Dental microwear texture analysis of two families of subfossil lemurs from Madagascar

Journal of Human Evolution 56 (2009) 405–416

Contents lists available at ScienceDirect

Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol

Dental microwear texture analysis of two families of subfossil lemurs from Madagascar J.R. Scott a, L.R. Godfrey b, W.L. Jungers c, R.S. Scott d, E.L. Simons e, M.F. Teaford f, P.S. Ungar g, *, A. Walker h a

Environmental Dynamics Doctoral Program, University of Arkansas, 113 Ozark Hall, Fayetteville, AR 72701, USA Department of Anthropology, University of Massachusetts, 240 Hicks Way, Amherst, MA 01003, USA Department of Anatomical Sciences, Health Sciences Center, School of Medicine, Stony Brook University, Stony Brook, NY 11794, USA d Department of Anthropology, Rutgers, State University of New Jersey, New Brunswick, NJ 08901, USA e Division of Fossil Primates, Duke Primate Center, 1013 Broad Street, Durham, NC 27705, USA f Center for Functional Anatomy and Evolution, Johns Hopkins University School of Medicine, 1830 E. Monument St., Baltimore, MD 21205, USA g Department of Anthropology, University of Arkansas, Old Main 330, Fayetteville, AR 72701, USA h Department of Anthropology and Biology, Pennsylvania State University, 409 Carpenter Building, University Park, PA 16802, USA b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 18 July 2008 Accepted 16 November 2008

This study employs dental microwear texture analysis to reconstruct the diets of two families of subfossil lemurs from Madagascar, the archaeolemurids and megaladapids. This technique is based on threedimensional surface measurements utilizing a white-light confocal profiler and scale-sensitive fractal analysis. Data were recorded for six texture variables previously used successfully to distinguish between living primates with known dietary differences. Statistical analyses revealed that the archaeolemurids and megaladapids have overlapping microwear texture signatures, suggesting that the two families occasionally depended on resources with similar mechanical properties. Even so, moderate variation in most attributes is evident, and results suggest potential differences in the foods consumed by the two families. The microwear pattern for the megaladapids indicates a preference for tougher foods, such as many leaves, while that of the archaeolemurids is consistent with the consumption of harder foods. The results also indicate some intraspecific differences among taxa within each family. This evidence suggests that the archaeolemurids and megaladapids, like many living primates, likely consumed a variety of food types. Ó 2008 Elsevier Ltd. All rights reserved.

Keywords: Diet Teeth Megaladapis Archaeolemur Hadropithecus

Introduction Diet is widely hypothesized to be a principal factor contributing to the differences between living primate species. For instance, it has been directly correlated with critical ecological factors such as group size and composition, habitat range, and even locomotion (Fleagle, 1999). With so many important elements of the primate niche tied to subsistence, it is no wonder that paleoprimatologists seek to learn all they can about the diets of past species. In fact, in addition to revealing information about critical aspects of the ecology of fossil taxa, dietary reconstructions help us understand the processes of evolution and extinction. The adaptive radiation of the lemurs of Madagascar provides a classic example of the potential usefulness of dietary

* Corresponding author. E-mail address: [email protected] (P.S. Ungar). 0047-2484/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2008.11.003

reconstruction. Geographic isolation and limited competition have made these forms the primate equivalent of Darwin’s finches. Extant lemurs are represented by more than 100 species within five families, with a substantive range of adaptations (see summary by Wright, 1999). But the subfossil record shows that this radiation was even more remarkable just a few hundred years ago. In fact, during the past two millennia, the range of their sizes, shapes, and adaptations was greater than that of the rest of the primate order (summarized in Godfrey and Jungers, 2002; Jungers et al., 2002). What were they like? What ecological niches on Madagascar did they occupy? These are questions that can best be addressed with careful reconstruction of their paleoecology, especially of their diets. Dental microwear is the study of microscopic scratches and pits formed on the surfaces of teeth as the result of use. Because of the direct relationship between the microwear and the material properties of foods and abrasives, analysis of dental microwear reveals important clues regarding the diet and ecology of fossil

406

J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416

species. Scratches on the tooth surface are associated with the shearing of tough foods, like most types of leaves, although some woody seeds can also be tough (Teaford and Walker, 1984; Teaford, 1988; Lucas, 2004, Lucas et al., 2008). Pits are indicative of hard food consumption, like many seeds (Strait, 1993; Silcox and Teaford, 2002). Dental microwear has been examined for both fossil and extant mammals representing a broad range of taxa, including primates (e.g., Jacobs, 1981; Rafferty and Teaford, 1992; Strait, 1993; Daegling and Grine, 1994; Lucas and Teaford, 1994; Teaford et al., 1996; Ungar, 1996, 1998; Ungar and Teaford, 1996; King, 2001; Rafferty et al., 2002; Leakey et al., 2003; Godfrey et al., 2004; Ungar et al., 2004, 2008; El Zaatari et al., 2005; Merceron et al., 2005a), perissodactyls (e.g., Hayek et al., 1991; MacFadden et al., 1999; Solounias and Semprebon, 2002; Kaiser et al., 2003), artiodactyls (e.g., Solounias et al., 1988; Solounias and Moelleken, 1993; Hunter and Fortelius, 1994; Rivals and Deniaux, 2003; Franz-Odendaal and Solounias, 2004; Merceron et al., 2004a,b; Semprebon et al., 2004; Merceron et al., 2005b; Merceron and Ungar, 2005; Merceron and Madelaine, 2006; Schubert et al., 2006; Ungar et al., 2007), rodents (Gutierrez et al., 1998; Lewis et al., 2000; Hopley et al., 2006), carnivorans (Van Valkenburgh et al., 1990; Anyonge, 1996), proboscideans (Capozza, 2001; Filippi et al., 2001; Green et al., 2005), and other taxa (Krause, 1982; Biknevicius, 1986; O’Leary and Teaford, 1992; Silcox and Teaford, 2002). Previous studies of dental microwear in subfossil lemurs have yielded differing results, particularly regarding the degree of dietary specialization in the Archaeolemuridae and Megaladapidae, as well as variation between species within these families (Rafferty et al., 2002; Godfrey et al., 2004). These studies used different methods of characterizing the enamel surface, looking at microwear features at entirely different scales, so it is possible that overlap might be reported using one method, but not the other. One of these studies, using conventional scanning electron microscope (SEM) based analysis, reported that Archaeolemur did not specialize solely on hard objects and that there were interspecific differences in diet and dental microwear for both families (Rafferty et al., 2002). By contrast, the other study, using low-magnification light microscopy, found no overlap between the Archaeolemuridae (which the authors classified as hard-object feeders) and the Megaladapidae (classified as folivores; Godfrey et al., 2004).

Previous reconstructions of diet Archaeolemur The dentitions of archaeolemurids are highly derived and have been the ultimate source of much debate concerning their diet. Archaeolemurids have large, spatulate incisors, bilophodont molars that converge on those found in extant cercopithecines, and upper and lower premolars that form a continuous shearing blade. Early reconstructions based on these features made analogies to modern baboons and suggested that the archaeolemurids were primarily fruit eaters with some hard-object feeding related to fruit selection (Tattersall, 1973, 1982). Recent studies of dental microstructure and dental development have refined these earlier hypotheses and assigned a more specialized hard-object diet to Archaeolemur (Ravosa and Simons, 1994; King et al., 2001; Godfrey et al., 2005). Like Cebus and Paranthropus, Archaeolemur has very thick and highly decussated enamel, two traits also thought to be related to hard-object processing, given expected shear forces across the joint, although Ravosa and Simons (1994) described variation in the ontogeny of this feature. Studies of fecal pellets associated with several individuals of Archaeolemur cf. edwardsi have, on the other hand, suggested a generalized and omnivorous diet, including fruit

and seeds, gastropods, arthropods, crustaceans, and small vertebrates (Burney et al., 1997; Vasey et al., in preparation). Dental microwear evidence has also been used to interpret the diet of Archaeolemur. A study of dental microwear using SEM techniques reconstructed this genus as having an eclectic diet based on the absence of clear diagnostic microwear features (Rafferty et al., 2002). Among the species of Archaeolemur, larger features were documented on the teeth of A. majori and A. cf. edwardsi, the northern variety of A. edwardsi. This was thought to indicate either ecogeographic variation in the incidence of hardobject feeding among the archaeolemurids or perhaps the importance of ‘‘fallback foods’’ in the diet of Archaeolemur (Rafferty et al., 2002). Low magnification light microscopy analysis of Archaeolemur microwear provided different results. Godfrey et al. (2004) found the Archaeolemuridae had dietary signatures that were not similar to any of those in extant lemurs, with the singular exception of some similarities to Daubentonia madagascariensis. They concluded that the Archaeolemuridae were frugivorous seed predators that regularly exploited hard objects. High frequencies of pitting on the enamel surface were documented, along with scratches that were classified as coarse and hypercoarse. The authors found examples of large pits on the teeth of all surveyed individuals, as well as features they described as puncture pits. No significant differences were found in use wear signatures between the two species of Archaeolemur. Hadropithecus Dietary reconstructions of Hadropithecus have varied, depending on the traits examined. Hadropithecus has large, thick-enameled molars that wear flat and relatively smaller anterior teeth, much like the dentition of the extant gelada baboon (Jolly, 1970; Tattersall, 1973). Jolly argued that the long forelimbs of H. stenognathus would have allowed it to sit on the ground and pluck grass from its surroundings, much like Theropithecus gelada today. This, combined with the dentition, suggested a graminivorous or granivorous diet for Hadropithecus to both Jolly (1970) and Tattersall (1973). These findings were later questioned based on new attributions of postcranial remains of Hadropithecus that demonstrated that the forelimbs were not nearly as elongated as Jolly hypothesized (Godfrey et al., 1997). Dental microwear evidence has been used to argue against the gelada baboon model. Although Hadropithecus material is rare and the sample size analyzed was therefore small, SEM-based study of microwear revealed a high overall incidence of features suggesting an abrasive diet (Rafferty et al., 2002). Occlusal surfaces were described as dominated by wide features, particularly scratches. The microwear surface of Hadropithecus bore no resemblance to the often compared Theropithecus and ruled out a grass-eating specialization. Low magnification light microscopy documented high pit frequencies on the enamel surfaces of Hadropithecus suggesting a close association with the hard-object feeder, Cebus apella (Godfrey et al., 2004). According to this study, Hadropithecus use-wear signatures are least like those of Theropithecus, the taxon to which these subfossil lemurs are most often compared. The authors documented similar surface features on the teeth of Hadropithecus and Archaeolemur: a high frequency of pits, puncture pits, coarse, and hypercoarse scratches. Hadropithecus, however, had even greater numbers of puncture pits than either of the Archaeolemur species. Thus, the authors suggested Hadropithecus was a more dedicated hard-object feeder. However, a recent study of dietary indicators including stable isotope analysis, relative enamel thickness, and orientation patch counts has suggested that the diet of

J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416

Hadropithecus might have been more like that of Theropithecus than previously thought (Godfrey et al., 2008). Megaladapis The megaladapids lack maxillary incisors and have molars that increase in size from anterior to posterior (Godfrey and Jungers, 2002). Members of the genus, along with other subfossil lemurs, also have a fused mandibular symphysis, a rarity in strepsirrhines. Their enormous teeth exhibit large shearing crests on the upper and lower molars, which led early researchers to conclude that Megaladapis was likely a folivore (Thenius, 1953). Tattersall (1975) also invoked a folivory model by comparing the Megaladapis jaw apparatus to that of extant Australian koalas. Based on dental morphology, Godfrey et al. (1997) posited up to 20% frugivory in all species of Megaladapis, with the majority of the remaining diet being accounted for by folivory. More recently, Jungers et al. (2002) calculated the shearing quotients of several species of Megaladapis and other extinct and extant lemurs, corroborating the inference of strong folivory in the former. Dietary reconstruction inferred using an SEM-based study of dental microwear confirmed the folivore label. The documented microwear features included narrow pits, a high incidence of narrow scratching, and a low overall frequency of pitting (Rafferty et al., 2002). The study suggested differences within the genus in degree of folivory, with M. grandidieri and M. madagascariensis, the smaller species, trending towards more varied diets. M. edwardsi was classified as a ‘‘hyper-folivore,’’ with narrow scratches and the lowest frequency of pitting recorded for any primate. Godfrey et al. (2004), using low magnification light microscopy, agreed that all Megaladapis species were leaf dominated browsers and compared them most closely to the extant genera Avahi, Lepilemur, and Alouatta. Their study found no evidence of hard-object feeding or seed predation, based on a lack of puncture pitting and a low incidence of pitting overall. They also found no significant differences between the species of Megaladapis, although M. edwardsi had slightly larger features and more pitting than the smaller species. Godfrey and co-authors suggested that this difference may be related to habitat, as M. edwardsi shared the spiny scrub forests of southern Madagascar currently occupied by Lepilemur leucopus, a species with similar use wear patterns. They also hypothesized that this variation, although not statistically significant, could be evidence for niche differentiation in the southern part of Madagascar, where M. edwardsi and M. madagascariensis overlap in range. This paper brings a new technique, dental microwear texture analysis, to bear on the study of subfossil lemur microwear, to provide a new set of results that may illuminate the issue of diet. This technique is automated and the results are repeatable when the same area of the facet is scanned. The technique also allows characterization of surfaces in three-dimensions over a continuous range of scales and operates at high resolution to facilitate the identification and exclusion of taphonomically damaged specimens (Scott et al., 2005, 2006; Ungar et al., 2008). Results should therefore allow an independent assessment of interspecific variation among the Archaeolemuridae and Megaladapidae, as well as interspecific differences within each genus. Methods We examined all identified species of archaeolemurids and megaladapids for this study. These included both species within the genus Archaeolemur: A. edwardsi (n ¼ 35), and A. majori (n ¼ 7). To test for the possibility of dietary differences between A. edwardsi from northern and central Madagascar, specimens from the two

407

geographic regions were analyzed separately. Although the sample size for A. majori is small, this taxon was included in the statistical analyses. Specimens for the only species within the genus Hadropithecus, H. stenognathus, were also examined, although only a small number (n ¼ 5) were without postmortem damage and suitable for microwear analysis. All species within the genus Megaladapis were also included: M. edwardsi (n ¼ 15), M. grandidieri (n ¼ 15), and M. madagascariensis (n ¼ 9). The specimens used in this study are housed at the American Museum of Natural History (AMNH), the British Museum of Natural History (BMNH), the Duke University Lemur Center (DUPC), the Acade´mie Malgache (AM), Vienna Naturhistorisches Museum (NHNW), Oxford University Natural History Museum (OXUM), and the University of Antananarivo (UA). Table 1 lists the included taxa and specimens used in the analysis. Data collection As in previous studies of dental microwear (see Teaford and Robinson, 1989; Teaford and Runestad, 1992), the maxillary second molar was used in the analysis whenever possible. When the maxillary tooth was unavailable or exhibited postmortem damage that obscured microwear, the second mandibular molar or first maxillary molar was substituted to maximize sample sizes, especially for rare subfossil material. Conventional SEM-based microwear studies have shown no consistent pattern of differences in upper and lower microwear pattern or between tooth types (Gordon, 1982, 1984; Teaford and Walker, 1984; Teaford, 1985, 1986; Grine, 1986, 1987; Bullington, 1991). Additionally, this study focused on the so-called ‘‘Phase II’’ facets (facets 9, 10 n, and x), as is usual for dental microwear analysis (Kay, 1977; Gordon, 1982; Teaford and Walker, 1984; Krueger et al., 2008). The criteria used for determining suitability for microwear analysis were those of Teaford (1988) and based on examination of the sides and occlusal surfaces of the teeth, and a ‘‘clean’’ enamel use-wear surface free of post mortem damage, coating, adhesive, or casting defects. The specimens used in this study came from two different collections and replicas were prepared separately by three of us (LG, WJ, and MT). High resolution replicas were prepared using conventional procedures (Ungar, 1996). Teeth were cleaned using either acetone or alcohol, and the crown surfaces were molded Table 1 Subfossil lemur specimens used in this analysis.a Archaeolemur cf. edwardsi: DUPC10850, DUPC10895, DUPC10903, DUPC11729, DUPC11744, DUPC11807, DUPC11819, DUPC11828, DUPC11829, DUPC11830, DUPC11883, DUPC6803, DUPC7849, DUPC7900, DUPC7927, DUPC7928, DUPC7943, DUPC7970, DUPC9104, DUPC9106, DUPC9890, DUPC9899, DUPC9907 Archaeolemur edwardsi: BMNH9909, BMNH9965, BMNH9966, BMNH9968, BMNH9969, BMNH9970, BMNH9972, OXUM5098, UA2769, UA2850, UA5135, UA6773 Archaeolemur majori: AMNH30007, DULCBB2, BMNH13923, BMNH7374, OXUM5099, UA2808, UA5377 Hadropithecus stenognathus: AM Display, AM6382, UA5170, Vienna 1934.IV.2, Vienna1934. IV.1/2 Megaladapis edwardsi: AM6031, AM6071, AM6143, AM6174, AMNH30024, AMNH30025, AMNH30027, AMNH30028, DUPC13663, BMNH13912, BMNH13916, BMNH13917, BMNH7370, BMNH7438, MMV Megaladapis grandidieri: AM6173, BMNH9917, BMNH9918, BMNH9920, BMNH9921A, BMNH9921B, BMNH9921C, BMNH9922A, BMNH9922B, BMNH9922E, BMNH9975, BMNH9976, BMNH9977, OXUM5101, OXUM5103 Megaladapis madagascariensis: BMNH4848, BMNH4849, DUPC11787, DUPC17218, DUPC18827, DUPC18935, DUPC18938, OXUM5105, UA5484 a AM ¼ Acade´mie Malgache, AMNH ¼ American Museum of Natural History, BMNH ¼ British Museum, Natural History, DUPC ¼ Duke University Lemur Center, UA ¼ University of Antananarivo, OXUM ¼ Oxford University Natural History Museum, UA ¼ University of Antananarivo, Vienna ¼ Vienna Naturhistorisches Museum.

408

J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416

with President’s Jet Plus polyvinylsiloxane Regular Body Dental Impression Material (Colte`ne-Whaledent). Casts were then poured using clear Epotek 501 epoxy resin and hardener (Epoxy Technologies). Because white-light confocal microscopy uses white-light to probe the tooth surface instead of electrons, it was not necessary to mount replicas on stubs or to coat them with a conductive metal as would be required for SEM. Facet 9 of each specimen was scanned using a Sensofar Plm white-light confocal imaging profiler (Solarius Development Inc., Sunnyvale, California). This instrument was used because of its ability to collect accurate 3D point clouds from the surface of wear facets to generate digital elevation models. Elevations are measured at set x and y intervals, allowing for the construction of a 3D matrix (Ungar et al., 2003; Scott et al., 2005, 2006). A 100x objective was used to generate a point cloud for each surface with a lateral sampling interval of 0.18 mm, a vertical resolution of 0.005 mm, and a field of view of 138  102 mm. We collected data for four adjoining fields to sample a larger area of about 276  204 mm. The scans were then leveled using Solarmap Universal software (Solarius Development Inc., Sunnyvale, CA). Defects such as dust or other adherents were removed using the erase function in Solarmap and slope-filtering in Sfrax (Surfract, www.surfract.com). Resulting data files were saved in .sur format for analysis using scale-sensitive fractal analysis software (see Scott et al., 2006 for details). Scale sensitive fractal analysis Point cloud data files were analyzed using Toothfrax and Sfrax programs (Surfract, www.surfract.com). This approach has been used for a wide variety of industrial applications including adhesion analyses and food texture studies (Kennedy et al., 1999; Pedreschi et al., 2000, 2002; Brown and Siegmann, 2001; Zang et al., 2002; Jordan and Brown, 2006), as well as dental microwear analysis (Ungar et al., 2003, 2007, 2008; Scott et al., 2005, 2006). Scale-sensitive fractal analysis takes its origin from studies of fractal geometry. It is based on the principle that the texture of a surface changes with the scale at which it is observed. The apparent profile length of a surface, the apparent area of that surface, and the apparent volume of features on it change with the scale of observation. This means a surface that appears to be smooth when viewed at a coarse scale may be demonstrably rough at finer scales. Changes in apparent texture at different scales can be examined for profiles across a surface (length-scale analysis), or whole surfaces (area-scale and volume-filling vs. scale analyses). Several texture variables of potential value to microwear researchers have been identified (Ungar et al., 2003; Scott et al., 2005, 2006). We present data for five of these here: complexity, scale of maximal complexity, anisotropy, textural fill volume, and heterogeneity. Values for individual surfaces are reported as medians of the four fields sampled following Scott et al. (2006). The texture variables used in this study have been described at length (Ungar et al., 2003, 2007, 2008; Scott et al., 2005, 2006) and can be summarized briefly here (see Table 2). Complexity (Asfc). Area-scale fractal complexity is defined in terms of change in surface roughness at different scales. Asfc is the slope of the steepest part of a curve fit to a plot of relative area versus scale over the range of scales at which those measurements are made. The steeper the slope, the more complex the surface. Pits and scratches of different sizes overlaying one another would generally result in a more complex surface (Ungar et al., 2008). Complexity has been used successfully to distinguish, among other things, primates that eat harder foods from those that consume tougher foods. For example, Scott et al. (2005) demonstrated that Cebus apella, known for a diet of fruit flesh and hard objects

Table 2 Dental microwear texture variables, definitions, and examples. Variable Definition Asfc Smc

epLsar

Tfv Ftfv HAsfc

Example

Surface complexity

Pits and scratches overlapping one another would represent a complex surface Scale of maximum A surface dominated by large pits with an complexity absence of complexity of fine scratches would have a high value for Smc Anisotropy A surface dominated by scratches all running in the same direction would have a high epLsar value Textural fill volume A surface dominated by deep features like pits would have a high Tfv value Fine textural fill volume A surface dominated by deep features like pits volume would have a high Ftfv value Heterogeneity A surface with variable patterns of pitting and scratches across a facet would have a high HAsfc value

like some seeds, has higher and more variable Asfc values than Alouatta palliata, with its diet of leaves and other tough food items (also see Ungar et al., 2003). Based on previous reconstructions of diet, we expected that the archaeolemurids would have higher values for Asfc than the megaladapids. Scale of maximum complexity (Smc). Previous studies using scale-sensitive fractal analysis have suggested that the scale range over which Asfc is calculated may also be informative (Scott et al., 2005, 2006). Asfc is calculated for the scales where the relative area versus scale curve is steepest. These scales yield the scale of maximum complexity (Smc). Surfaces with greater values for Smc will tend to have less wear at very fine scales and/or more wear features at coarser scales. For instance, a surface dominated by large pits with an absence of fine scratches might have a high Smc. We predicted that the archaeolemurids would have higher values for Smc than the megaladapids. Anisotropy (epLsar). Length-scale anisotropy of relief is a measure of orientation concentration of surface roughness. Surface anisotropy is calculated by taking profiles of the microwear surface at different orientations; in this case, five degree intervals ‘‘around the clock.’’ When the surface is highly anisotropic, the relative lengths of the profiles differ with orientation. Relative lengths at given orientations can then be defined as vectors. The normalized relative length vectors form a rosette diagram when displayed graphically and the length of the mean of these vectors is a measure of surface anisotropy. A surface dominated by scratches all running in the same direction would have a high epLsar. The epLsar measure has been used to distinguish between primates with tough and hard diets. For example, Scott et al. (2005) showed that the tough food consumer, Alouatta palliata has significantly higher anisotropy values than the hard-object feeder, Cebus apella. They used this distinction to suggest that hard foods that can be associated with pits leave a complex microwear pattern, while tough, fibrous foods associated with scratches produce a more directional pattern. Based on previous reconstructions of diet, we expected that the megaladapids would have higher values for epLsar than the archaeolemurids. Textural fill volume (Tfv, Ftfv). The textural fill volume algorithm examines the summed volume of square cuboids of a given scale that fill a surface. Textural fill volume can be computed on a coarse (Tfv) or fine scale (Ftfv). Tfv is computed as the difference in summed volume for fine cuboids (for this study 2 mm on a side) and larger ones (for this study 10 mm on a side). This removes the structure of the overall surface (e.g., facet curvature), limiting characterization to the microwear features themselves. A surface that is dominated by more features in the mid scale range is expected to have a high Tfv.

J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416

Tfv has also been suggested to have the potential to distinguish between primates that consume foods with different fracture properties. Cebus apella, for example, has high values for Tfv, a reflection of the higher pit count on the surface. Tough food consumers that rely on leaves may have lower Tfv values that correspond to the fine, scratched microwear surface these foods produce. We expected that the archaeolemurids would have higher values for Tfv than the megaladapids. Heterogeneity (HAsfc). As discussed in the above sections, variables including surface complexity, roughness, and anisotropy can provide accurate descriptions of microwear surfaces. However useful these might be, adjoining scans of the same surface can vary in their values for each variable. In fact, the amount of variation in complexity, roughness, and anisotropy across a facet or even a single scan may be important in characterizing the microwear surface. Heterogeneity of area-scale fractal complexity (HAsfc) is calculated by splitting individual scanned areas into successively smaller subregions given equal numbers of rows and columns. This algorithm is performed by using the Auto-Split function in the Toothfrax software. HAsfc is calculated by splitting each individual scan into smaller sections with equal numbers of rows and columns. The scans are divided first into 2  2 and into increasingly smaller sections up to 11 11. Resulting distributions are typically skewed, so the relative variations in complexity for each set of subregions were calculated as the median absolute deviation of Asfc divided by the median of Asfc. Based on previous reconstructions of diet, we expected that the archaeolemurids would have higher values for HAsfc(9) and HAsfc(81) than the megaladapids. Statistical analyses were performed to determine the extent of variation in microwear texture among taxa following Ungar et al. (2006, 2008). All data were rank-transformed before analysis (Conover and Iman, 1981) because unranked microwear data typically violate assumptions associated with parametric statistical tests. Data for the variables were compared among species using a multivariate analysis of variance model, with taxon as the factor, Asfc, Smc, epLsar, Tfv, HAsfc(9), and HAsfc(81) as the dependent variables, and values for each individual as the replicates. This test assesses significance of variation among the taxa in overall microwear surface texture. Single classification ANOVAs for each variable and multiple comparisons tests were used to determine the sources of significant variation (but see Enders, 2003; Keselman et al., 1998 for alternate approaches to analysis). Because these groups were chosen for their dietary (and expected microwear) differences, Fisher’s LSD a priori tests were used to compare species. Tukey’s HSD post hoc tests were also run to balance risks of Type I and Type II errors (Cook and Farewell, 1996). Results Examples of microwear surfaces for each taxon are illustrated in Figure 1. Figure 2 shows three-dimensional renderings of surfaces for both families. Results suggest differences between the two families and between the species within the families for at least some of the tested texture variables. Both Wilks’ l and Pillai Trace results indicated significant variation in the model. The archaeolemurids tended to have surfaces dominated by larger features, usually pits, with low anisotropy and moderate heterogeneity. The megaladapids, in contrast, more often had surfaces dominated by scratches of varying sizes and depth, with high anisotropy and moderate heterogeneity. Thus, the two families seem to fall into two clusters (Fig. 3), with some overlap between them. Individual ANOVA results indicate that the archaeolemurids have significantly higher Asfc, Tfv, and Ftfv than do the megaladapids (Table 3).

409

Some differences are also evident within each of the families. For example, both the central and northern variants of A. edwardsi tend to have smaller, shallower features than A. majori and H. stenognathus. Further, M. edwardsi tends to have smaller, shallower features than the other megaladapids. These visually apparent differences are confirmed by statistical analyses (Table 4). Tukey’s test results indicate significant differences between A. cf. edwardsi and A. majori in Tfv, Smc, and Ftfv, with A. majori having higher values for all variables. A. cf. edwardsi also had significantly lower Smc values than H. stenognathus. No significant differences in microwear texture were found between the geographic variants of A. edwardsi or between A. majori and H. stenognathus. Within the megaladapids, M. grandidieri has higher values for Tfv, Ftfv, and HAsfc(81) than M. edwardsi. M. edwardsi also has higher Smc values than M. madagascariensis. Results from Fisher’s LSD Test generally corroborate those from Tukey’s, as well as suggesting additional differences between the archaeolemurids in epLsar and HAsfc(81). In summary, within the archaeolemurids, the two geographic variants of A. edwardsi were not consistently different, although only A. cf. edwardsi sensu stricto is significantly different from A. majori and H. stenognathus. Overall, A. majori and H. stenognathus have higher values for fill volume and the scale of maximal complexity. Within the megaladapids, M. edwardsi has lower values for fill volume than M. grandidieri and higher scales of maximal complexity than M. madagascariensis. The data suggest that, among the archaeolemurids, A. majori and H. stenognathus have larger, deeper surface features and that among the megaladapids, M. edwardsi has smaller, shallower surface features. These results are consistent with dietary differences both between and within Archaeolemuridae and Megaladapidae. Discussion This study presents new data on the dental microwear of the Archaeolemuridae and Megaladapidae, based on the application of a new technique, dental microwear texture analysis. These data corroborate many of the previous dietary inferences made about the Archaeolemuridae and Megaladapidae using other methods of microwear analysis. In essence, they affirm the dietary separation between the two families and some variation within each family. This study suggests that these subfossil lemurs, like the majority of living primates, did not focus on specific food types and tightly controlled dietary categories. The question then becomes one of degree. How dedicated a folivore was Megaladapis or how specialized a hard-object feeder was Archaeolemur or Hadropithecus? The characterization of Megaladapis as a folivore is reaffirmed by the low epLsar and Tfv values revealed here. An interesting difference between these results and those of previous studies concerns the inference of differences in dietary signals between species of Megaladapis. Significant differences between the species were not found using low magnification light microscopy. However, similarities between M. edwardsi and the extant spiny forest/open woodland-adapted lemur, Lepilemur leucopus and between M. grandidieri and M. madagascariensis and closed forest lepilemurs were noted (Godfrey et al., 2004). SEM analysis suggested that M. edwardsi was more folivorous than other members of the genus (Rafferty et al., 2002). Results of the present study confirm the variability within Megaladapis with significant differences from the other taxa in almost every variable, with a more homogenous surface and smaller features. When compared to previously published data by Scott et al. (2006) for the folivore Alouatta palliata, M. edwardsi has higher mean values for Asfc, suggesting the inclusion of harder objects in the diet; however, the lower values for Tfv are consistent with a highly folivorous diet.

410

J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416

Fig. 1. Photosimulations of microwear surfaces generated from point clouds. Each represents a field of view of 204 mm  276 mm.

Fig. 2. Meshed axiomatic representations of microwear surfaces in three dimensions. Each represents a field of view of 204 mm  276 mm. Vertical scales indicate depth.

J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416

411

Light microscopy studies suggested that archaeolemurid microwear signals were similar to those of Cebus apella (Godfrey et al., 2004). Godfrey et al. (2004) concluded that the archaeolemurids were hard-object ‘‘specialists.’’ While microwear texture analysis results indicate that some of the archaeolemurids had significantly lower Asfc and higher Tfv than reported for C. apella (Scott et al., 2005), these subfossil lemurs did have values in line with those reported for Lophocebus albigena (Scott et al., 2005), an occasional hard-object feeder (Chalmers, 1968; Lambert et al., 2004). Previous SEM analysis of the archaeolemurids recorded larger pits on the surfaces of A. cf. edwardsi than A. edwardsi, and Rafferty et al. (2002) opined that ecogeographic variation might explain the difference. Even though this difference was only confirmed with the Smc variable, ecogeographic variation could be responsible for some interspecific variation within Archaeolemuridae, particularly between A. edwardsi, a species with a texture signature that indicates the presence of both hard and tough foods, and the apparent hard-object feeders, A. majori and H. stenognathus. Godfrey et al. (1999) proposed that A. edwardsi and A. majori were sympatric in part of their range in the central highlands and that dietary differences might reflect niche partitioning. Microwear evidence from SEM and texture analysis both suggest that A. majori diet included harder foods than A. edwardsi and probably incorporated more hard objects (Rafferty et al., 2002). Dietary differences between some of the archaeolemurids were also suggested by a study of d13C measurements on collagen from bones of the Archaeolemuridae, particularly between Archaeolemur and Hadropithecus (Godfrey et al., 2005). Studies of stable isotopes have been conducted on extant lemurs, successfully distinguishing differences in habitats between closely related species (Schoeninger et al., 1998; McGee and Vaughn, 2006; Loudon et al., 2007). These studies suggest that such data can effectively reconstruct past environments of fossil taxa, and therefore, potential sources of dietary variation. d13C values for Hadropithecus imply a diet richer in C4 and/or Crassulacean acid metabolism (CAM) plants and/or invertebrates that feed on C4 or CAM plants. A more recent analysis including more specimens proposed obligate CAM and C4 plant consumption for Hadropithecus (Godfrey et al., 2008). A. majori had stable carbon isotope values corresponding to a diet mixed diet of C3 and C4 or CAM plants, with CAM plants being likely for southern Madagascar, where arid habitats are more common (Godfrey et al.,

Fig. 3. Bivariate plot of anisotropy and complexity for the two families. Individual point values for each specimen have been plotted rather than means. Open symbols represent archaeolemurids (B ¼ A. cf. edwardsi, , ¼ A. edwardsi, D¼ A. majori, > ¼ H. stenognathus) and closed symbols indicate megaladapids (C ¼ M. edwardsi, - ¼ M. grandidieri, : ¼ M. madagascariensis).

Megaladapis edwardsi was the largest of the megaladapids, with an estimated weight of approximately 85 kg, larger than an adult male chimpanzee (Jungers et al., 2008). Members of the subgenus Megaladapis, M. madagascariensis (the smallest megaladapid) and M. grandidieri, evince larger surface features and less anisotropic surfaces, consistent with a diet including more hard objects, possibly some fruits. This is consistent with Godfrey et al.’s (1997) inference that the diet of the Megaladapis species consisted of approximately 0–20% fruit and 80–100% leaves. While the microwear data for the megaladapids are more-orless consistent with those of earlier studies that reconstructed members of the genus as folivores, those for the archaeolemurids are less clearly in agreement. Archaeolemur has been considered a primary frugivore and hard-object feeder based primarily on its craniofacial adaptations, dental microstructure, and highly derived dentition, including large, spatulate upper incisors, a premolar shearing blade, and quadrate, bilophodont molars (Tattersall 1973, 1982). These adaptations, along with the study of coprolites, have suggested to previous investigators at least partial reliance on hard objects and/or tough skinned fruits (Tattersall, 1973; Tattersall and Schwartz, 1974; King et al., 2001; Godfrey et al., 2005).

Table 3 Descriptive microwear texture statistics for Archaeolemuridae and Megaladapidae. Asfc

epLsar

Mean SD

0.84653 0.466062

0.00321 0.001260

6058.71 5141.017

13023.9 4.159160

1.77029 6180.635

0.50681 0.154674

Mean SD

0.88891 0.185991

0.00336 0.001286

8445.97 3715.661

14478.6 33.52228

11.0988 3421.373

0.53852 0.137304

Mean SD

1.08751 0.315264

0.00464 0.001166

13236.1 3178.903

20175.5 15.71293

9.36555 3572.848

0.45473 0.104693

Mean SD

0.68400 0.072301

0.00484 0.001416

10515.8 5839.826

18463.7 7.039325

5.59097 5430.533

0.39697 0.066487

Mean SD

0.59853 0.215656

0.00443 0.002536

1764.51 1990.558

7908.68 0.471319

0.87534 3085.039

0.40385 0.131268

Mean SD M. madagascariensis n¼9 Mean SD

0.54326 0.163827

0.00495 0.002054

6401.47 3983.097

41.4787 3787.064

0.51854 0.131017

0.55055 0.206329

0.00307 0.000999

4440.98 4869.011

A. cf. edwardsi n ¼ 23 A. edwardsi n ¼ 12 A. majori n¼7 H. stenognathus n¼5 M. edwardsi n ¼ 15 M. grandidieri n ¼ 15

Tfv

Ftfv

Smc

12779.1 158.5782 0.47201 0.226601

10757.6 5113.928

Hasfc (9)

0.48000 0.075850

412

J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416

Table 4 Statistical Analyses.a A. Multivariate Nested Analysis of Variance Between families Test statistic Wilks’ Lambda 0.554 Pillai Trace 0.446 Hotelling-Lawley 0.806

F 8.516 8.516 8.516

df 7, 74 7, 74 7, 74

pb 0.000 0.000 0.000

Between species nested within families Test statistic Wilks’ Lambda 0.321 Pillai Trace 0.958 Hotelling-Lawley 1.366

F 2.778 2.641 2.825

df 35, 313 35, 390 35, 362

pb 0.000 0.000 0.000

B. Nested ANOVAs Between families Variable Asfc epLsar Tfv Smc Ftfv HAsfc9 HAsfc81

F 23.00 0.087 28.32 8.778 35.42 0.046 1.636

df 1, 80 1, 80 1, 80 1, 80 1, 80 1, 80 1, 80

pb 0.000 0.769 0.000 0.004 0.000 0.831 0.205

Between species within families Variable Asfc epLsar Tfv Smc Ftfv HAsfc9 HAsfc81

F 1.865 3.487 5.661 4.542 4.943 2.765 1.383

df 5, 80 5, 80 5, 80 5, 80 5, 80 5, 80 5, 80

pb 0.110 0.007 0.000 0.001 0.001 0.024 0.240

C. Matrices of pairwise differences (within family comparisons)c Archaeolemurids 1. epLsar A.edwardsi A. cf. edwardsi A. edwardsi 0.607 A. majori 13.85* 13.24* H. stenognathus 15.14* 14.54* 2. Tfv A. cf. edwardsi A. edwardsi A. edwardsi 6.678 A. majori 18.83** 12.15* H. stenognathus 10.76 4.083 3. Sm A. cf. edwardsi A. edwardsi A. edwardsi 8.437* A. majori 14.83** 6.399 H. stenognathus 17.64** 9.208

Megaladapids A. majori

M. edwardsi 3.667 7.267

M. grandidieri

M. grandidieri M. madagascariensis

M. edwardsi 14.00** 8.011

M. grandidieri

M. grandidieri M. madagascariensis

10.93*

1.298 A. majori

5.989

8.071 A. majori

M. edwardsi 7.700 12.58**

M. grandidieri

M. grandidieri M. madagascariensis

M. edwardsi 13.93** 6.822

M. grandidieri

M. grandidieri M. madagascariensis

M. edwardsi 9.733** 8.044

M. grandidieri

M. grandidieri M. madagascariensis

4.889

2.810

4. Ftfv A. edwardsi A. majori H. stenognathus 5. HASFC A. edwardsi A. majori H. stenognathus a b c

A. cf. edwardsi 2.304 17.44** 13.47* A. cf. edwardsi 4.051 4.497 13.11*

A. edwardsi

A. majori

15.14* 11.16

3.976

A. edwardsi

A. majori

8.548 17.16*

7.111

1.689

8.619

All analyses on ranked data. P values reported as 0.000, while effectively zero probabilites, represent actual values of less than 0.001. * significant with Fisher’s Least Significance Test; ** significant with Tukeys HSD Multiple Comparisons Test.

2005). The values for A. edwardsi were consistent with a diet dominated by C3 plants, which are associated with mosaic or forested habitats. Coprolite analysis for A. edwardsi suggests a diet of frugivory and omnivory for A. edwardsi (Vasey et al., in preparation). The sample size of Hadropithecus stenognathus is small (n ¼ 5) and any differences between it and the larger samples of other taxa

should be taken as suggestive at best. The microwear of H. stenognathus was similar to that of A. majori, with high values for Tfv, Ftfv, and Smc. Fisher’s test results indicate that Hadropithecus had significantly higher values for anisotropy and heterogeneity than did A. edwardsi and A. cf. edwardsi. Along with the other archaeolemurids, the microwear signature of Hadropithecus is consistent with that of a mixed feeder, although with the highest values for

J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416

volume among the studied taxa, it is likely that hard objects were a more frequent part of the diet for Hadropithecus than for the other included subfossils. If this is the case, the hard object feeding adaptations reflected in Hadropithecus could have evolved to allow them to fall back on harder foods when preferred resources were scarce. However, it is also possible that the higher anisotropy values reported for H. stenognathus and A. majori could imply a reliance on tough foods that require more repetitive tooth-food-tooth movements. Isotope analysis also suggests that Hadropithecus ate more leaves and other plant material, while Archaeolemur ate more fruit and animal products (Godfrey et al., 2008; Ryan et al., 2008). The results of the present study support a reconstruction of the archaeolemurids as at least occasional or facultative hard-object feeders, as has previously been suggested by both Rafferty et al. (2002) and Godfrey et al. (2004). The microwear texture analysis results also appear to reflect ecogeographic differences within the genus, as earlier hypothesized by both Godfrey et al. (1997) and Rafferty et al. (2002). As for the specialized morphological adaptations in Archaeolemur, it is important to note that adaptations for tough or hard-object processing may not have been necessary to process all its foods. In other words, Archaeolemur may have had the capability to process such hard or tough foods, but not always done so. Rafferty et al. (2002) argued that the dental microwear of Archaeolemur indicated an eclectic diet with no distinctive signatures. Some individuals were documented to have larger features than others, suggesting to the authors ecogeographic variation in diet or the use of hard objects as fallback resources. Godfrey et al. (2004) found that the dental microwear of Archaeolemur most closely resembled that of Cebus apella, a primate that, while utilizing a variety of resources, has anatomical specializations that it regularly uses for hard-object processing. It was suggested that, as in Cebus, the morphological specializations of Archaeolemur such as extremely thick and heavily decussated enamel, might have also been used to supplement a variable diet. The results of the current study support both conclusions and suggest that the archaeolemurids probably had a variable diet that included hard-objects in addition to other resources. The microwear texture data suggest complex surfaces with a mosaic of layered features of various sizes. The textural variable data for the archaeolemurids overlap with the lower ranges of data reported for C. apella but are concentrated near values more similar to those reported for Lophocebus albigena, a generalist primate that consumes hard objects as fallback items. This suggests that while the archaeolemurids did utilize some hard-objects, they may have done so less frequently than did Cebus. Studies of primate dentition and diet have suggested correlations between morphological features, including tooth shape and enamel thickness, with the ability of a species to utilize certain resources (Lucas, 1979; Lucas and Peters, 2000). The application of dental morphological analysis to the study of dietary preferences in the subfossil lemurs has suggested that taxa had specialized adaptations, such as the fast-wearing premolar shearing blade found in Archaeolemur (Tattersall 1973, 1982) and the high molar shearing crests and loss of upper incisors in Megaladapis (Thenius, 1953), allowing them to take advantage of hard or tough resources, respectively. However, these seemingly specialized adaptations do not tell us whether selective pressures resulted from preferred foods or critical ones taken only on occasion. As described by Liem (1980), species that seem to be very specialized in terms of morphological or behavioral adaptations can, in reality, be ecological generalists. In some cases, the resources that organisms seem specialized to exploit may comprise only a small percentage of their total diet. This phenomenon has become known as Liem’s Paradox (Robinson and Wilson, 1998). For example, a species may have specialized

413

adaptations to allow the consumption of hard or tough fallback foods when less mechanically challenging preferred foods are unavailable. The preferred items may not require any specialized processing (e.g., young leaves or fruit flesh), and therefore may not select for specialized morphology. Thus, while functional morphology can tell us something about what an animal is capable of eating, it does not necessarily give us insights into its food preferences, or how often it ate foods with given fracture properties. Primate diets are highly variable and they depend on preferred resource availability and the occasional use of fallback resources. Differences between taxa are often obscured by the fact that primates assigned to different diet categories in the popular literature often eat similar foodsde.g., gorillas have traditionally been described as folivores, while chimpanzees are known as frugivores. However, Ungar et al. (2008) found overlap in dental microwear signatures between the two species. In fact, gorillas have been reported to consume 73% of the same species eaten by sympatric chimpanzees at Lope´, Gabon (Tutin and Fernandez, 1985). Thus, the lack of clear differences described by Ungar et al. (2008) in central dietary tendencies between chimpanzees and gorillas is not unexpected. Primates tend to prefer high energy foods, such as ripe fruits, that do not require specialization to process (Remis, 1997; Remis et al., 2001; Marshall and Wrangham, 2007). Fallback foods such as hard seeds or tough leaves may require morphological specializations to process efficiently, and so it seems that dental morphology should actually be more reflective of fallback resource use than preferred diet (Robinson and Wilson, 1998). A study of the dental morphology and diet of five lemur species by Yamashita (1998b) revealed that the hardest and toughest resources consumed were fallback foods and that these were more tightly correlated with the dental adaptations found in the lemurs than were the most commonly consumed resources. Reports on the amount of dietary overlap between living lemurs have yielded different results. Many examples of dietary variation and fallback resource use have been reported for lemurs (e.g., Strait and Overdorff, 1996; Yamashita, 1996, 1998a,b; Simmen et al., 2003) and several species of generalist lemurs are known, including Lemur catta. A recent study of lemur seed dispersal at Ranomafana suggests that there is a lack of dietary overlap between species (Wright, 2008). Varecia variegata, Eulemur fulvus, Eulemur rubriventer, and Propithecus edwardsi were reported to not overlap in many of the fruits consumed. Yamashita (2002) also found little overlap in resources selected between Lemur catta and Propithecus verreauxi verreauxi at Beza Mahafaly Special Reserve but did find that these species utilized foods with similar mechanical properties. This suggests that in some habitats lemurs may not overlap in specific foods, but does not mean that they limit themselves to only a few food types or that they always choose foods with the same mechanical properties Individual microwear features on a tooth surface are themselves ultimately worn away and replaced by others. The ‘‘lifespan’’ of a feature depends on its depth. This is known as the ‘‘Last Supper Effect’’ and indicates that microwear features on the enamel surface only reflect feeding activity in the days or weeks prior to death (Grine, 1986). Most primate species exploit a variety of resources with varying fracture properties and abrasives. As a result, it is likely that even species with different central dietary tendencies will overlap in their microwear patterning. But then again, some may also vary dramatically at one period and not the next. Thus, it is only when larger samples sizes are used, preferably taken from specimens that were collected at different times of the year, that the bigger picture of specialization and dietary overlap begins to emerge. This suggests that to understand dietary adaptations and behaviors of primates, a measure other than the central microwear

414

J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416

tendency is important. Given the short lifespan of individual features on the facet, microwear may well give us the opportunity to examine within species variation in dietary patterns given sufficient sample sizes (Teaford and Robinson, 1989). A few outlier specimens, such as is observed for Smc of Archaeolemur, are likely to be more informative of differences in dietary behaviors in many cases (such as fallback food exploitation) than comparisons of sample means (see Scott et al., 2005 for discussion), assuming the individuals sampled are representative of group behavior. The ability to detect subtle differences in within-sample variation may be a key to realizing the potential of dental microwear analyses. Even with the demonstration of extensive overlap in microwear signatures between taxa, this study provides a new set of results that may help to reconstruct the diets of the archaeolemurids and megaladapids. Both the microwear and cranial adaptations are consistent with Megaladapis species focusing on leaves. Interspecific differences in microwear signals suggest that M. edwardsi was the most folivorous of the genus. The results also imply that while the megaladapids focused on tough foods such as some leaves, Archaeolemur at least occasionally ingested harder foods. These data also suggest that ecogeographic differences might help explain the apparently differing levels of frugivory and hard-object feeding in the genus. Conclusions 1. The microwear textures of archaeolemurids are consistent with a generalist diet, and they probably relied on softer, weaker items, such as fruit and perhaps young leaves, and ‘‘fell back’’ on harder objects during times of ecological stress. Two species within the archaeolemurids group, Archaeolemur majori and Hadropithecus stenognathus, have microwear texture signatures consistent with higher levels of hard-object predation than either Archaeolemur edwardsi variant. Archaeolemur edwardsi overlapped with the megaladapids in several variables, suggesting a higher amount of tough foods in the Archaeolemur diet. 2. Microwear textures of the megaladapids are consistent with previous reconstructions of the family as primary folivores with some variation between the taxa. Megaladapis edwardsi has a microwear texture signature consistent with previous reconstructions of the species as having been the most dedicated folivore in the family. Megaladapis grandidieri and Megaladapis madagascariensis both have larger surface features and overall lower values for anisotropy, consistent with a diet including more hard objects. It is possible that these two species included some fruit or hard objects in their diets to supplement the leaves. Acknowledgements We would like to thank the curators at the Acade´mie Malgache, the American Museum of Natural History, the British Museum of Natural History, the Duke University Lemur Center, Oxford University Natural History Museum, the University of Antananarivo, and the Vienna Naturhistorisches Museum for allowing us to study the specimens in their care. We would also like to thank the anonymous reviewers for their helpful comments on an earlier version of this paper. This research was supported by NSF Grants SBR-0315157 (to PSU, AW, and MFT), BCS-0129185 (to LRG and WLJ), and BCS-0237388 (to LRG). References Anyonge, W., 1996. Microwear on canines and killing behavior in large carnivores: saber function in Smilodon fatalis. J. Mammal. 77, 1059–1067.

Biknevicius, A.R., 1986. Dental function and diet in the Carpolestidae (Primates, Plesiadapiformes). Am. J. Phys. Anthropol. 71, 157–171. Brown, C.A., Siegmann, S., 2001. Fundamental scales of adhesion and area-scale fractal analysis. Int. J. Mach. Tools Manuf. 41, 1927–1933. Bullington, J., 1991. Dental microwear of prehistoric juveniles from the lower Illinois River Valley. Am. J. Phys. Anthropol. 84, 59–73. Burney, D.A., James, H.F., Grady, F.V., Rafamantanantsoa, J.G., RamilisoninaWright, H.T., Cowart, J.B., 1997. Environmental change, extinction, and human activity: evidence from caves in NW Madagascar. J. Biogeogr. 24, 755–767. Capozza, M., 2002. Microwear analysis of Mammuthus meridionalis (Nesti, 1825) molar from Campo del Conte (Frosinone, Italy). In: The World of ElephantsdInternational Congress, Rome, pp. 529–533. Chalmers, N.R., 1968. Group composition, ecology and daily activities of free living mangabeys in Uganda. Folia Primatol. (Basel) 8, 247–262. Conover, W.J., Iman, R.L., 1981. Rank transformations as a bridge between parametric and nonparametric statistics. Am. Stat. 35, 124–129. Cook, R.J., Farewell, V.T., 1996. Multiplicity considerations in the design and analysis of clinical trials. J. R. Stat. Soc. Ser. A. 159, 93–110. Daegling, D.J., Grine, F.E., 1994. Bamboo feeding, dental microwear, and diet of the Pleistocene ape Gigantopithecus blacki. S. Afr. J. Sci. 90, 527–532. El Zaatari, S., Grine, F.E., Teaford, M.F., Smith, H.F., 2005. Molar microwear and dietary reconstruction of fossil Cercopithecoidea from the Plio-Pleistocene deposits of South Africa. J. Hum. Evol. 49, 180–205. Enders, C., 2003. Performing multivariate group comparisons following a statistically significant MANOVA. Measurement and Evaluation in Counseling and Development. Available from: http://findarticles.com/p/articles/mi_go2531/is_ 200304/ai_n6438143. Filippi, M.L.; Palombo, M.R.; Barbieri, M.; Capozza, M.; Iacumin, P.; Longinelli, A., 2001. Isotope and microwear analyses on teeth of late Middle Pleistocene Elephas antiquus from the Rome area (La Polledrara, Casal de’ Pazzi). In: The World of ElephantsdInternational Congress, Rome, pp. 534–539. Fleagle, J.G., 1999. Primate Adaptation and Evolution, second ed. Academic Press. Franz-Odendaal, T.A., Solounias, N., 2004. Comparative dietary evaluations of an extinct giraffid (Sivatherium hendeyi) (Mammalia, Giraffidae, Sivatheriinae) from Langebaanweg, South Africa (early Pliocene). Geodiversitas 26, 675–685. Godfrey, L.R., Crowley, B.E., Muldoon, K.M., King, S.J., Burney, D.A., 2008. The Hadropithecus conundrum. Am. J. Phys. Anthropol. Suppl. 46, 105. Godfrey, L.R., Jungers, W.L., 2002. Quaternary fossil lemurs. In: Hartwig, W. (Ed.), The Primate Fossil Record. Cambridge University Press, Cambridge, pp. 97–122. Godfrey, L.R., Jungers, W.L., Reed, K.E., Simons, E.L., Chatrath, P.S., 1997. Subfossil lemurs: inferences about past and present primate communities in Madagascar. In: Goodman, S.M., Patterson, B.D. (Eds.), Natural Change and Human Impact in Madagascar. Smithsonian Institution Press, Washington D.C, pp. 218–256. Godfrey, L.R., Jungers, W.L., Simons, E.L., Chatrath, P.S., Rakotosamimanana, B., 1999. Past and present distributions of lemurs in Madagascar. In: Rakotosamimanana, B., Rasamimanana, H., Ganzhorn, J.U., Goodman, S.M. (Eds.), New Directions in Lemur Studies. Kluwer Academic/Plenum Publishers, New York, pp. 19–53. Godfrey, L.R., Semprebon, G.M., Jungers, W.L., Sutherland, M.R., Simons, E.L., Solounias, N., 2004. Dental use wear in extinct lemurs: evidence of diet and differentiation. J. Hum. Evol. 47, 145–169. Godfrey, L.R., Semprebon, G.M., Schwartz, G.T., Burney, D.A., Jungers, W.L., Flanagan, E.K., Cuozzo, F.P., King, S.J., 2005. New insights into old lemurs: the trophic adaptations of the Archaeolemuridae. Int. J. Primatol. 26, 825–854. Gordon, K.D., 1982. A study of microwear on chimpanzee molars: implications of dental microwear analysis. Am. J. Phys. Anthropol. 59, 195–215. Gordon, K.D., 1984. Hominoid dental microwear: complications in the use of microwear analysis to detect diet. J. Dent. Res. 63, 1043–1046. Green, J.L., Semprebon, G.M., Solounias, N., 2005. Reconstructing the palaeodiet of Florida Mammut americanum via low-magnification stereomicroscopy. Palaeogeogr. Palaeoclimatol. Palaeoecol. 223, 34–48. Grine, F.E., 1986. Dental evidence for dietary differences in Australopithecus and Paranthropus. J. Hum. Evol. 15, 783–822. Grine, F.E., 1987. Quantitative analysis of occlusal microwear in Australopithecus and Paranthropus. Scanning. Microsc. 1, 647–656. Gutierrez, M., Lewis, P.J., Johnson, E., 1998. Evidence of paleoenvironmental change from muskrat dental microwear patterns. Curr. Res. Pleistocene. 15, 107–108. Hayek, L.A.C., Bernor, R.L., Solounias, N., Steigerwald, P., 1991. Preliminary studies of hipparionine horse diet as measured by tooth microwear. Annls. Zool. Fennici. 28, 187–200. Hopley, P.J., Latham, A.G., Marshall, J.D., 2006. Palaeoenvironments and palaeodiets of mid-Pliocene micromammals from Makapansgat Limeworks, South Africa: a stable isotope and dental microwear approach. Palaeogeogr. Palaeoclimatol. Palaeoecol. 233, 235–251. Hunter, J.P., Fortelius, M., 1994. Comparative dental occlusal morphology, facet development, and microwear in two sympatric species of Listriodon (Mammalia, Suidae) from the Middle Miocene of Western Anatolia (Turkey). J. Vert. Paleontol. 14, 105–126. Jacobs, L.L., 1981. Miocene lorisid primates from the Pakistan Siwaliks. Nature 289, 585–587. Jolly, C.J.,1970. Hadropithecus: a lemuroid small-object feeder. Manuscripts 5, 619–626. Jordan, S.E., Brown, C.A., 2006. Comparing texture characterization parameters on their ability to differentiate ground polyethylene ski bases. Wear 261, 398–409. Jungers, W.L., Demes, B., Godfrey, L.R., 2008. How big were the ‘‘giant’’ extinct lemurs of Madagascar? In: Fleagle, J.G., Gilbert, C.C. (Eds.), Elywn Simons: A Search for Origins. Springer Press, New York, pp. 343–360.

J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416 Jungers, W.L., Godfrey, L.R., Simons, E.L., Wunderlich, R.E., Richmond, B.G., Chatrath, P.S., 2002. Ecomorphology and behavior of giant extinct lemurs from Madagascar. In: Plavcan, J.M., Kay, R.F., Jungers, W.L., van Schaik, C.P. (Eds.), Reconstructing Behavior in the Primate Fossil Record. Kluwer Academic/Plenum Publishers, New York, pp. 371–411. Kaiser, T.M., Bernor, R.L., Franzen, J., Scott, R.S., Solounias, N., 2003. New interpretations of the systematics and palaeoecology of the Dorn-Du¨rkheim 1 hipparions (Late Miocene, Turolian Age [MN11]), Rheinhessen, Germany. Senckenbergiana Lethaea. 83, 103–133. Kay, R.F., 1977. Evolution of molar occlusion in Cercopithecidae and early catarrhines. Am. J. Phys. Anthropol. 46, 327–352. Kennedy, F.E., Brown, C.A., Kolodny, J., Sheldon, B.M., 1999. Fractal analysis of hard disk surface roughness and correlation with static and lowspeed friction. ASME J. Tribol. 121 (4), 968–974. Keselman, H.J., Huberty, C.J., Lix, L.M., Olejnik, S., Cribbie, R.A., Donahue, B., Kowalchuk, R.K., Lowman, L.L., Petoskey, M.D., Keselman, J.C., Levin, J.R., 1998. Statistical practices of educational researchers: an analysis of their ANOVA, MANOVA, and ANCOVA. Rev. Ed. Res. 68, 350–386. King, S.J., Godfrey, L.R., Simons, E.L., 2001. Adaptive and phylogenetic significance of ontogenetic sequences in Archaeolemur, subfossil lemur from Madagascar. J. Hum. Evol. 41, 545–576. King, T., 2001. Dental microwear and diet in Eurasian Miocene catarrhines. In: de Bonis, L., Koufos, G.D., Andrews, P. (Eds.), Phylogeny of the Neogene Hominoid Primates in Europe. Cambridge University Press, Cambridge, pp. 102–117. Krause, D.W., 1982. Jaw movement, dental function, and diet in the Paleocene multituberculate Ptilodus. Paleobiology 8, 265–281. Krueger, K.L., Scott, J.R., Kay, R.F., Ungar, P.S., 2008. Dental microwear textures of ‘‘Phase I’’ and ‘‘Phase II’’ facets. Am. J. Phys. Anthropol. 137, 485–490. Lambert, J.E., Chapman, C.A., Wrangham, R.W., Conklin-Brittain, N.L., 2004. The hardness of Cercopithecine foods: implications for the critical function of enamel thickness in exploiting fallback foods. Am. J. Phys. Anthropol. 214, 363–368. Leakey, M.G., Teaford, M.F., Ward, C.V., 2003. Cercopithecidae from Lothagam. In: Leakey, M.G., Harris, J. (Eds.). Columbia University Press, New York, pp. 130–177. Lewis, P.J., Gutierrez, M., Johnson, E., 2000. Ondatra zibethicus (Arvicolinae, Rodentia) dental microwear patterns as a potential tool for palaeoenvironmental reconstruction. J. Archaeol. Sci. 27, 789–798. Liem, K.F., 1980. Adaptive significance of intra- and interspecific differences in the feeding repertoires of cichlid fishes. Am. Zool. 2, 295–314. Loudon, J.E., Sponheimer, M., Sauther, M.L., Cuozzo, F.P., 2007. Intraspecific variation in hair d13C and d15N values of ring-tailed lemurs (Lemur catta) with known individual histories, behavior, and feeding ecology. Am. J. Phys. Anthropol. 133, 978–985. Lucas, P.W., 1979. The dental-dietary adaptations of mammals. Neues Jahrbuch Fu¨r Geologies und Palaontologie 8, 486–512. Lucas, P.W., 2004. Dental Functional Morphology: How Teeth Work. Cambridge University Press, New York. Lucas, P.W., Constantino, P., Wood, B., Lawn, B., 2008. Dental enamel as a dietary indicator in mammals. Bioessays 30, 374–385. Lucas, P.W., Peters, C.R., 2000. Function of postcanine tooth crown shape in mammals. In: Teaford, M.F., Smith, M.M., Ferguson, M.W.J. (Eds.), Development, Function, and Evolution of Teeth. Cambridge University Press, Cambridge, pp. 282–289. Lucas, P.W., Teaford, M.F., 1994. Functional morphology of colobine teeth. In: Davies, A.G., Oates, J.F. (Eds.), Colobine Monkeys: Their Ecology, Behaviour and Evolution. Cambridge University Press, Cambridge, pp. 173–203. MacFadden, B.J., Solounias, N., Cerling, T.E., 1999. Ancient diets, ecology, and extinction of 5-million-year-old horses from Florida. Science 283, 824–827. Marshall, A.J., Wrangham, R.W., 2007. Evolutionary consequences of fallback foods. Int. J. Primatol. 28, 1219–1235. McGee, E., Vaughn, S., 2006. Stable isotope analysis: a technique for evaluating ecological change in disturbed habitats. Int. J. Primatol. 27 (Suppl. 1), 499. Merceron, G., Blondel, C., de Bonis, L., Koufos, G.D., Viriot, L., 2005a. A new method of dental microwear analysis: Application to extant primates and Ouranopithecus macedoniensis (Late Miocene of Greece). Palaios 20, 551–561. Merceron, G., Blondel, C., Brunet, M., Sen, S., Solounias, N., Viriot, L., Heintz, E., 2004a. The Late Miocene paleoenvironment of Afghanistan as inferred from dental microwear in artiodactyls. Palaeogeogr. Palaeoclimatol. Palaeoecol. 207, 143–163. Merceron, G., de Bonis, L., Viriot, L., Blondel, C., 2005b. Dental microwear of fossil bovids from northern Greece: paleoenvironmental conditions in the eastern Mediterranean during the Messinian. Palaeogeogr. Palaeoclimatol. Palaeoecol. 217, 173–185. Merceron, G., Madelaine, S., 2006. Molar microwear pattern and palaeoecology of ungulates from La Berbie (Dordogne, France): environment of Neanderthals and modern human populations of the Middle/Upper Palaeolithic. Boreas 35, 272–278. Merceron, G., Ungar, P., 2005. Dental microwear and palaeoecology of bovids from the Early Pliocene of Langebaanweg, Western Cape province, South Africa. S. Afr. J. Sci. 101, 365–370. Merceron, G., Viriot, L., Blondel, C., 2004b. Tooth microwear pattern in roe deer (Capreolus capreolus, L.) from Chize (Western France) and relation to food composition. Small Ruminant Res. 53, 125–132. O’Leary, M., Teaford, M.F., 1992. Dental microwear and diet of Mesonychids. J. Vert. Paleontol. 12, 45A. Pedreschi, F., Aguilera, J.M., Brown, C.A., 2000. Quantitative characterization of food surfaces using scale-sensitive fractal analysis. J. Food. Process. Eng. 23, 127–143. Pedreschi, F., Aguilera, J.M., Brown, C.A., 2002. Characterization of the surface properties of chocolate using scale-sensitive fractal analysis. Int. J. Food Prop. 5, 523–535.

415

Rafferty, K., Teaford, M.F., 1992. Diet and dental microwear in Malagasy subfossil lemurs. Am. J. Phys. Anthropol. Suppl. 14, 134. Rafferty, K.L., Teaford, M.F., Jungers, W.L., 2002. Molar microwear of subfossil lemurs: improving the resolution of dietary inferences. J. Hum. Evol. 43, 645–657. Ravosa, M.J., Simons, E.L., 1994. Mandibular growth and function in Archaeolemur. Am. J. Phys. Anthropol. 95, 63–76. Remis, M.J., 1997. Western lowland gorillas (Gorilla gorilla gorilla) as seasonal frugivores: use of variable resources. Am. J. Phys. Anthropol. 43, 87–109. Remis, M.J., Dierenfeld, E.S., Mowry, C.B., Carroll, R.W., 2001. Nutritional aspects of western lowland gorilla diet during seasons of fruit scarcity at Bai Hokou, Central African Republic. Int. J. Primatol. 22, 807–836. Rivals, F., Deniaux, B., 2003. Dental microwear analysis for investigating the diet of an argali population (Ovis ammon antiqua) of mid-Pleistocene age, Caune de I’Arago cave, eastern Pyrenees, France. Palaeogeogr. Palaeoclimatol. Palaeoecol. 193, 443–455. Robinson, B.W., Wilson, D.S., 1998. Optimum foraging, specialization, and a solution to Liem’s Paradox. Am. Nat. 151, 223–235. Ryan, T.M., Burney, D.A., Godfrey, L.R., Go¨hlich, U., Jungers, W.L., Vasey, N., RamilisoninaWalker, A., Weber, G.W., 2008. A reconstruction of the Vienna skull of Hadropithecus stenognathus. Proc. Natl. Acad. Sci. 105 (31), 10698–10701. Schoeninger, M.J., Iwaniec, U.T., Nash, L.T., 1998. Ecological attributes recorded in stable isotope ratios of arboreal prosimian hair. Oecologia. 113, 222–230. Schubert, B., Ungar, P.S., Sponheimer, M., Reed, K.E., 2006. Microwear evidence for Plio-Pleistocene bovid diets from Makapansgat Limeworks Cave, South Africa. Palaeogeogr. Palaeoclimatol. Palaeoecol. 241, 301–319. Scott, R.S., Ungar, P.S., Bergstrom, T.S., Brown, C.A., Childs, B.E., Teaford, M.F., Walker, A., 2006. Dental microwear texture analysis: technical considerations. J. Hum. Evol. 51, 339–349. Scott, R.S., Ungar, P.S., Bergstrom, T.S., Brown, C.A., Grine, F.E., Teaford, M.F., Walker, A., 2005. Dental microwear texture analysis shows within species dietary variability in fossil hominins. Nature 436, 693–695. Semprebon, G.M., Godfrey, L.R., Solounias, N., Sutherland, M.R., Jungers, W.L., 2004. Can low-magnification stereomicroscopy reveal diet? J. Hum. Evol. 47, 115–144. Silcox, M.T., Teaford, M.F., 2002. The diet of worms: an analysis of mole dental microwear. J. Mammal. 83, 804–814. Simmen, B., Hladik, A., Ramasiarisoa, P., 2003. Food intake and dietary overlap in native Lemur catta and Propithecus verreauxi and introduced Eulemur fulvus at Berenty, southern Madagascar. Int. J. Primatol. 24, 948–967. Solounias, N., Moelleken, S.M.C., 1993. Tooth microwear and premaxillary shape of an archaic antelope. Lethaia 26, 261–268. Solounias, N., Semprebon, G., 2002. Advances in the reconstruction of ungulate ecomorphology with application to early fossil equids. Am. Mus. Novit. 3366 (1), 1–49. Solounias, N., Teaford, M., Walker, A., 1988. Interpreting the diet of extinct ruminants: the case of a non-browsing giraffid. Paleobiology 14, 287–300. Strait, S.G., 1993. Molar microwear in extant small-bodied faunivorous mammals: an analysis of feature density and pit frequency. Am. J. Phys. Anthropol. 92, 63–79. Strait, S., Overdorff, D., 1996. Food properties of fruit eaten by four species of Malagasy prosimian primate. Am. J. Phys. Anthropol. Suppl. 22, 224. Tattersall, I., 1973. Cranial anatomy of the Archaeolemurinae (Lemuroidea, Primates). Anthropol. Pap. Am. Mus. Nat. Hist. 52, 1–110. Tattersall, I., 1975. Notes on the cranial anatomy of the subfossil Malagasy lemurs. In: Tattersall, I., Sussman, R.W. (Eds.), Lemur Biology. Plenum Press, New York, pp. 111–124. Tattersall, I., 1982. The Primates of Madagascar. Columbia University Press, New York. Tattersall, I., Schwartz, J.H., 1974. Craniodental morphology and the systematics of the Malagasy lemurs (Primates, Prosimii). Anthropol. Pap. Am. Mus. Nat. Hist. 52, 139–192. Teaford, M.F., 1985. Molar microwear and diet in the genus Cebus. Am. J. Phys. Anthropol. 66, 363–370. Teaford, M.F., 1986. Dental microwear and diet in two species of Colobus. In: Proceedings of the 10th Annual International Primatology Conference. Primate Ecology and Conservation. Cambridge University Press, Cambridge, pp. 63–66. Teaford, M.F., 1988. Scanning electron microscope diagnosis of wear patterns versus artifacts on fossil teeth. Scanning. Microsc. 2, 1167–1175. Teaford, M.F., Maas, M.C., Simons, E.L., 1996. Dental microwear and microstructure in early Oligocene primates from the Fayum, Egypt: implications for diet. Am. J. Phys. Anthropol. 101, 527–543. Teaford, M.F., Robinson, J.G., 1989. Seasonal or ecological differences in diet and molar microwear in Cebus nigrivittatus. Am. J. Phys. Anthropol. 80, 391–401. Teaford, M.F., Runestad, J.A., 1992. Dental microwear and diet in Venezuelan primates. Am. J. Phys. Anthropol. 88, 347–364. Teaford, M.F., Walker, A., 1984. Quantitative differences in dental microwear between primate species with different diets and a comment on the presumed diet of Sivapithecus. Am. J. Phys. Anthropol. 64, 191–200. Thenius, E., 1953. Zur Gebiss-Analyse von Megaladapis edwardsi (Lemur, Mammal). Zool. Anz. 150, 251–260. Tutin, C.E.G., Fernandez, M., 1985. Foods consumed by sympatric populations of Gorilla g. gorilla and Pan t. troglodytes in Gabon: some preliminary data. Int. J. Primatol. 6, 27–43. Ungar, P.S., 1996. Dental microwear of European Miocene catarrhines: evidence for diets and tooth use. J. Hum. Evol. 31, 335–366. Ungar, P.S., 1998. Dental allometry, morphology, and wear as evidence for diet in fossil primates. Evol. Anthropol. 6, 205–217.

416

J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416

Ungar, P.S., Brown, C.A., Bergstrom, T.S., Walker, A., 2003. A quantification of dental microwear by tandem scanning confocal microscopy and scale-sensitive fractal analysis. Scanning 25, 189–193. Ungar, P.S., Grine, F.E., Teaford, M.F., El Zaatari, S., 2006. Dental microwear and diets of African early Homo. J. Hum. Evol. 50, 78–95. Ungar, P.S., Merceron, G., Scott, R.S., 2007. Dental microwear texture analysis of Varswater bovids and early Pliocene paleoecology of Langebaanweg, Western Cape Province, South Africa. J. Mammal. Evol. 14, 163–181. Ungar, P.S., Scott, R.S., Scott, J.R., Teaford, M.F., 2008. Dental microwear analysis: historical perspectives and new approaches. In: Irish, J.D. (Ed.), Technique and Application in Dental Anthropology. Cambridge University Press, Cambridge, pp. 389–425. Ungar, P.S., Teaford, M.F., 1996. Preliminary examination of non-occlusal dental microwear in anthropoids: implications for the study of fossil primates. Am. J. Phys. Anthropol. 100, 101–113. Ungar, P.S., Teaford, M.F., Kay, R.F., 2004. Molar microwear and shearing crest development in Miocene catarrhines. Anthropology 42, 21–35. Van Valkenburgh, B., Teaford, M.F., Walker, A., 1990. Molar microwear and diet in large carnivores: inferences concerning diet in the sabretooth cat, Smilodon fatalis. J. Zool. 222, 319–340.

Vasey, N.; Burney, D.A.; Godfrey, L.R., Archaeolemur coprolites from Anjohikely Cave in Northwestern Madagascar reveal dietary diversity and cave use in a subfossil prosimian. In: (Masters, J.; Gamba, M.; Genin, F. (Eds.)), Leaping Ahead: Advances in Prosimian Biology. Springer Verlag, in preparation Wright, P.C., 1999. Lemur traits and Madagascar ecology: coping with an island environment. Yearb. Phys. Anthropol. 42, 31–72. Wright, P.C. 2008. What is the role of lemurs in maintaining ecosystem health in Madagascar forests? Association for Tropical Biology and Conservation Conference Oral Presentation, 2008. Yamashita, N., 1996. Seasonality and site-specificity of mechanical dietary patterns in two Malagasy lemur families (Lemur and Indriidae). Int. J. Primatol. 17, 355–387. Yamashita, N., 1998b. Functional dental correlates of food properties in five Malagasy lemur species. Am. J. Phys. Anthropol. 106, 169–188. Yamashita, N., 1998a. Molar morphology and variation in two Malagasy lemur families (Lemuridae and Indriidae). J. Hum. Evol. 35, 137–162. Yamashita, N., 2002. Diets of two lemur species in different microhabitats in Beza Mahafaly Special Reserve, Madagascar. Int. J. Primatol. 23, 1025–1051. Zang, B., Brown, C.A., Bergstrom, T.S., 2002. Microgrinding of nanostructured material coatings. Ann. CIRP 51, 251–254.