS The major result of this study is the raise of new dental evidence for supporting the assignment of Protolipternidae to the order Litopterna, as suggested by Cifelli (1983b). Other postcranial features presented by Bergqvist (1996) had already corroborated the taxonomical position of the family Proterotheriidae, but the morphological pattern, level of molarization of the deciduous premolars and size of the upper and lower milk dentition, which are close to the pattern found among Proterotheridae, represent new dental support for the placement of Protolipternidae among Litopterna. ACKNOWLEDGMENTS We are indebted to D. A. Campos, of Departamento Nacional da Produção Mineral, Rio de Janeiro, for providing the materials here studied. We are grateful to G.M. Spyrides, of Universidade Federal do Rio de Janeiro, for the help with teeth radiographies, and to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) for supporting this study. REFERENCES AMEGHINO, F Nuevos restos de mamíferos fósiles oligocenos recogidos por el profesor Pedro Scalabrini y pertenecientes al Muso provincial de la cuidad del Paraná. Boletín de la Academia Nacional de Ciencias de Córdoba, 8:5 205 AMEGHINO, F Enumeración sistemática de las especies de mamíferos fósiles coleccionados por C. Ameghino en los terrenos eocenos de la Patagonia austral. Boletín del Museo de La Plata, I:1 26. AMEGHINO, F Contribution al conocimiento de los mamíferos fósiles de la República Argentina. Acta de la Academia Nacional de Ciencias de Córdoba, Number 6, AMEGHINO, F Notices préliminaries sur dês ongulés noveaux des terrains crétacés de Patagonie. 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