A peculiar specimen of Panochthus (Xenarthra, Glyptodontidae) from the Eastern Cordillera, Bolivia

. Panochthus Burmeister is one of the most diversified and widely distributed glyptodonts in the Pleistocene of South America, which includes areas located at high altitudes (>4,000 m a.s.l.). Within the genus, eight species ( P. intermedius Lydekker, P. subintermedius Castellanos, P. tuberculatus (Owen), P. frenzelianus Ameghino, P. greslebini Castellanos, P. jaguaribensis Moreira, P. hipsilis Zurita, Zamorano, Scillato-Yané, Fidel, Iriondo and Gillette, and P. florensis Brambilla, López and Parent) are currently recognized. Here, we report a dorsal carapace (UATF-V n/n) from the Pleistocene of the surroundings of Potosí, Bolivia, that shows some morphological particularities when compared to the carapace of P. intermedius, P. frenzelianus, P. subintermedius and P. tuberculatus , including: a) its maximum dorso-ventral diameter is at the anterior half, meanwhile in other species is at mid-point ( e.g. , Propalaehoplophorus ) or at posterior half ( e.g. , Glyptodon ); b) the dorsal profile is different in comparison to other glyptodonts ( e.g. , Glyptodon , Glyptotherium , Neosclerocalyptus , Propalaehoplophorus ); c) the ornamentation pattern of the osteoderms shows a central figure surrounded by small polygonal figures along the most exposed surface of the carapace (except for the mid-dorsal region that shows reticular ornamentation pattern), being different from that of the remaining species: of Panochthus , in which central figures are limited to the caudal/cephalic and most lateral regions of the carapace. In summary, the combination of characters suggests that it could belong to a new species or, alternatively, to P. floriensis or P. jaguaribensis in which the dorsal carapace is not yet known . The phylogenetic analysis confirms its basal position among Panochthus and highlights the importance of these high elevation areas of the Andes in South America in order to understand the complex evolutionary history of glyptodonts.


Introduction
Xenarthra is a particular group of mammals typical of the Neotropical Region; they are widely represented in the South American fossil record, being conspicuous because of their temporal extension (Early Eocene-Recent), and the frequency of their findings (Paula Couto, 1979;Oliveira and Bergqvist, 1998;Bergqvist et al., 2004;Gaudin and Croft, 2015;Delsuc et al., 2016). During most of the Cenozoic they were among the most diversified clades of South America, although their current diversity is quite reduced (Scillato-Yané, 1982;Abba et al., 2012).
Of the two great clades currently recognized, Pilosa and Cingulata; the cingulates achieved the greatest diversification and temporal range. Cingulata has near 220 species distributed in ca. 105 genera known in the fossil record since the Early Eocene (Scillato-Yané, 1980, 1982McKenna and Bell, 1997), in contrast with the modern diversity, reduced to ca. 21 species (Abba et al., 2012;Feijó et al., 2019).
Within Cingulata, Glyptodontidae is the clade that reached the largest size (Soibelzon et al., 2012). This group is first recorded in the Late Eocene of the Patagonian region of Argentina (Ameghino, 1902;Gaudin and Croft, 2015), and later experienced a diversification and radiation process since the Late Miocene (Fernicola, 2008;González-Ruiz et al., 2012;Zurita et al., 2016), probably related to the development of open biomes of grasslands (Delsuc et al., 2004;Carlini and Zurita, 2010;Iglesias et al., 2011;Mitchell et al., 2016).
Glyptodontidae are relatively well known in southern South America since the pioneering studies of Ameghino (1889), Burmeister (1870Burmeister ( -1874 and Scott (1903Scott ( -1904, among others. However, one of the regions in which their diversity and evolutionary history is least known is that of the Andean and sub-Andean areas of Bolivia and Peru where, traditionally, glyptodonts were only mentioned as part of paleofaunal lists (i.e., Hoffstetter, 1973;Pujos and Salas, 2004).
More recently, the finding of new specimens allowed a better knowledge of these large armored herbivores, especially those of the Pleistocene. Zurita et al. (2011) reported the first record of Panochthus intermedius Lydekker, 1895 from the middle Pleistocene out of the current territory of Argentina, near Cochabamba, Bolivia. Later on, Zurita et al. (2017) recognized the first glyptodont species exclusive from the current territory of Bolivia, Panochthus hipsilis Zurita, Zamorano, Scillato-Yané, Fidel, Iriondo and Gillette, 2017, which in turn is one of the fossils of Xenarthra found at the highest altitude, ca. 4,500 m a.s.l., together with the Glyptodontinae Glyptodon jatunkhirkhi Cuadrelli, Zurita, Toriño, Miño-Boilini, Perea, Luna, Gillette and Medina, 2020. More recently, Zamorano and Almonte (2018) reported the first record of the genus Panochthus Burmeister, 1866 from Peru (ca. 3,800 m a.s.l.) (Zamorano and Oliva, 2020).

Materials and methods
The specimen here described belongs to the Vertebrate Paleontology Collections, "Universidad Autónoma Tomas Frías", Potosí, Bolivia. The list of characters and character states are indicated in the Appendix 1. The materials used for comparison and phylogenetic analysis (Appendix 2) include the holotypes and most complete materials assigned to the different species of Panochthus and Propanochthus Castellanos, 1925(see Burmeister, 1874. For chronological purposes, we follow the International Chronostratigraphic Chart 1 (Cohen et al., 2013; International Commission on Stratigraphy, 2020).
Description of the phylogenetic analysis: The material here studied (UATF-V n/n) was included in a cladistic analysis modified from that of Zurita et al. (2017)  Index abbreviations: TL: antero-posterior length of the dorsal carapace without considering the dorsal curvature; APLDC: antero-posterior length of the dorsal carapace along dorsal curvature; ICDC: Index of Convexity of the Dorsal Carapace: ratio of the length of the dorsal carapace (in a straight line, without considering curvature) and the length considering the curvature.
Other abbreviations: L: tree length; RI: retention index; CI: consistency index; MPT: most parsimonious tree; Ma: million years; m a.s.l.: meters above sea level.

Geographical and geological setting
Mojotorillo (ca. 3205 m a.s.l.) is a fossiliferous locality placed in the area between Betanzos and Ckonapaya, north-east of Potosí Department, Bolivia ( Fig. 1). It is located in the homonymous basin that regionally belongs to the southern part of the Bloque Andino Oriental (Gubbels et al., 1993;Kley, 1996). The basin is geomorphologically characterized by gullies produced by the strong fluvial erosion of the Jachcha LLuIu river that crosses the site from east to west, exposing continental sediments. The lithology of the Mojotorillo basin is composed of Cretaceous sandstones overlain by a sequence of Quaternary sediments assigned to the Pleistocene-Holocene (Aubouin et al., 1965). The general sequence reaches a maximum of ca. 20 m thick, and is formed from base to top by brown-yellowish siltstones interbedded with conglomerates with clasts of Paleozoic rocks; followed by levels of brown-reddish claystones and lenses of fine to medium grain sandstones. A horizon of volcanic tuff, more than 1 m thick is exposed 2 m below the top of the stratigraphic sequence (Pinto Yupanqui, 2015). Outcrops are limited to ravines, whose fossiliferous horizons are below and over the tuff level. At the precise point where UATF-V n/n was recovered, the sequence is ca. 5 m thick (Fig. 1), and locally represented by an interbedding of brownish massive medium grain sandstones and silty fine grain sandstones, with the occasional development of thin levels of clay. Towards the middle of the sequence, below the UATF-V n/n bearing level, there is interbedded a level of conglomerates.

Systematic
The dorsal profile of UATF-V n/n differs even more from that corresponding to the carapace of P. frenzelianus and P. intermedius, since in the latter species the highest point is at the midpoint of the carapace and descends towards both ends (anterior and posterior) with an angle of ca. 15°.
Cephalic notch (Fig. 2). It is partially reconstructed, hiding the morphology of osteoderms. Antero-dorsal region ( Fig. 2A). Towards the anterodorsal region (immediately behind the restored osteoderms that delimit the cephalic notch), a series of osteoderms are visible.   Antero-lateral region. Osteoderms that delimit the margin of this region of the dorsal carapace are mostly reconstructed. However, subsequent osteoderms have an ornamentation pattern similar to those of the middorsal region (Fig. 2B), forming a reticular pattern, but with a shorter relative diameter. This condition is shared with the remaining species of the genus (e.g., Porpino et al., 2010). Middle-lateral region. Osteoderms that limit the ventral margin of this region are mostly reconstructed.
Original osteoderms show that the exposed surface of the most anterior area of this region shows a reticular pattern with ca. 17

Discussion
The comparative study carried out in this work indicates that the dorsal carapace UATF-V n/n has a combination of characters typical of the genus Panochthus, i.e., dorsal carapace with thick osteoderms polygonal in outline, with small, isodiametric, polygonal tubercles, forming a reticular pattern on the mid-dorsal region; or, in "rosette" in other regions, with a flat and smooth central figure, never elevated as in Propanochthus, Nopachtus, or Phlytaenopyga Zamorano et al., 2014). In turn, UATF-V n/n has its own characteristics in the carapace, different from the other Panochthus species in which this structure is known. Among them, the dorsal profile (i.e., maximum height at the level of the anterior region, with a slope ca. 30º from this point to the cephalic end, and posterior profile from the maximum height almost horizontal) and the ornamentation pattern of the osteoderms of the antero-dorsal, postero-dorsal and postero-lateral regions and posterior area of the middle-lateral region (i.e., distinguishable central figure, flat, smooth and sub-circular, surrounded by up to five series of peripheral figures) (Fig. 2). This combination of characters suggests that UATF-V n/n may represent a new species of Panochthus. However, it has to be noted that, up to date, the dorsal carapace of some species, such as P. jaguaribensis and P. floresiensis is still unknown, preventing a rigorous comparison between these taxa and UATF-V n/n. From a phylogenetic standpoint (Fig. 4), the analysis here developed confirms the monophyly of the genus Panochthus (node C), thus corroborating the proposal of Zamorano and Brandoni (2013) (see Zamorano et al., 2014;Zurita et al., 2017) ) support the inclusion of UATF-V n/n in this genus, occupying a basal position within the lineage Propanochthus + Panochthus (although with more derived characters than Pr. bullifer and P. intermedius). This basal position of UATF-V n/n results similar to that obtained by Cuadrelli et al. (2020) for another sub-andean glyptodont, G. jatunkhirkhi, in which this latter appears as sister group of G. reticulatus + G. munizi. Thus, taxa from high areas belonging to different lineages (i.e., G. jatunkhirkhi and P. hipsilis) consistently show basal phylogenetic positions relative to lowland Pleistocene taxa of both genera, Glyptodon and Panochthus (Zurita et al., 2017;Cuadrelli et al., 2020).
These results support the ideas posed, in a precladistic context, by Castellanos (1942), suggesting that the presence of a single evolutionary lineage characterized by the progressive change of ornamentation of osteoderms of the dorsal carapace, from the most plesiomorphic condition of a "rosette" pattern (central figures surrounded by one or more series of peripheral figures, such as Propanochthus), up to the most apomorphic condition, with a "reticular" pattern (osteoderms with only isodiametric figures, without distinguishable central figures, such as most regions of the carapace of Panochthus) (Zamorano, 2012;Zurita et al., 2017). On the other hand, the phylogenetic distribution of the representatives of the genus Panochthus, together with related taxa, is also in agreement with the last proposal of Zurita et al. (2017) for this clade, in which Pr. bullifer forms the sister group of Panochthus (Fig. 4).
From a paleobiogeographic point of view, Cuadrelli et al. (2020) suggested an early dichotomic radiation of Glyptodontidae, with two lineages: one of northern origin, with a wide latitudinal distribution and low specific diversity (i.e., Glyptodontinae) and another one of southern origin (not yet formally named), with more restricted latitudinal distribution but higher specific diversity (i.e., the remaining representatives of Glyptodontidae). Within this last radiation, geographically more restricted ("southern radiation"), Panochthus represents the clade with the largest latitudinal distribution, with records in Argentina (Chaco-Pampean, Mesopotamic, sub-Andean and Patagonian regions), Uruguay; Brazil (southeast and northeast) Paraguay (southeast), Bolivia (central and south), and Peru (southeast). In this scenario, the southernmost limit belongs to the locality of Fitz Roy, Deseado Department, Santa Cruz Province, Argentina (P. tuberculatus, 47°01' S 67°14' W, Tauber and Palacios, 2007), whereas the records of northeastern Brazil represent its northern limit (P. greslebini and P. jaguaribensis, 05°11' S 39°17' W; Porpino et al., 2014).
From a paleoecological perspective, the records of Panochthus are commonly associated with the presence of Glyptodon (e.g., Duarte, 1997;Porpino et al., 2004;Oliveira et al., 2010;Gasparini et al., 2016). In this sense, in low-land regions (i.e., Argentina, Uruguay and south of Brazil) the presence of both genera (Glyptodon and Panochthus) are commonly related to open or semi-open grasslands and semi-forested environments, under wide range of different paleoclimatic conditions, at least for the late Pleistocene (Gasparini et al., 2016;Krapovickas and Tauber, 2016;Ferrero et al., 2017;Ubilla et al., 2017).
In turn, the records of Panochthus in the intertropical region (i.e., northeastern Brazil) corresponds to P. greslebini and P. jaguaribensis (the latter species considered endemic to this region), however the holotypes of these species have no stratigraphic provenance and can only be assigned to the Pleistocene sensu lato (Porpino et al., 2014;Zamorano et al., 2014). Although this situation difficult determining the type of environment inhabited by these species, the presence of Panochthus in this intertropical region, together with Glyptotherium and Pachyarmatherium, indicates a variety of ecological niches (Oliveira et al., 2010), linked to dense vegetation and high humidity that characterized the northeastern Brazil during the Pleistocene (Vivo and Camingnotto, 2004;Cione et al., 2009;Zamorano et al., 2014). In this sense, the presence of Panochthus in northeastern Brazil could be explained by the movement of these glyptodonts through arid corridors, grasslands or savannas (Scillato-Yané et al., 1995;Zamorano et al., 2014) following, for example, the eastern route proposed by Prado et al. (2003) to explain the dispersal of Stegomastodon (= Notiomastodon Cabrera, 1929) in South America, or it could indicate that the endemic species of Panochthus in this region (P. jaguaribensis) was adapted to more humid conditions compared to the remaining species of Panochthus.
Regarding to high elevation areas, the representatives of Panochthus from Bolivia include: (1) an incomplete skull and almost complete dorsal carapace (MURB 1906A/1906B) holotype of P. hipsilis, and a caudal tube (MHNS 8) assigned to P. hipsilis, from the surroundings of Potosí (Bolivia), at ca. 4,000 m a.s.l.; (2) an isolate osteoderm (MUSM-s / n) referable to Panochthus sp., from Desaguadero (Peru) at ̴ 3,800 m a.s.l. (found very close to the limit with Bolivia); (3) an almost complete dorsal carapace (UATF-V n/n) here assigned to Panochthus sp., from the surroundings of Potosí (Bolivia), at ca. 3,205 m a.s.l.; (4) an almost complete specimen (MHNC-13491) assigned to P. intermedius, from near Cochabamba (Bolivia), at ca. 2,600 m a.s.l.; (5) one osteoderm and fragments of a caudal tube (MNPA-V 006598) assigned to Panochthus sp., from the Tarija Valley (Bolivia), at ca. 1,870 m a.s.l. (Zamorano and Almonte, 2018;Zamorano and Oliva, 2020). In this sense, these five records of Panochthus, together with the large diversity of herbivores and megaherbivores (i.e., Glyptodontidae, Gomphotheriidae, Megatheriidae, Toxodontidae) from the Andean region of central Bolivia and southern Peru, may be likely related to the "Minchin paleolakes system", a huge system of water bodies located in the Andean Altiplano, that would have increased the primary productivity of these ecosystems during the Pleistocene (Sánchez-Saldías and Fariña, 2014). Specifically, the locality of Mojotorillo has provided several remains belonging to large (i.e., Equidae and Carnivora) and megamammals (i.e., Xenarthra and Litopterna) (Pinto Yupanqui, 2015), including this particular specimen of Panochthus. Although we cannot confirm the co-occurrence of this palaeofauna, the restricted stratigraphical level from which most of them were recovered, suggests that these fauna could have lived in a very short geological time. If so, this could support the idea that mountainous areas developed a large vegetal diversity supporting a high faunal variety, both with significant levels of endemism (Wardle, 1991;Rogers and Walker, 2005;Burke 2007;Sadler and Bradfield, 2010, among others).
These paleobiogeographic and paleoecologic aspects suggest that the different species of Panochthus were likely adapted to a specific environment. This is particularly evident in those taxa that inhabited high-altitude ecosystems in the Eastern Cordillera of Bolivia, associated with high primary productivity and high biodiversity (Wardle, 1991;Roger and Walker, 2005;Burke 2007;Sadler and Bradfield, 2010;Sánchez-Saldías and Fariña, 2014) such as P. hipsilis and UATF-V n/n, or those species from the Amazon, related to dense vegetation and high humidity levels, such as P. jaguaribensis (Scillato-Yané et al., 1995;Vivo and Camingnotto, 2004;Cione et al., 2009;Zamorano et al., 2014). Both cases contrasting with the Pampean species, commonly associated with temperate savannas and temperate grasslands related to high variation of annual temperature (Ray and Adams, 2001;Vivo and Carmignotto, 2004;Mayle, 2006;Varela et al., 2018), such as P. frenzelianus, P. subintermedius and P. florensis (Zurita et al., 2017;Zamorano et al., 2021).

Conclusions
In this work, a new record of Panochthus from the Pleistocene of Mojotorillo, Potosí, Bolivia, is reported. This is the second most complete specimen recovered in the high Andes of Bolivia. The specimen here described is assigned to Panochthus sp. because it shares some features with the other species of the genus (i.e., osteoderms of the middorsal region with a reticular pattern); however, it has also features not yet described for any other species of Panochthus from which the dorsal carapace is known (i.e., distinguishable central figure in the osteoderms of most regions of the dorsal carapace). The existence of three species (P. greslebini, P. jaguaribensis and P. florensis) in which the dorsal carapace is not yet known prevents confirming that it is a new taxon.
Phylogenetically, UATF-V n/n has f ive synapomorphies allowing its inclusion within the genus Panochthus, occupying a basal position within the obtained cladogram, as sister group of all Panochthus spp. but P. intermedius.