DA and DT led to the identification of a simple morphological pattern that allows a good discrimination between ungulate species that feed in open, mixed and closed habitats (Fig. 1). According to this pattern, the HI seems to play a major role in the adaptation of ungulates to habitats with different degrees of tree coverage. The bivariate plot of Fig. 1 shows that, with the only exception of several species with specific ecological adaptations (e.g. high-level browsers; see below), HI allows an almost complete discrimination between ungulates from forest (HI≤2) and those from open and mixed environments (HI≥2). HI does not discriminate the species from open and mixed habitats because the minimum threshold of hypsodonty for feeding in open habitats increases with the relative length of the anterior part of the jaw (JLB, size-adjusted distance between the base of the first incisor and the limit between the premolars and molars). Thus, what makes possible a good characterization of those ungulates adapted to feed in habitats with different degrees of tree coverage is a combination of HI and JLB (Fig. 1).
There is a group of species, however, which, according to their low values of HI, could be tentatively identified as forest species, although most of them live in open or mixed habitats. They cluster in the bottom-right region of the morphospace depicted in Fig. 1. Among them, the giraffe Giraffa camelopardalis, the dibatag Ammodorcas clarkey and the gerenuk Litocranius walleri live in open habitats and eat leaves at high levels above the ground. Although there are no data on grit and dust contents in the vegetation that grows at high and ground levels in open habitats, it is not unreasonable to expect lower levels of exogenous abrasives accumulating on tree leaves than on near-ground shrubs and herbs (Janis, 1988). This suggests that the difference in hypsodonty between high-level browsers and other ungulates from open habitats is motivated by differences in the amounts of airborne grit (Williams & Kay, 2001; Mendoza et al., 2002). Two other high-level browsers of this region of the morphospace, the okapi Okapia johnstoni and the moose Alces alces, inhabit forest. Another species with high JLB and low HI values is the mountain tapir Tapirus pinchaque, which lives in forests and grasslands. This species mainly eats leaves of the myrtle tree, which grow far from the ground and probably also accumulate less grit. The caribou Rangifer tarandus inhabits subarctic (boreal) forest regions, but also lives in the arctic tundra; therefore, it was classified in the mixed tree-coverage category. Given that the snow covers the ground in the arctic tundra during part of the year, grit and dust do not accumulate on the plants consumed by caribous. Finally, the marsh deer Blastocerus dichotomus, the Chinese water deer Hydropotes inermis, the Baird's tapir Tapirus bairdii and the Indian rhino Rhinoceros unicornis live in grasslands or both in grasslands and forests, but they are usually found in marshy, swampy ground with standing water or waterside habitats. There are no data on the amounts of airborne grit adhering to the surface of riparian plants. However, given that they are frequently submerged, it is reasonable to expect lower levels than in the vegetation that grows in drier habitats. Riparian plants, however, are loaded with concentrations of phytoliths similar to those found in the vegetation from shrub steppes and savannas (Bremond et al., 2005). Therefore, the low hypsodonty of those ungulates that feed on riparian plants supports the hypothesis that higher silica levels did not play an essential role in the evolution of hypsodonty.
The Indian rhino is the only riparian species with a relatively short anterior part of the jaw. However, other species of rhinos of open habitats such as the browsing black rhino Diceros bicornis and the grazing white rhino Ceratotherium simum also show very short anterior parts of the jaw (see Fig. 1). This morphological trait could be related to the fact that rhinos take food with their prehensile lips instead of using the incisor teeth.
The craniodental morphology of the common hippo Hippopotamus amphibius and the pygmy hippo Hexaprotodon liberiensis is unique among the living ungulates. Although both species live in different habitats, they have a very short anterior part of the jaw and brachydont teeth. In the case of Hi. amphibious, the reason for its low hypsodonty (which probably also applies to He. liberiensis) is most likely that it has a low metabolic rate, consuming less food per day than would be expected for an animal of its body size (Nowak, 2001). This means that the total amount of wear on the teeth is correspondingly less (Mendoza et al., 2002). In addition, hippos feed in or near water habitats on grasses that are probably less abrasive as a result of being frequently immersed in water (Mendoza et al., 2002). Moreover, a recent study of the isotopic composition of enamel in several populations of Hi. amphibious has shown that hippos have a more varied diet than usually believed, including significant amounts of C3 plants in closed to moderately open environments (Boisserie et al., 2005).
Two other species that have specific ecological adaptations also show a combination of low HI and high JLB values: the mule deer Odocoileus hemionus and the white tailed deer Odocoileus virginianus. Both live in an extremely wide range of habitats in North America, including deserts, grasslands, chaparral, forests, mountains, rainforests, scrub forest and swamps. Thus, their low hypsodonty cannot be explained by the absence of grit on the plants consumed.
Finally, there are two ungulates that show an unexpected combination of HI and JLB values in relation to the degree of tree coverage of their habitat: the European bison Bison bonasus and the lowland anoa Bubalus depressicornis. The European bison, also called the wisent, is the largest herbivore in Europe. Historically, the wisent was distributed through western, central and south-eastern Europe, but its range was severely shortened by the beginning of the 20th century, and now only small populations remain in a few isolated areas. The largest concentration lives in the temperate coniferous forests of Bialowieza Natural Park in Poland, and so the wisent was classified as a closed forest dweller. Although wisents browse in this closed habitat, they graze where grasses are available. In fact, Borowski & Kossak (1972) revealed that in wisents, leaves and shrubs constitute 33% of the diet, while grasses, sedges and herbs comprise up to 67% of the diet. Analysis of the rumen contents has confirmed that the wisent's basic diet contains grasses, sedges and herbs, which constitute 90% of the rumen capacity (Gebczynska, Gebczynski & Martynowicz, 1991). Wisents living in anthropogenic landscapes feed mostly on grass and agricultural crops, and browse usage is restricted mainly to winter (Balciauskas, 1999). Among modern ungulates, there are no grazing species in closed, forested habitats. This suggests that the European bison probably evolved in grasslands or mixed habitats.
The lowland anoa B. depressicornis also shows the craniodental morphology of an ungulate from an open habitat (Fig. 1). Little is known about the original habitat and feeding behaviour of this domesticated bovid, although it is thought to be a solitary browser that inhabits lowland forests, including secondary formations and swampy areas, and it was once common along the coasts (Whitten, Mustafa & Henderson, 1987). However, a recent study of diet digestibility and ingesta passage times in captive anoas has revealed a comparatively high fibre digestibility and high selective particle retention in the forestomach, which suggests that this species is adapted to feed significant amounts of grasses (Flores-Miyamoto et al., 2005). In addition, its jaw morphology is the one typical of a grazer. Thus, the combination of HI and JLB values depicted by the lowland anoa, typical of those ungulates from open environments, could reveal the original habitat of this species before its domestication.
The representation of the taxonomic affinities of the species in the morphospace of HI and JLB (Fig. 1) shows that the patterning is not related to the phylogeny. Some ungulate families are only present in one of the categories (e.g. equids and tragulids) and do not allow testing whether the phylogenetic legacy hides the adaptive morphological patterns. Other families, however, are mostly represented in one of the ecological categories but have one or two species that belong to another guild. The warthog Phacochoerus aethiopicus is perhaps the clearest example: it is the only suid that lives in open habitats, feeding mainly on grasses (Harris & Cerling, 2002), and is clearly more hypsodont than the other suids, which all dwell in forests and show the typical morphology of closed habitat species (Fig. 1). Cervids are present in the four ecological categories, and all of them are correctly classified. Only two species forage in open habitats: the chital Axis axis and the pampas deer Ozotoceros bezoarticus. Even the pampas deer, which has one of the most brachydont dentitions among the species of open and even mixed habitats (Mendoza et al., 2002), is correctly classified because it also has a very short anterior part of the jaw (Fig. 1). The short-crowned teeth of O. bezoarticus and its bordering position could evidence that the habitat of the pampas deer also includes areas temporarily inundated by fresh or estuarine waters (Jackson, 1987). The moose is the only high-level browser among cervids and combines brachydont teeth with a long anterior part of the jaw, characteristic of the ungulates with this particular feeding behaviour. Bovids, the most diverse family among extant ungulates, are represented by 72 species in the dataset, and these species are present in the four ecological categories. It is worth noting that if they are represented alone (not shown here), the same morphological pattern emerges as in the case of all ungulates. All these cases provide clear support to the adaptive origin of the HI–JLB pattern, ruling out the effects of phylogeny and the possibility of a random patterning.
The use of DTs led to the identification of another simple morphological pattern (Fig. 2), which involves HI combined with the relative width of the muzzle (MZW, size-adjusted distance between the outer junctions of the boundary between the maxilla and premaxilla). Muzzle shape reflects the adaptations related to the ‘cropping mechanism’ of ungulates: selective browsers have narrow, pointed muzzles consisting of a rounded incisor arcade with the first incisor generally larger than the third; in contrast, grazers have broad, square-shaped muzzles with transversely straight incisor arcades, showing equal or sub-equal-sized incisor teeth. These features reflect decreasing selectivity in food foraging (Gordon & Illius, 1988; Janis & Ehrhardt, 1988; Solounias & Moelleken, 1993).
Figure 2. Distribution of 134 extant ungulate species in the morphospace defined by the hypsodonty index (HI) and the relative width of the muzzle (MZW), which allows characterizing aspects of the craniodental morphology of grazers compared with non-grazing species, including mixed feeders, browsers and omnivores. White symbols: species from an open habitat; grey symbols: species from a mixed habitat; black symbols: species from a closed habitat; dotted symbols: species with special adaptations (see legend of Fig. 1). For a description of the morphological variables, see text and fig. 1 in Mendoza & Palmqvist (2006b).
Download figure to PowerPoint
According to the pattern of Fig. 2, grazers have a wider muzzle than other ungulates from an open habitat. However, although this pattern provides an almost perfect characterization of the craniodental anatomy of grazers, their range of HI values (3.5–8.7) exhibits a considerable overlap (65% of species) with that of mixed feeders from an open habitat (HI=1.5–5.3). This suggests that the level of hypsodonty is a relatively poor indicator of the percentage of grass consumed. Therefore, the comparatively high HI values of grazers could reflect that most species of this dietary group live in open habitat, which would be the main factor determining the degree of hypsodonty. On the contrary, MZW does allow an almost perfect discrimination between grazers and other species from open habitats such as mixed feeders and browsers. However, given that some species from closed habitats also show wide muzzles, it is only a combination of MZW and HI that makes possible the characterization of grazers with respect to other ungulates.
Browsers and mixed feeders from open habitats show, in general terms, a narrower muzzle than those species from mixed and closed habitats. In fact, with only the exception of the grey rhebok Pelea capreolus, the few browsers that live in habitats without tree coverage have some of the narrowest muzzles among ungulates, visibly narrower than in the browsing and mixed-feeding species from forest (Fig. 2). This could reflect a higher selectivity of food, as the plants from open habitats (e.g. acacia trees) are tougher and thornier than those that grow in forested environments. However, while MZW is a good indicator of a grazing diet for those species from open and mixed habitats, it is not an ecological indicator of open habitats (Fig. 2).
Figure 2 shows that the common hippo has a remarkably wide muzzle, which reveals its grazing habits, and brachydont teeth. As explained above, its short-crowned teeth are not typical of a grazer from open habitats and may result from the low metabolic rate of this species.
The common rhebok shows a muzzle width typical of a mixed feeder from an open habitat (Fig. 2). It is, however, predominantly a browser, as faecal analysis shows that dicotyledonous material comprises 88% of its diet (Mills & Hes, 1997). This species lives among rocks and tangled growth on mountain sides and plateaus. However, where protected it ventures to grassy valleys and probably frequented such valleys regularly before being driven out by human activity (Nowak, 2001). This recent change in habitat could have translated into an increase in browsing. In addition, the subspecies known as Vaal Rhebuck shows a mixed diet of grasses and leaves (Nowak, 2001), which indicates that the craniodental morphology of this species also allows regular consumption of grass.
The white rhino is a typical grazer, but its muzzle is relatively narrower than in most mixed feeders (Fig. 2). This can be a consequence of its strategy for food foraging, as the wide, square-shaped lips of white rhinos are ideally suited for swathing short grasses.
Finally, the lowland anoa and the European bison show the typical muzzle morphology of those grazing ungulates that forage in an open habitat (Fig. 2), although both species live, at present, in forested areas. Therefore, these results confirm their adaptation to graze in open environments.