American Journal of Primatology 9999:1–15 (2015) RESEARCH ARTICLE What did Hadropithecus Eat, and Why Should Paleoanthropologists Care? LAURIE R. GODFREY1*, BROOKE E. CROWLEY2, KATHLEEN M. MULDOON3, ELIZABETH A. KELLEY4, 1 1 5 STEPHEN J. KING , ANDREW W. BEST , AND MICHAEL A. BERTHAUME 1Department of Anthropology, University of Massachusetts, Amherst, Massachusetts 2Departments of Geology and Anthropology, University of Cincinnati, Cincinnati, Ohio 3Department of Anatomy, Arizona College of Osteopathic Medicine, Midwestern University, Glendale, Arizona 4Department of Sociology and Anthropology, Saint Louis University, St. Louis, Missouri 5Max Planck Weizmann Center for Integrative Archaeology and Anthropology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany Over 40 years ago, Clifford Jolly noted different ways in which Hadropithecus stenognathus converged in its craniodental anatomy with basal hominins and with geladas. The Malagasy subfossil lemur Hadropithecus departs from its sister taxon, Archaeolemur, in that it displays comparatively large molars, reduced incisors and canines, a shortened rostrum, and thickened mandibular corpus. Its molars, however, look nothing like those of basal hominins; rather, they much more closely resemble molars of grazers such as Theropithecus. A number of tools have been used to interpret these traits, including dental microwear and texture analysis, molar internal and external morphology, and finite element analysis of crania. These tools, however, have failed to provide support for a simple dietary interpretation; whereas there is some consistency in the inferences they support, dietary inferences (e.g., that it was graminivorous, or that it specialized on hard objects) have been downright contradictory. Cranial shape may correlate poorly with diet. But a fundamental question remains unresolved: why do the various cranial and dental convergences exemplified by Hadropithecus, basal hominins, and Theropithecus exist? In this paper we review prior hypotheses regarding the diet of Hadropithecus. We then use stable carbon and nitrogen isotope data to elucidate this species’ diet, summarizing earlier stable isotope analyses and presenting new data for lemurs from the central highlands of Madagascar, where Hadropithecus exhibits an isotopic signature strikingly different from that seen in other parts of the island. We offer a dietary explanation for these differences. Hadropithecus likely specialized neither on grasses nor hard objects; its staples were probably the succulent leaves of CAM plants. Nevertheless, aspects of prior hypotheses regarding the ecological significance of its morphology can be supported. Am. J. Primatol. 9999:1–15, 2015. © 2015 Wiley Periodicals, Inc. Key words: Hadropithecus; d13C; d15N; crassulacean acid metabolism INTRODUCTION raised high above the mandibular occlusal plane. In Hadropithecus stenognathus, a recently extinct contrast, its molar occlusal morphology looks nothing giant lemur (Primates, Archaeolemuridae) from like that of a basal hominin. Its relatively tall cusps fl Madagascar, bears remarkable resemblance in its and crests form complex at ribbons of enamel that cranial morphology and dental proportions to basal retain sharp edges as they wear. Its enamel is only hominins (especially robust australopiths such as moderately thick (as in Theropithecus) and its enamel Paranthropus boisei and P. robustus) [Ryan et al., 2008] and in its molar occlusal morphology to grazing Contract grant sponsor: University of California Lab Fees mammals such as geladas (Theropithecus), capybaras Research Program; contract grant number: 115818. (Hydrochoerus), hippopotamuses (Hippopotamus), and kangaroos (Macropus) (Fig. 1). Like basal ÃCorrespondence to: Laurie R. Godfrey, Department of Anthro- hominins, Hadropithecus has a short face, small pology, University of Massachusetts, 240 Hicks Way, Machmer and orthally implanted upper and lower incisors, Hall, Amherst, MA 01003. E-mail: [email protected] small canines, early fusion of the mandibular sym- Received 31 December 2014; revised 30 October 2015; revision physis, thick mandibular corpus, flaring zygoma, accepted 30 October 2015 molariform posterior premolars and large and bucco- DOI: 10.1002/ajp.22506 lingually expanded molars. Its mandibular ascending Published online XX Month Year in Wiley Online Library ramus is tall so that the temporomandibular joint is (wileyonlinelibrary.com). © 2015 Wiley Periodicals, Inc. 2/Godfrey et al. Fig. 1. Casts of mandibular cheek teeth (p4-m3) of (left to right) Hadropithecus stenognathus (left hemi-mandible mirror-imaged to look right, MNHN 1925-13, from Ambovombe, southern Madagascar), Theropithecus gelada (right hemi-mandible, AMNH 80126), and Paranthropus boisei (Peninj mandible). Note complex unguliform enamel folds in Hadropithecus and Theropithecus. prisms are only weakly decussated [Godfrey et al., conclusion, citing similarities in molar morphol- 2005]. Understanding how an animal with molars so ogy to the molars of hippos, while also describing similar to those of geladas and other grazers might postcranial similarities to monkeys, and cranial also converge so strongly in cranial architecture, similarities to fossil and living humans. incisor and canine reduction, P4 molarization, and H2 : Hadropithecus was a small-object feeder. molar hypertrophication with basal hominins is Jolly [1970] embraced the notion that Hadropi- clearly of paleoanthropological significance. thecus ate grasses, but he proposed a somewhat At least four hypotheses have been proposed broader concept to simultaneously explain this to account for the morphological convergences of animal’s dental convergence with grazers such Hadropithecus with hominins, geladas, or both. as Theropithecus gelada and cranial convergen- Most have focused on diet, some more on the metric ces with basal hominins [see also Tattersall, properties of food items, and others more on their 1973]. In effect, Jolly identified an adaptive material properties. complex involving extreme terrestrialism and While not entirely mutually exclusive, these a diet of small, tough food objects, which, he hypotheses do differ considerably. argued, could account for the dental and cranial differences between Hadropithecus and its sister H1 : Hadropithecus was graminivorous. Shortly taxon, Archaeolemur, just as it could account after Hadropithecus was first described [Lorenz for parallel differences between Theropithecus von Liburnau, 1899], Forsyth-Major [1900] and Papio or Mandrillus, and between Austral- concluded on the basis of its molar morphology opithecus and Pan. Small food items, he argued, that it was a grazer. In his monograph of this do not require heavy incisal preparation but extinct lemur, Lamberton [1938] drew the same may require heavy repetitive mastication. Am. J. Primatol. Stable Isotopes and Diet of Hadropithecus /3 Specifically for Hadropithecus, Jolly [1970] skull of Hadropithecus than in Archaeolemur argued, “By analogy with living forms, it seems under specified loading conditions (P4 biting at likely that Archaeolemur fed mainly upon maximum gape, M2 biting at maximum gape), relatively large food-items, probably mostly whether or not scaled to equal body size. On the fruit, requiring incisal preparation, while the other hand, Hadropithecus had greater mechan- diet of Hadropithecus was centred upon the ical advantage in converting muscle force to bite stems, rhizomes, and probably also seeds of force (especially for its molars). Dumont et al. grasses, which, being a primate and lacking front [2011] therefore interpreted the craniofacial and teeth adapted for grazing, it presumably picked dental features of Hadropithecus as adaptations up by hand” (p. 622). for withstanding repetitive loads. They also H3 : Hadropithecus was a hard-object feeder. Stud- interpreted the “hard-object” signal found in ies of dental microwear using scanning electron microwear and enamel surface texture analysis microscopy [Rafferty et al., 2002] and low as possibly related instead to high grit in magnification [Godfrey et al., 2004], as well as open environments. Constantino et al. [2012] studies of microwear “texture” using confocal effectively supported this idea. They estimated microscopy [Scott et al., 2009], all supported the maximum bite forces (critical failure loads) of hard-object feeding for Hadropithecus. Stress- Hadropithecus, Archaeolemur and other subfos- limited (hard) foods (such as nuts or certain sil lemurs using dental fracture mechanics seeds) can be large or small; they are simply foods (taking into consideration tooth size and abso- that fail under the high loads required to fracture lute enamel thickness). They found maximum them. While the enamel of Hadropithecus was bite force in Hadropithecus to be comparable to quite a bit thinner than that of its sister taxon, that of modern Homo sapiens, slightly lower Archaeolemur (and thinner than fossil hominins) than that of the largest-bodied Archaeolemur [Godfrey et al., 2005], its relative enamel (A. edwardsi), and considerably lower than those thickness overlapped that of orangutans; thus, of basal hominins (especially Paranthropus). hard-object feeding could not be ruled out on this They concluded on this basis that Hadropithecus basis. Baab et al. [2014] found weak support for was not a hard-object processor. the hypothesis that diet accounts for variation in skull form in subfossil and living lemurs; Testing the above hypotheses requires under- however,