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Food Mechanical Properties, Feeding Ecology, and the Mandibular Morphology of Wild Orangutans

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Food Mechanical Properties, Feeding Ecology, and the Mandibular Morphology of Wild Orangutans See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/264038729 Food mechanical properties, feeding ecology, and the mandibular morphology of wild orangutans Article in Journal of Human Evolution · October 2014 DOI: 10.1016/j.jhevol.2014.05.007 CITATIONS READS 27 368 6 authors, including: Erin R. Vogel Astri Zu Rutgers, The State University of New Jersey universitas nasional 95 PUBLICATIONS 1,759 CITATIONS 8 PUBLICATIONS 106 CITATIONS SEE PROFILE SEE PROFILE Madeleine E Hardus Serge Wich Pongo Foundation Liverpool John Moores University 26 PUBLICATIONS 559 CITATIONS 341 PUBLICATIONS 8,929 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: Functional and evolutionary correlates of jaw-muscle fiber architecture in primates View project Impact of feeding behavior on the deformations of the macaque mandible. View project All content following this page was uploaded by Nathaniel J Dominy on 21 April 2018. The user has requested enhancement of the downloaded file. Journal of Human Evolution 75 (2014) 110e124 Contents lists available at ScienceDirect Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol Food mechanical properties, feeding ecology, and the mandibular morphology of wild orangutans * Erin R. Vogel a, , Astri Zulfa b, Madeleine Hardus c, Serge A. Wich d, Nathaniel J. Dominy e, Andrea B. Taylor f, g a Department of Anthropology and Center for Human Evolutionary Studies, Rutgers, The State University of New Jersey, 131 George Street, Ruth Adams Building Suite 306, New Brunswick, NJ 08901-1414, USA b Universitas Nasional Jakarta, Jakarta, Indonesia c Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands d School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, UK e Department of Anthropology, 6047 Silsby Hall, Dartmouth College, Hanover, NH, USA f Department of Community and Family Medicine, Duke University School of Medicine, Box 104002, Durham, NC 27708, USA g Department of Evolutionary Anthropology, Duke University, 104 Biological Sciences Building, Box 90383, Durham, NC 27708-9976, USA article info abstract Article history: Bornean orangutan mandibular morphology has been functionally linked to the exploitation of hard and Received 24 September 2013 tough foods, based on evidence that Pongo pygmaeus wurmbii spends a greater percentage of time Accepted 16 May 2014 feeding on bark, seeds and vegetation compared with Pongo abelii (Sumatran orangutans) and the Available online 16 July 2014 assumption that these tissues are more challenging to process than fruit pulp. We measured and compared toughness (R) and Young's modulus (E) of ripe and unripe foods exploited by P. abelii and P. p. Keywords: wurmbii. Additionally, we recorded and compared the percentage of time these orangutans fed on plants/ Toughness fi ' plant parts of varying degrees of R and E. Compared with P. abelii, P. p. wurmbii consumed signi cantly Young s modulus 0.5 fi Mandibular morphology tougher and more displacement limited (R/E) fruit parts, leaves and inner bark, and spent a signi - Feeding behavior cantly greater percentage of time feeding on immature leaves, unripe fruit and other vegetation. Modulus Diet did not vary as expected between species, likely because we failed to capture the high-end range of Pongo modulus values for tissues consumed by P. p. wurmbii. Notably, P. p. wurmbii spent ~40% of its feeding À time on the toughest foods consumed (between 1000 and 4000 J m 2). Thus, the hypothesis that mandibular robusticity in P. p. wurmbii is functionally linked to feeding on tough foods is supported and is likely related to countering relatively larger external forces and/or repetitive loads required to process the toughest tissues. The importance of elastic modulus on morphological divergence awaits future studies capturing the full range of this material property for P. p. wurmbii. Finally, phenophase and fruit availability influence orangutan species differences in food material properties and percentage of time spent feeding on various foods, emphasizing the importance of incorporating these variables in future studies of feeding ecology and craniodental morphology in extant taxa. © 2014 Elsevier Ltd. All rights reserved. Introduction et al., 2011; Ross et al., 2012). When primates chew or bite, their jaw muscles apply loads to the mandible. These loads, in turn, cause The relationships among primate feeding behavior, diet, and internal stresses and strains in the mandible. Food material prop- mandibular morphology are of central importance to anthropolo- erties (FMPs) modulate both the magnitude and duration of jaw- gists seeking to link behavioral ecology with functional and muscle activity (Ahlgren, 1966; Luschei and Goodwin, 1974; evolutionary morphology (e.g., Hylander, 1979a; Bouvier, 1986; Hiiemae, 1978; Hylander, 1979b; Thexton et al., 1980; Oron and Ravosa, 1991, 1996a; Daegling, 1992; Taylor, 2002, 2006; Wright, Crompton, 1985; Chew et al., 1988; Hylander and Johnson, 1994; 2005; Daegling and McGraw, 2007; Taylor et al., 2008; Hogg Agrawal et al., 1998; Ross et al., 2007) such that food elastic modulus and toughness are associated with the complexity of jaw movements, recruitment levels of jaw-muscle force, and/or jaw * Corresponding author. loads. It is this empirically demonstrated relationship between E-mail address: [email protected] (E.R. Vogel). FMPs, jaw-muscle activity patterns, and mandibular loads that has http://dx.doi.org/10.1016/j.jhevol.2014.05.007 0047-2484/© 2014 Elsevier Ltd. All rights reserved. E.R. Vogel et al. / Journal of Human Evolution 75 (2014) 110e124 111 led many investigators to draw functional and adaptive conclusions feeding on items that have been identified as fallback foods, about feeding behavior and diet from jaw form in both living and including inner bark, leaves, and other vegetation. Fallback foods fossil primates (Jolly, 1970; Hylander, 1979a, 1988; Smith, 1983; (sensu Marshall and Wrangham, 2007) are low-quality, abundant Daegling, 1989, 1992; Cole, 1992; Spencer and Demes, 1993; items that are eaten when preferred foods are scarce. The majority Anton, 1996; Ravosa, 1996a, 2000; Taylor, 2002, 2006; Wright, of Bornean orangutan fallback foods is significantly tougher and 2005; Vinyard and Ryan, 2006; Strait et al., 2009; Dumont et al., more resistant to deformation than their preferred fruits (Vogel 2011). Identifying morphological responses to mandibular loads et al., 2008) and feeding on mechanically challenging fallback in extant taxa is key to testing diet-based ecological models of foods has been argued to play an important evolutionary role in species diversification, and to extending these models to fossil taxa. shaping primate craniodental morphology (Rodman, 1977; Kay, However, the functional relationships among jaw form, feeding 1981; Lambert et al., 2004; Ungar, 2004; Laden and Wrangham, behavior, and diet are complex and expected morphological dif- 2005; Wright, 2005; Taylor, 2006; Marshall and Wrangham, ferences have not been consistently observed (Daegling and 2007; Taylor et al., 2008; Ungar et al., 2008; Vogel et al., 2008, Hylander, 2000; Daegling and McGraw, 2001, 2007; Taylor et al., 2009; Constantino et al., 2009; Marshall et al., 2009; Wright 2008; Ross et al., 2009, 2012). et al., 2009; Daegling et al., 2011; McGraw and Daegling, 2012). One reason for the variance between theoretical expectations In a previous study, Taylor (2006) compared mandibular and empirical findings may relate to the historic reliance on qual- morphology among Bornean and Sumatran orangutan populations. itative descriptions of coarse-grained diet classifications (e.g., foli- At the time the study was conducted, feeding behavior and diet vore, frugivore) and food classes (e.g., fruit, terrestrial herbaceous were based on documented differences in habitat productivity, vegetation) as meaningful proxies for FMPs (Hylander, 1979a; qualitative estimates of FMPS inferred from food type (i.e., bark and Daegling, 1992; Anapol and Lee, 1994; Ravosa, 1996b; Taylor, some vegetation were presumed to be mechanically more difficult 2006). Numerous comparative studies of primate mandibular to process than fruit pulp), and field observations of percentage of morphology have been based on the classically held assumption time spent feeding on these different foods (MacKinnon, 1974; that leaves are tough, seeds are hard, and fruits are soft, and thus it Rodman, 1977, 1988; Rijksen, 1978; Leighton, 1993; van Schaik, has been assumed that food mechanical properties map neatly onto 1999; Delgado and van Schaik, 2000; van Schaik and Knott, dietary categories (Hylander, 1975; Rosenberger and Kinzey, 1976; 2001). Dietary profiles based on these data led Taylor to hypothe- Beecher, 1979; Smith, 1983, 1984; Peters, 1987, 1993; Rosenberger, size that P. p. wurmbii load their jaws more frequently, and possibly 1992; Anapol and Lee, 1994; Daegling and McGraw, 2001; Taylor, with relatively greater forces, compared with P. abelii. Thus, Taylor 2006). Not surprisingly, for some of these studies, predicted predicted that P. p. wurmbii would exhibit mandibular features that morphological relationships based on these broad dietary classes reflect the demands of a more mechanically challenging diet. Tay- have not been systematically borne out by the data (Bouvier, 1986; lor's predictions were generally supported
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