Tooth wear as a tool for reconstructing diet in fossil ungulates

 

Recreating paleobiology from fossils has often included considerable speculation. Even rigorous studies can sometimes misjudge diet due to phylogenetic constraints in the morphology (MacFadden et al. 1999). In spite of the difficulties, diet aids in interpretation of the habitat and ecological interactions. The indirect evidence from herbivores is sometimes the only indication of plant types in the area, because the fluctuation of herbivore abundance yields insight to the climatic transitions of an area.

The diet of fossil ungulates provides valuable information about the food resources in a given habitat and thus is a useful tool in reconstructing paleohabitats. Additionally, information about the diet of fossil mammals provides insight into the resource partitioning and dietary behaviour of ungulate populations. Consequently it is also proposed to allow inference on the differential dietary regimes and seasonal fluctuation in diets. The dietary interpretation of mammalian teeth has traditionally involved either direct (actualistic) comparison with living animals, the application of general functional principles, or - increasingly during the latest few decades - the study of the wear patterns left on teeth by food.

In extant mammals, field observation, analysis of gut contents and faeces are the principal sources of dietary information. In fossil taxa however hard tissues are the only sources of evidence we usually have. As the diet related interface between the organism and its habitat, teeth may provide a significant part of this evidence. Ungulates generally have certain biomechanical adaptations of their dentition in common, which are closely related to their particular herbivorous diets. The methodology proposed here does therefore restrict dietary analysis to the cheek tooth dentition of herbivorous ungulates, because for taphonomic reasons cheek teeth are among the most frequently preserved skeletal elements in almost all fossil mammal assemblages. Information about dietary preferences, that can be gained based on the dentition accessible for a wide variety of Pleistocene mammalian palaeocommunities.

Because the diet varies through time, such information can be used to propose a reconstruction of seasonality in forage selection in fossil and sub-fossil ungulates communities.


Methods assessing dietary traits based on dental wear evidence

The dietary interpretation of mammalian teeth has been so far dealing with the application of general functional adaptations, (e.g. Rensberger et al. 1984, Kaiser 2001, Eisenmann 1998), the analysis of stable isotopes of the dental tissue (e.g. Cerling et al. 1997, Balasse et al. 2002a, 2002b, Bocherens et al. 1996, Koch et al. 1998) and the investigation of wear patterns (e.g. Butler 1972, Fortelius 1985, Fortelius & Solounias 2000). The morphology of an unworn tooth mirrors the evolutionary adaptation over a long, previous chronologic interval. The wear pattern however observed with the naked eye (mesowear pattern) mirrors a considerable part of the life time of an individual, and the microscopic defects on the occlusal enamel (microwear) represents a snapshot of these, sometimes representing the animals’ last meal. The high degree of functional similarity in occlusal mechanics for unimodal chewing systems of many herbivorous ungulates provides the prerequisite for an interpretation of the mesowear pattern as a trophic signal (Fortelius & Solounias 2000). Until recently, reliable reconstructions of paleodiet based on molar and premolar wear have been very laborious. It was difficult to apply them to more than just a few individuals and fossil localities (Fortelius 1982, Fortelius 1985, Hunter & Fortelius 1994, Janis 1990, Janis & Fortelius 1988, Rensberger 1973, Rensberger et al. 1984, Hayek et al. 1992, Solounias & Moelleken 1992a, 1992b, Solounias et al. 1994, 1995, Teaford & Walker 1984). The mesowear method (Fortelius & Solounias 2000) and the ”extended” mesowear method (Kaiser and Solounias 2003, Franz-Odendaal & Kaiser 2003) however allow us to use occlusal wear features to reconstruct a biologically based dietary adaptation.


The Mesowear method

The attrition (tooth to tooth contact) controlled occlusal pattern of ungulates (Rensberger 1973, Lucas 1979, Walker 1984) is superimposed by food specific abrasion (tooth to food contact). Thus equilibrium is established, which causes the mesowear pattern, which is stable over a long period of time (Fortelius & Solounias 2000, Kaiser et al. 2000a, 2000b, Kaiser et al. 2003). It has been shown that the mesowear variables are well suited to classify 63 recent ungulate species according to their prevalent trophic regimes (Fortelius & Solounias 2000, Kaiser et al. 2000a). This approach has been applied to various fossil and extant Equidae (Kaiser 2001, Kaiser 2002, Kaiser & Bernor 2001a, 2001b, Kaiser et al. 2000a, 2000b, 2000c, 2001, 2003, Kaiser et al. 2001, Kaiser & Solounias 2003, Kaiser & Fortelius 2003, Franz-Odendaal & Kaiser 2003, Franz-Odendaal et al. 2003, Kaiser & Franz-Odendaal 2004) to fossil Cervidae (Kaiser & Croitor 2002, Kaiser & Croitor 2004). This results in the identification of the dietary regime and allows us to infer the ecological role of a fossil taxon in a given habitat (Every 1970, Janis 1990, Guthrie 1990, Kaiser 2002).

The mesowear method has currently been developed further by Kaiser et al. (2000a), Kaiser & Solounias (2003) and Franz-Odendaal & Kaiser (2003). The extension of the method is of particular importance for small assemblages of isolated teeth, which otherwise would not be accessible to mesowear analysis. The emerging ”extended” mesowear method now allows us to assign a trophic reference taxon to small fossil populations. Compared to the microwear method, which was established 10 years ago, (e.g. Hayek et al. 1992) the ”extended” mesowear method is much less laborious. This method allows to include large series of specimens for the first time. Additionally the extension allows a much higher stratigraphic resolution in large faunas, because it now is possible to establish palaeodietary reconstruction throughout well established stratigraphic sections.


The Microwear method

At first, scanning electron microscopy (SEM) has been used to examine dental microwear for nearly two decades. Rensberger (1978) for example, employed a scanning electron microscope to examine rodent molars, and related differences in incidences of different microwear types to a variety of factors, including food properties, tooth shape, enamel microstructure, occlusal pressure and chewing rates. Further, Walker et al. (1978) demonstrated molar microwear correlates to diets of hyraxes. For example, browsing tends to produce pits, while grazing leads to a preponderance of parallel microwear scratches. Much of the research that has followed has focused on assessing the limitations and potentials of microwear research. Gordon (1982, 1984a, b, c) for example, has found that quantification and subsequent statistical analyses reveal microwear patterning not obvious in qualitative investigations. Also, further study has demonstrated that microwear does discriminate among extant primates with differing diets. Teaford & Walker (1984) showed that frugivorous anthropoids have a higher percentage of pits on their molar crushing surfaces than do folivores and, among frugivores, hard-object feeders can be differentiated by even higher relative frequencies of pits. Work progressed to understand the complexity of microwear formation and the roles of plant phytoliths (Lucas & Teaford 1995), abrasive grits (Maas 1991, 1994, Ungar et al. 1995) and varying compressive forces (Maas 1994) with influence the formation of specific dental microwear patterns are determined.

Researchers have documented molar microwear patterns for a great variety of fossil taxa, including thylacinids (Robson & Young 1990), aplodontids (Rensberger 1982), multi-tuberculates (Krause 1982), carpolestids (Biknevicius 1986), Miocene hominoids (Teaford & Walker 1984, Daegling & Grine 1994, Walker et al. 1994), ruminants (Solounias & Hayek 1993, Rivals & Deniaux 2003), Pleistocene felids (Van Valkenburgh et al. 1990), Eocene prosimians (Strait 1991), subfossil lemurs (Rafferty & Teaford 1992), Pleistocene cercopithecines (Lucas & Teaford 1994, Teaford & Leakey 1992, Ungar & Teaford 1996) and finally, Pliocene and Pleistocene hominids (Grine 1977, 1981, 1984, 1986, 1987, Grine & Kay 1987, Lalueza Fox & Peréz-Peréz 1993, Lalueza et al. 1993, Puech 1979, 1982, 1986a, 1986b, Puech & Albertini 1983, 1984, Puech et al. 1980, 1981, 1983, 1985, 1986a, 1986b, Walker 1981).

In 2002, Solounias and Semprebon proposed a new and greatly simplified methodology for the assessment of the dietary adaptations of living and fossil taxa. It was developed to allow for microwear scar topography to be accurately analysed at low magnification (35x) using a standard stereomicroscope. A large extant comparative ungulate microwear database (809 individuals; 50 species) is presented and interpreted to elucidate the diets of extant ungulates. This method has been successfully applied to ungulates (Solounias & Semprebon 2002, Merceron et al. 2004, Semprebon et al. 2004a, b) and primates (Godfrey et al. 2004).


Combined use of microwear and mesowear

Rivals and Semprebon (2006) and Rivals et al. (2007) use both microwear and mesowear analysis to study the diet of extinct animals by comparison to a database of extant species as reference. This combination has been shown to add different pieces of evidence to the dietary behaviour, environmental context and their change through time that are complementary, but not congruent. Dental microwear analysis allows characterization of the last 15 day diet (Mainland 1998b) and mesowear of the last few months (Fortelius & Solounias 2000).

The two methods thus provide access to very different time frames within the life history of an animal. Using both methods in reconstructing the diet of fossil herbivore is thus expected to allow inference on seasonal variation as well as average dietary signals and also allow to merge both and calibrate mesowear for seasonality and vice versa.


The extended mesowear technique

The mesowear method was introduced by Fortelius & Solounias (2000) as an efficient and easy way of ranking a species diet within a spectrum of extant ungulate species that vary from dedicated browser to dedicated grazer. The mesowear method treats ungulate cheek tooth mesowear as two variables: occlusal relief and cusp shape. The sharper buccal cusp of the second upper molar (either the paracone or the metacone) is scored. Occlusal relief is classified as high (h) or low (l), depending on how high the cusps rise above the valley between them. Negative relief (cusp tip lower than sides) is sometimes seen in hypsodont equids, and is treated as low. The second mesowear variable, cusp shape, includes three scored attributes: sharp (s), round (r) and blunt (b) according to the degree of facet development. A sharp cusp terminates to a point and has practically no rounded area between the mesial and distal phase I facets, a rounded cusp has a distinctly rounded tip (apex) without planar facet wear, but retains facets on the lower slopes, while a blunt cusp lacks distinct facets altogether. We only use specimens in which the last molar is in occlusion and the first molar retained an occlusal shape similar to the second molar i.e. adults individuals. Consequently, the effect of age is minimized. The progressive blunting of a cusp will inevitably reduce occlusal relief. That is to say, cusp shape and relief are not entirely independent, but converge at the low and blunt ("grazer") end of the spectrum. Rivals et al. (2007) proposed a standardization of the method by developing a mesowear scale combining both cusp relief and cusp shape using extant ungulates of known diet.

Mesowear parameters scored are subsequently databased. The comparison with modern species will be done using the mesowear database of extant species elaborated by Fortelius & Solounias (2000). Recent ungulate taxa representing corresponding dietary preferences will thus be identified for each population investigated. The mesowear method has been extensively tested by Kaiser et al. (2000) and has been developed further by Kaiser & Solounias (2003) allowing also small samples to be investigated.

Microwear methodology

Examination of microwear is done on the second enamel band of the paracone of the upper M2 (Figure 1). Transparent epoxy casts are examined at 35x magnification using a stereomicroscope. Upper M2 paracones are analysed in teeth where M1-M3 are in occlusion. Such animals are more likely to have been eating representative foods before they died than young or old. Under the light microscope, pits and scratches are identified and counted within a standard 0.4 mm x 0.4 mm square area. Two representative enamel locations on the second band of enamel of the paracone (the crest adjacent to the central cavity as opposed to the most buccal band) are counted to standardize the methodology. This procedure is used because microwear is somewhat variable on a single tooth. The selected second band used here is intermediate in terms of the amount of wear features observed.

The number of pits versus scratches for individuals per taxon is recorded in two locations on the same enamel band. The two counts per paracone (per individual cast) are then averaged to obtain a mean number of pits and scratches per cast. New microwear characters are scored with the intent of providing a mechanism to further refine the dietary categorization of ungulates beyond the broad categories of browser versus grazer versus mixed feeder. Thus, the quantity of large versus small pits is also scored by noting if more than four large pits are present or absent per microscope field. Small pits are very regular in appearance with sharp, distinct borders, being circular in nature and very refractive or shiny (and bright). Large pits are deeper, less refractive (always dark), generally at least about twice the diameter of small pits, and often have less regular outlines than do small pits but are still generally circular. Scratches are also distinguished according to their geometry and frequency (e.g. purely coarse scratches, purely fine scratches, or a mixture of both types). Fine scratches are defined as those scratches that appear the narrowest, they are relatively shallow and have lower refractivity (are duller) than do coarse scratches. Coarse scratches are defined as those scratches that appear the widest, they are also relatively deep and have high refractivity (relatively shiny). The mixed scratch category is based on the finding of a high percentage of both fine and coarsely textured scratches in the same enamel band. The presence or absence of more than four cross scratches per microscope field is also recorded. Cross scratches have been noted in prior microwear studies and are defined here similarly as those scratches which are oriented somewhat perpendicular to the majority of scratches observed on dental enamel. Some enamel bands show microwear scars that are quite distinct from pits but are still fairly circular when located within the enamel band proper. These features are here called "gouges". Gouges in enamel are rarer than pits but are very distinctive when present. They have ragged, irregular edges and are much larger (approximately 2-3 times as large) and deeper than large pits. They are relatively dark features with low refractivity and are most often observed on the edges of the buccal side of the second enamel band (enamel band one and four shows little gouging). The presence or absence of gouges in a microscope field is recorded.

Data from each individual tooth therefore consisted of the following variables:
1. Average number of pits
2. Average number of scratches
3. Percentage of individuals per taxon displaying more than four large pits per field
4. Percentage of individuals with more than four cross scratches per field
5. Percentage of individuals per taxon with fine versus coarse versus a mixture of fine and coarse scratches
6. Percentage of individuals per taxon with gouges present.

To assess our fossil species to a dietary category we use a microwear database of 50 extant species developed by Solounias & Semprebon (2002).

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