Cidaris Revista Ilicitana de Paleontología y Mineralogía

Núm. 30 2010

VIII Encuentro de Jóvenes Investigadores en Paleontología VOLUMEN DE ACTAS

GRUPO CULTURAL PALEONTOLÓGICO DE ELCHE EVOLUTION OF HYPSODONTY IN A CRICETID (RODENTIA) LINEAGE: PRELIMINARY RESULTS USING PATCH ANALYSIS

EVOLUCIÓN DE LA HIPSODONCIA EN UN LINAJE DE CRICÉTIDOS (RODENTIA): RESULTADOS PRELIMINARES UTILIZANDO “PATCH ANALYSIS”

Silvia Pineda-Muñoz1, Isaac Casanovas-Vilar1, Daniel De Miguel1, Aleksis Karme3, Alistair R. Evans2 and Mikael Fortelius2, 3

1Institut Català de Paleontologia (ICP). Mòdul ICP, Campus de la UAB, 08193 Cerdanyola del Vallès (Barcelona). [email protected], [email protected], [email protected]. 2Evolution and Development Unit, Institute of Biotechnology. PO Box 56, Viikinkaari 9, FIN-0014 University of Helsinki, Finland. 3Department of Geology, University of Helsinki. PO Box 64, Gustaf Hällströmin katu 2a, FIN-0014 University of Helsinki, Finland.

ABSTRACT

The development of hypsodonty in the Cricetulodon hartenbergeri – Cricetulodon sabadellensis- Rotundomys montisro- tundi – Rotundomys bressanus lineage is studied using patch analysis. The lower second molar of a sample of each species is scanned using a 3D laser scanner. Then, the scans are processed with GIS software which provides orientation maps of the slopes of the occlusal surface. Contiguous points with the same orientation are grouped into a ‘patch’ that represents a functional structure of the molar crown, so the number of patches relates to dental complexity. This parameter is found to decrease in the lineage coupled with increased crown height. This is interpreted as a result of the evolution of crown planation and loss of cusp interlocking in Rotundomys.

Palabras clave: Morfología funcional, “patch analysis”, Rodentia, , Cricetulodon, Rotundomys, Mioceno, Cuenca del Vallès-Penedès.

RESUMEN Se estudia el desarrollo de la hipsodoncia en el linaje Cricetulodon hartenbergeri – Cricetulodon sabadellensis – Rotun- domys montisrotundi – Rotundomys bressanus mediante “patch analysis”. Para ello se ha escaneado mediante un escáner 3D el segundo molar inferior de una muestra de cada especie. Los escaneos son procesados mediante programas de GIS los cuales permiten obtener un mapa de orientación de los pendientes de la superfi cie oclusal. Los puntos contiguos con la misma orientación son agrupados en un “patch” que representa una estructura funcional de la corona, de modo que el número de “patches” se relaciona con la complejidad dental. Dicho parámetro decrece en este linaje conforme incrementa la altura de la corona. Esto se interpreta como resultado de la evolución de una superfi cie de desgaste plana y a la perdida de la oclusión inter-cúspides en Rotundomys.

Keywords: Functional morphology, patch analysis, Rodentia, Cricetidae, Cricetulodon, Rotundomys, Miocene, Vallès- Penedès Basin.

1. INTRODUCTION adaptive response to cope with the excessive rates of den- tal wear brought about by a new diet (grazing) in more open and dry environments (grasslands). 1.1. HYPSODONTY IN MAMMALIAN HERBIVORES Although there is an ongoing discussion on the causes The acquisition of a hypsodont dentition is a classic behind hypsodonty, silica phytoliths and fi ber of grasses example of evolutionary process among (Janis, (McNaughton et al., 1985), exogenous particles (grit and 1988; Fortelius, 1985). Hypsodonty refers to the tooth dust) attached to the vegetation (Williams and Kay, 2001; crown height (the higher the crown of the tooth is the Mendoza and Palmqvist, 2007), and higher masticatory more hypsodont the ) and is considered to be an efforts as a result of low-nutritional foods (Janis, 1976)

Cidaris (2010).30 - VIII EJIP, pág. 247-252 247 Silvia Pineda-Muñoz et al. have been proposed as main factors favoring a high rate such as Rotundomys and Microtocricetus, could be re- of wear on the teeth. lated to other factors.

Hypsodonty has been acquired independently by sev- Rotundomys is one of the fi rst ‘microtoid cricetids’ eral mammalian herbivores, particularly during the last (only Microtocricetus occurs in older deposits) which is 20 million years. Interestingly, a number of lineages of only known from the Late Vallesian (MN 10) of France, have also experimented a convergent evolution Spain and Portugal. It is believed to have evolved from toward increased crown height (Mödden, 1994). Hence, the more widespread brachyodont genus Cricetulodon and since rodents are the more diversifi ed of all mamma- (Freudenthal, 1967) that ranges from the Late Aragonian lian orders and show an equally diverse suite of feeding (MN7+8) in Turkey (Ünay et al., 2003) to the Middle specializations (seeds, fruits, grass, tubercles and roots, Turolian (MN12) in Spain (Freudenthal et al., 1998). insects or even fi sh) and morphological modifi cations, The genus Rotundomys developed higher crowned mo- they constitute a relevant group for the study of hypso- lars with a simpler lophodont occlusal pattern as com- donty within the context of morphological, dietary and pared to Cricetulodon. The wear surface in Rotundomys environmental changes. is completely plane whereas Cricetulodon shows crested to terraced molars (terminology for dental planation fol- Cheek teeth of rodents include an astonishing array lows Hershkovitz, 1967). The development of fl at wear of different morphologies from the simple molars of the surfaces in the molars has been related to the sim- piscivore species that consist only in shallow basins sur- plifi cation of the chewing stroke, which originally con- rounded by cutting edges to the incredibly complex mo- sisted of two phases (buccal and lingual) with cusp in- lars of the hazel dormouse with many parallel ridges, terlocking, to a single oblique or propalinal stroke with or the lamellar molars of the capybara, just to cite two no cusp interlocking (Butler, 1980, 1985; Lazzari et al., examples. The same dietary adaptations have appeared 2008). independently in different rodent families, and the evolu- tion of increasingly hypsodont molars is not an exception. Two different Rotundomys lineages are known. The fi rst High-crowned molars have arisen convergently in almost one is a small-sized one of rather unknown phylogenetic every rodent family, sometimes more than a single time relationships that includes R. freirensis and R. mundi from within the same family. Portugal and Spain, respectively. The second one, is known from France and Catalonia only, and includes the larger- sized species Rotundomys montisrotundi and Rotundomys 1.2. THE ‘MICROTOID CRICETIDS’ bressanus. Freudenthal (1967) was the fi rst to establish the During the Late Miocene several unrelated muroid phylogenetic lineage Cricetulodon hartenbergeri – Cri- rodents developed higher crowned molars almost simul- cetulodon sabadellensis – Rotundomys montisrotundi in taneously. These muroid lineages include murids (rats which each successive species would show increasingly and mice), gerbillids (gerbils) and a number of cricetids hypsodont teeth coupled with a progressively simplifi ed (relatives of hamsters and New World rats and mice) lophodont pattern. Later on, Mein (1975), added a last that comprise the genera Microtocricetus, Microtodon, member to this lineage, Rotundomys bressanus, which he Anatolomys, Microtoscoptes, Ischymomys, Celadensia, wrongly interpreted as a missing link between cricetids and Blancomys and Rotundomys. The emergence of the arvi- arvicolids. This well-defi ned lineage has been confi rmed colids (voles), perhaps one of the muroid groups where by successive reviews of the genus and its phylogenetic the development of hypsodonty is taken further, by the relationships (see for example Freudenthal et al., 1998). Late Miocene (Martin, 2008) may be seen as part of Nevertheless, there are still many unanswered questions this radiation as well. Schaub (1934) coined the non- regarding the evolution of hypsodonty in this cricetid line- taxonomic term ‘microtoid cricetids’ to refer to all the age: the chewing stroke was oblique or propalinal? when Late Miocene and Early Pliocene (e.g. Trilophomys, was cusp interlocking lost? did this imply any change in Bjornkurtenia, Baranomys) cricetid genera that devel- the masticatory muscles? to which dietary changes (grass-, oped similar hypsodont teeth with a lophodont occlusal fruit- or leaf-eating) was it related? pattern. This parallel development of hypsodonty may have been related to the consumption of more fi brous, In order to answer all these major questions we have less nutritive vegetal material, such as grasses, but this designed a multiproxy study of these rodents that will hypothesis has not been formally tested. The Late Mi- make use of all the techniques that have been success- ocene coincides with the time of major expansion of fully applied to the study of feeding specializations in the grass-dominated ecosystems in Eurasia (Quade and dentitions of larger mammals (dental microwear, analysis Cerling, 1995; Cerling et al., 1997; Jacobs et al., 1999). of the stable isotopes in tooth enamel, geometric morpho- Grasslands now occupy wide areas of central Asia, de- metrics and 3D modelling of teeth). Here we present our fi ning a wide and continuous belt from the shores of the preliminary results of the application of 3D modelling Yellow Sea to those of the Black Sea. However, major and GIS (Geographical Information Software) to study grass-dominated ecosystems never extended across the the complexity of the dental pattern of these rodents by Mediterranean regions (Jacobs et al., 1999), so the evo- the means of the patch analysis technique (Evans et al., lution of hypsodonty in certain ‘microtoid cricetids’, 2007). 248 Cidaris Evolution of hypsodonty in a cricetid lineage

Figure 1. Molar complexity in the Cricetulodon-Rotundomys lineage. Three-dimensional occlusal reconstructions, patch maps and rose diagram for slopes directions of a second lower molar (m2), the number of patches is also indicated. A) Cricetulodon hartenbergeri. B) Cricetulodon sabadellensis. C) Rotundomys montisrotundi. D) Rotundomys bressanus. The Cricetulodon sabadellensis specimen is a right m2 that has been reversed and the Rotundomys montisrotundi specimen and their respective rose diagrams have been slightly rotated for the sake of comparison.

2. MATERIAL AND METHODS than Can Llobateres 1 (9.3-9.5 Ma) whereas Torrent de Febulines 3 belongs to the latest Vallesian (9-8.7 Ma).

2.1. STUDIED SPECIES AND PROVENANCE OF THE MATERIAL 2.2. TOPOGRAPHIC MODELS OF MOLAR CROWNS AND MEASUREMENT OF DENTAL The studied material comprises complete molar series COMPLEXITY as well as isolated molars that belong to four different spe- In this preliminary study just one lower second molar cies C. hartenbergeri, C. sabadellensis, R. montisrotundi (m2) of each one of the four species is studied in order to and R. bressanus. All the specimens are housed within test the validity of the methods. The study focuses on the the collections of the ‘Institut Català de Paleontologia’ m2 because these teeth show an intermediate wear stage, (ICP) and were recovered from different Vallesian sites of and microwear pattern, between the fi rst and the third the Vallès-Penedès Basin. The Vallès-Penedès Basin is a mo lar. relatively small and elongated half-graben that is situated between the Catalan Coastal Ranges, thus being parallel The methods for generating the 3D elevation models, to the Catalan coastline. This basin originated as a result to build topographic and orientation maps and to calcu- of an extension episode that affected much of the Western late measures of dental complexity are after Evans et al. Mediterranean during the latest Paleogene and the Neo- (2007). First, the teeth were scanned using a 3D laser gene and was fi lled mostly during the Miocene by conti- scanner Hawk Nextec at the Viiki Kampus of the Uni- nental sediments (see Cabrera et al., 2004). The Miocene versity of Helsinki. The scanning resolution is 10μm. In Vallesian successions have been particularly well studied order to avoid sparkles and obtaining clearer pictures the and have delivered an important number of rich sites for teeth were covered with powdered talcum spray. The mo- which an accurate dating on the basis of bio- and mag- lars were oriented according to their mesio-distal axis and netostratigraphy is available (Agustí et al., 1997). The inclined to maximize crown-base projection. The scans specimens analyzed come from four different sites: Can were plotted using Surfer for Windows (Golden Soft- Ponsic (C. hartenbergeri; Hartenberger and Crusafont, ware, Inc.). Image size was standardized by re-gridding 1979), Can Llobateres 1 (C. sabadellensis; Hartenberger, the initial scans to a resolution of 150 data rows so all the 1965), Rubí-Terrassa motorway site 11 (R. montisrotundi; teeth were scaled to the same length. Then, topographic listed as sp.nov for Agustí et al., 1997) and Torrent de and orientation maps of the molars were generated using Febulines 3 (R. bressanus; Agustí and Gibert, 1982). Can a GIS software written by one of the authors (A.R.E; see Ponsic and Can Llobateres 1 are placed in the Early Valle- also Evans et al., 2007). Using the same software orien- sian, although Can Llobateres 1 is certainly younger, with tation maps were generated after calculating the slope an estimated age of 9.5-9.7 Ma (Agustí et al., 1997). The direction for all the points with a minimum slope of 10 Late Vallesian site of Rubí-Terrassa is somewhat younger degrees in the topographic maps. Then, these slopes were Cidaris 249 Silvia Pineda-Muñoz et al. classifi ed into 8 different categories of orientation, each tion results from a progressive change in the shape of the one covering 45º (see Fig. 1). The maps of the rodent mo- cusps and crests so their walls tend to become more verti- lars were divided into different patches that result from cal (Lazzari et al., 2008). Since dental complexity is mea- grouping contiguous points with the same orientation as a sured as the number of orientation patches (OPC) it is ex- patch (Fig. 1). This was done using the OPC (Orientation pected that this parameter will show lower values in plane Patch Count) algorithm with a minimum patch size of 15 (sensu Hershkovitz, 1967) molars as compared to crested points. The measurement of OPC can be used as a meas- or terraced ones because the diversity of orientations is ure of dental complexity since it can be interpreted as the reduced and all the slopes approach 90º. The evolution number of functional areas or ‘tools’ in the molar crown of simpler dental morphologies is known to have evol- used to process food items. This functional complexity is ved in association with increasing hypsodonty in lineages thought to be related to the dietary habits so the ingestion from several rodent families, including the theridomyids of foods that require more mechanical processing result in (Hautier et al, 2010), cricetids (Hershkovitz, 1967) or the more complex molar morphologies (Evans et al., 2007). heteromyids (Wood, 1935) just to cite some examples. In these rodent families increasingly hypsodont teeth are Tooth wear is known to alter crown topography. This is supposed to have evolved in relation to an increased in- not very important in molars with a fl attened crown (Her- take of grasses and abrasives, so in the more hypsodont shkovitz, 1967) but it dramatically alters the topography species the proportion of more though and fi brous plant of cuspidate molars (see Lazzari et al., 2008 and refer- materials and exogenous particles is greater. Evans et al. ences therein). In our case, Cricetulodon has cuspidate (2007) found that the complexity of molar morphology molars and in order to compare the different specimens it was greater in herbivorous Rodentia and Carnivora as is mandatory to take into account the degree of wear since compared to carnivorous ones. The OPC values obtained it may have profound effects on the measure of dental for C. hartenbergeri and C. sabadellensis fi t within the complexity. Therefore, and after excluding unworn teeth range of values for omnivore Rodentia as calculated by as well as specimens in very late wear, we have estab- Evans et al. (2007, fi g. 2), even though they are close to lished three very broad categories of tooth wear: 1) nearly the lower boundary. Quite surprisingly, the OPC values unworn teeth displaying wear only on the tips of the main for R. montisrotundi and R. bressanus are below the range cusps; 2) wear exposes a wide area of dentine in the main of rodents and fall within those of carnivore Carnivora cusps and also affects the ridges connecting these tuber- (Evans et al., 2007, fi g. 2). This discrepancy with the re- cles, eventually exposing a narrow dentine band in the sults of Evans et al. (2007) may be related to the fact that ridges; 3) worn molars with wide dentine areas exposed these authors considered the whole molar series whereas in the main cusps and ridges. In our analyses we have only we are just considering a single molar. Furthermore, it considered molars in wear stage 2. This wear stage is cho- could also be related to the fact that these authors only in- sen because of the availability of specimens. A subdivi- cluded a few relatively hypsodont species in their sample sion of the degree of wear into more than three categories of 49 muroid species. That work just considered three mu- may be possible, especially in the case of Cricetulodon. roid subfamilies, namely the sigmodontids, the otomyids This question as well as the intra-specifi c variation in the and the murids, discarding markedly hypsodont muroid number of patches between the categories of dental wear families such as the arvicolids and the spalacids (blind is going to be approached in forthcoming studies. mole rats). This question cannot be solved for the moment since it requires the collection of new data for both extant 3. RESULTS and fossil specimens. Fig. 1 shows the number of patches for the m2 of each As we have already exposed, simplifi cation of the den- one of the species considered. The number of coloured tal morphology can also be related to the loss of cusp inter- patches is indicated below each one of the fi gures so it can locking and to a change in the orientation of the chewing be appreciated that it decreases throughout the members stroke from two-phase ectental movement (see Butler, of this lineage. C. hartenbergeri shows 129 patches, C. sa- 1980, 1985) to a more oblique or even propalinal stroke. badellensis 128, R. montisrotundi 91 and R. bressanus 87. On the basis of dental microwear analyses and cusp orien- While the number of patches is almost identical in the two tation (measured using different methods) Lazzari et al. Cricetulodon species it is markedly lower in Rotundomys, (2008) have shown that R. montisrotundi had an oblique especially in R. bressanus. Dental complexity, measured chewing stroke. The more advanced R. bressanus may by OPC, seems to decrease with increasing hypsodonty in have also had an oblique stroke or a propalinal one, but this cricetid lineage. this question will be approached in forthcoming studies.

4. DISCUSSION 5. CONCLUSIONS AND FUTURE PROSPECTS The evolution of the C. hartenbergeri – R. bressanus Our results point towards a reduction of dental com- lineage implies the increase of tooth crown height, the de- plexity coupled with the evolution of hypsodonty and pla- velopment of a fl at wear occlusal surface (implying no nation in the C. hartenbergeri – R. bressanus lineage. This cusp interlocking) and a reduction in dental complexity simplifi cation of the tooth pattern may well be related to in the m2 of Rotundomys. The evolution of crown plana- the development of a fl at wear surface (which requires 250 Cidaris Evolution of hypsodonty in a cricetid lineage the slopes of the main cusps and ridges to be vertical ac- Spain and France. Treballs del Museu de Geologia de Barcelona, cording to Lazzari et al., 2008) and to the loss of cusp 7, 11-93. Hautier, L., Clavel, J., Lazzari, V., Gomes Rodrigues, H. and Vianey- interlocking as well. 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