Paleobiology, 29(2), 2003, pp. 230±242 Stable isotopes, hypsodonty, and the paleodiet of Hemiauchenia (Mammalia: Camelidae): a morphological specialization creating ecological generalization Robert S. Feranec Abstract.ÐMorphological adaptations may indicate increased specialization (narrowing of ecolog- ical niche) or expansion of the suite of lifestyles available to an organism (increasing niche breadth). Hypsodonty in mammals generally has been interpreted as a specialization into a grazing niche from a browsing niche. Here I examine the feeding strategy of the extinct hypsodont camel Hem- iauchenia through an analysis of stable carbon isotope values from its tooth enamel, which was used to clarify its feeding strategy and to resolve con¯icting interpretations of dental versus muzzle attributes. The paleodiet of Hemiauchenia is then used to test whether hypsodonty correlates to graz- ing within fossil Lamini. This study focuses on fossils from Florida, which is geographically ideal because unlike other regions of the country almost all extant plants on which animals browse use the C3 photosynthetic pathway. In contrast, most of the grasses and sedges utilized by grazers use the C4 photosynthetic pathway. If Hemiauchenia was an obligate grazer, the stable carbon isotope values of tooth enamel should re¯ect primarily a diet of C4 grass and sedge (.21.3½). If Hem- iauchenia was mainly a browser, the isotopic value should be considerably more negative re¯ecting 13 ingestion primarily of C3 browse (,27.9½). The mean d C values for Hemiauchenia during each time interval average more negative than 28.0½, indicating a dominantly C3 browse diet, and there is no evidence for abandonment of the browsing niche from the Hemphillian through the Ran- cholabrean North American Land Mammal Ages. However, an increase in the range of isotopic values indicates a diet with a higher proportion of C4 grasses and sedges through time. This study therefore suggests that Hemiauchenia was a hypsodont intermediate feeder with preference for browse during the past 5 million years. Hypsodonty is not strictly associated with obligate grazing; instead it may, in this case, represent an adaptation to widen niche breadth that allowed grazing as well as browsing. Robert S. Feranec. Department of Integrative Biology and Museum of Paleontology, University of Califor- nia, Berkeley, California 94720. E-mail: [email protected] Accepted: 31 October 2002 Introduction niche breadth by simply adding the ability to Determining the diet of ancient animals has graze. At issue is whether extinct hypsodont important implications for interpreting paleo- animals were obligate grazers, or whether community structure. For example, determin- they continued to utilize browse plants in sig- ing whether extinct herbivores are browsers, ni®cant quantities and added a grazing com- intermediate feeders, or grazers is required to ponent to their feeding strategy. understand details of resource partitioning, Because fossils are rarely preserved with which ultimately in¯uences diversity in eco- any direct physical evidence of diet, indirect systems by affecting competition and allow- proxies are commonly used to assess feeding ing for the co-occurrence of species (Hutch- strategies. Dietary proxies include morpho- inson 1958). The interpretation of feeding logical characteristics of the skull, such as strategy for ungulates is that there was a pro- hypsodonty of teeth and shape of the muzzle. gression through a pathway from browsing to Such data, however, can lead to con¯icting in- intermediate feeding to grazing, with the an- terpretations of diet (Webb 1974; Dompierre cestral state in diet being browsing and the and Churcher 1996). A prime example of this derived state being grazing (Perez-Barberia et con¯ict involves the feeding ecology of Hem- al. 2001). What has been unclear, however, is iauchenia. Hemiauchenia is an extinct genus of whether increasing hypsodonty indicates in- llama that ranged from the late Barstovian (ca. creased specialization for abrasive foods at the 13 Ma) to the late Rancholabrean (ca. 0.01 Ma) expense of browse, or an actual broadening of North American Land Mammal Ages (NAL- q 2003 The Paleontological Society. All rights reserved. 0094-8373/03/2902-0006/$1.00 PALEODIET OF HEMIAUCHENIA 231 MA) in North America (Honey et al. 1998). grasses and sedges; intermediate feeders, which This genus has been suggested to comprise have a composite diet of grasses and sedges, only browsers, according to morphological and browse. These three categories have been characteristics of the snout (Dompierre and adopted in much of the paleoecological liter- Churcher 1996), or to include intermediate ature for interpretation of paleoungulate diets, feeders with a preference for grasses, accord- and for use in paleoenvironment interpreta- ing to the presence of hypsodont teeth and tion (e.g., Janis 1988; Quade et al. 1992; So- abundant cementum (Webb 1974; Webb and lounias et al. 1995; MacFadden and Cerling Stehli 1995). This study uses stable carbon iso- 1996; Janis et al. 2000). In using these three cat- topes and measures of hypsodonty to deter- egories alone, much of the complexity in feed- mine the feeding strategy employed by Hem- ing in ungulates is obscured; for example, an iauchenia during the past 5 million years. The intermediate feeder does not necessarily have results are then used to assess whether the at- a diet midway between a browser and a graz- tainment of hypsodonty within the Lamini er. Hofmann and Stewart (1972) suggested evolved through the progression of browsing further subcategories within the three main to intermediate feeding to grazing, and categories to re¯ect some of this complexity. whether hypsodont animals are specialized Thus, concentrate selectors can be subdivided grazers. into tree and shrub foliage eaters and fruit and di- cot foliage eaters. Bulk and roughage feeders in- Background Information clude the subcategories roughage grazers, fresh As mentioned above, hypsodonty and the grass grazers, and dry region grazers. Within in- shape of the ungulate muzzle are but two termediate feeder are the subcategories prefer- morphological proxies used to interpret pa- ring grasses and preferring forbs, shrubs, and tree leodiet. Generally, more hypsodont animals foliage. However, these subcategories are sel- tend to feed on grasses and live in open hab- dom used in paleobiological studies because it itats. Because the spread of grasslands during generally is dif®cult to determine the percent the Miocene appears roughly coincident with of a particular forage type within the diet of widespread hypsodonty, it has been hypoth- an extinct ungulate. Whereas one can observe esized that hypsodonty evolved as a coevolu- the forage and droppings of modern ungu- tionary response to the spread of phytolith- lates, it is often dif®cult or impossible to link laden grasses, and as an adaptation to deal paleobotanical remains and/or coprolites to with grit and dirt that typically coats plants in particular extinct animals. However, as is ex- open habitats (McNaughton et al. 1985; Janis plained below, in a restricted geographical 1988, 1989, 1995; MacFadden 1997). With re- area in which the ¯ora is relatively well spect to the shape of the muzzle in ungulates, known, the analysis of stable carbon isotopes grazers have a broad muzzle capable of feed- in the tooth enamel of extinct herbivores pro- ing on large quantities of low-lying forage, vides a means for determining the percentage and browsers generally have narrow muzzles of certain forage in the diet. This proxy can be for manipulating through branches to select used to distinguish browsers, grazers, inter- choice, succulent forage. Intermediate feeders mediate feeder with a preference for grasses generally have muzzle widths in between and sedges, and intermediate feeder with a (Janis and Ehrhardt 1988; Solounias et al. preference for browse. 1988; Dompierre and Churcher 1996). Carbon Isotopes and Diet. The carbon iso- Modern Ungulate Feeding Categories. Hof- tope values of fossil teeth are useful in paleo- mann and Stewart (1972) used forage com- diet studies because different photosynthetic position and stomach structure, to character- pathways impart different ratios of 13C/12Cin ize modern ungulate feeding strategy into different kinds of plants, which are ultimately three main types: concentrate selectors (brows- re¯ected in the animals that eat them. Plants ers), which focus feeding on ¯ora other than can be grouped into three main photosyn- grasses and sedges (browse); bulk and roughage thetic pathways: C3,C4, and Crassulacean feeders (grazers), which concentrate feeding on Acid Metabolism (CAM). Tropical, warm-sea- 232 ROBERT S. FERANEC son sedges and grasses using the Hatch-Slack aceae, and up to 43% for Cyperaceae [Teeri photosynthetic pathway (C4) are enriched in and Stowe 1976; Teeri et al. 1980; Sage et al. the heavy carbon isotope (13C). Conversely, 1999]). Two studies of modern ¯oral compo- Calvin cycle plants (C3), including most sition on sites near fossil localities within this browse and high-latitude grasses, are en- study show that even though C3 grasses and riched in the light carbon isotope (12C). The sedges may be present and represent up to third pathway, the CAM pathway, is charac- 40% of the species richness of grasses, C3 teristic of succulents and incorporates inter- grasses are generally con®ned to wet and mediate ratios of 12Cand13C (O'Leary 1988; marshy areas