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Stressed out: Masticatory forces and primate circumorbital form

2000; Wiley; Volume: 261; Issue: 5 Linguagem: Inglês

10.1002/1097-0185(20001015)261

1097-0185

Matthew J. Ravosa, Christopher J. Vinyard, William L. Hylander,

Primate Behavior and Ecology

Editor's note: This pair of articles—Anat Rec (New Anat) 261:173–175 (Ravosa et al.) and 170–172 (Prossinger et al.), 2000—were originally submitted as a Letter to the Editor commenting on the article by Bookstein et al. [Anat Rec (New Anat) 257:217-224, 1999] and a Response by Bookstein et al. (1999). The Editorial Board concluded that the length and depth of this scientific discussion on one aspect of the referenced article—viz., possible relationships between browridge morphology and masticatory stress in ancient vs. modern hominids—warranted more space than is typically offered to Letters to the Editor. We therefore decided to publish these articles back to back, as brief Point/Counterpoint articles, in order to let the researcher present well-developed arguments on both sides of this intriguing debate. The authors of Bookstein et al. (1999) recently employed a suite of imaging techniques and morphometric analyses to describe evolutionary changes in circumorbital form among Pleistocene hominids. In discussing the broader implications of their study, they claim that, contrary to specific in vivo (Hylander et al., 1991a) and comparative (Ravosa, 1991b) work, “the external form of the browridges is related to the need to resolve the stresses in the face… induced by mastication” (Bookstein et al., 1999; p. 222). This conclusion is based on “the inner morphology of the frontal sinuses in the CT scans” of various hominoid crania, specifically the thin “anterior and posterior walls of the sinuses” (Bookstein et al., 1999; p. 222). According to the authors, “thinning minimizes bone mass without compromising the necessary strength, suggesting that…externally enormous supraorbital structures do relate to masticatory stresses” (Bookstein et al., 1999; p. 222). The purpose of our response is threefold. First, we address their argument regarding the functional significance of thin-walled browridges. Second, we indicate that recent in vivo bone-strain analyses provide no support for any masticatory-stress hypothesis of circumorbital form. Third, based on experimental and morphological data, we show that, rather than being adapted to counter masticatory stresses, variation in browridge proportions and frontal sinus pneumatization is supportive of the spatial model of supraorbital torus formation (Moss and Young, 1960; Shea, 1986; Ravosa, 1988, 1991a,, b; Hylander and Ravosa, 1992). If Bookstein et al. (1999) insist that a thin-walled supraorbital torus in humans is especially designed for resisting masticatory stresses, we should then ask what kind of evidence would support a refutation of this hypothesis. Presumably the presence of a thicker-walled supraorbital torus would constitute such a refutation. But this does not seem reasonable since we could just as easily argue that relatively thicker walls also represent an adaptation to larger routine masticatory forces. This dilemma highlights the inherent difficulty in evaluating the functional significance of skull form in the absence of experimental data. This is perhaps best underscored by the lesson of the macaque zygomatic arch. In this primate, the thin cortical bone of the posterior region of the arch experiences very low strains, whereas the thick cortical bone of the anterior portion is a high strain area (Hylander and Johnson, 1997). Such a pattern is opposite to what would be predicted if Bookstein et al.'s (1999) morphological criterion were the sole means of inferring browridge function. Thus, we argue that the data employed by Bookstein et al. can provide neither support for, nor a refutation of, their claim regarding the masticatory determinants of variation in the thickness of the walls of primate supraorbital tori. Instead, their argument is simply an assertion based on a preconceived notion as to the functional significance of browridges. Any hypothesis that states that the morphology of a specific bone (or bones) evinces maximum strength with a minimum of material to resist a particular load is essentially suggesting that this structure is optimized, and is hence adapted, for countering this load. To test such an hypothesis, it is critical to determine what constitutes a sufficient level of strain, stress or load for an element to be considered an adaptation to a given load. In vivo peak-strain magnitudes during forceful chewing and biting offer the best available criteria for evaluating the importance of a masticatory loading regime on skull form (Bouvier and Hylander, 1996a,b; Hylander and Johnson, 1992, 1997; Hylander et al., 1991a,b, 1998; Hylander and Ravosa, 1992). To demonstrate that a craniofacial structure such as the browridge is adapted to bear masticatory stresses, its corresponding safety factor—strain value at yield/observed strain magnitude—should be lower than 4 or 5 (Biewener, 1993; Bouvier and Hylander, 1996a,b; Hylander and Johnson, 1992, 1997; Hylander et al., 1991a,b, 1998; Hylander and Ravosa, 1992; Lanyon and Rubin, 1985; Ravosa et al., 2000a,b). In such a case where a skeletal element has a relatively low safety factor and thus by definition appears to exhibit a maximum amount of strength with a minimum of bony tissue, one can infer it is adapted for countering a given load. In positing an explanation for the functional significance of thin supraorbital bone overlying the hominid frontal sinus, Bookstein et al. (1999) overlook the implications of recent in vivo work on a phylogenetically diverse sample of catarrhine (Bouvier and Hylander, 1996a,b; Hylander and Johnson, 1992, 1997; Hylander et al., 1991a,b, 1998; Hylander and Ravosa, 1992), platyrrhine (Hylander et al., 1998; Ross and Hylander, 1996) and strepsirhine primates (Hylander et al., 1998; Ravosa et al., 2000a,b). Several generalizations regarding cranial safety factors and the optimization of skull form for resisting masticatory stress can be drawn from these investigations. First: primate mandibular, maxillary, and anterior zygomatic peak-strain magnitudes during forceful mastication and incision fall within the range of values for vertebrate postcranial elements during vigorous locomotion (Biewener, 1993; Lanyon and Rubin, 1985). In contrast, strains along the primate supraorbital rim, interorbital pillar, postorbital septum and postorbital bar are considerably lower during the same powerful chewing and biting episodes. Thus, peak-strain magnitudes along the primate circumorbital region are always substantially less than peak values found along many other skeletal elements. Therefore, contra Bookstein et al. (1999), browridge morphology is probably not specially adapted to counter masticatory stress because bone in this area could be reduced considerably without risking structural failure associated with forceful chewing and biting (Bouvier and Hylander, 1996a,b; Hylander and Johnson, 1992, 1997; Hylander et al., 1991a,b; Hylander and Ravosa, 1992; Ravosa et al., 2000a,b; Ross and Hylander, 1996). To do so, however, increases the risk of fracturing the circumorbital region due to traumatic non-masticatory loads (e.g., falls), and this would significantly reduce the fitness of such an organism (Hylander and Johnson, 1992, 1997; Hylander et al., 1991a,b; Hylander and Ravosa, 1992; Ravosa et al., 2000a,b). Bookstein et al.'s discussion of circumorbital form and function highlights a morphological relationship that cannot be explained by any masticatory-stress hypothesis. That is, if large browridges and frontal sinuses in the Petralona cranium (Bookstein et al., 1999; Figure seven: p. 223) are adaptations to resist masticatory loads, then why do orangutans, large-bodied apes with a very hard/tough diet, exhibit such diminutive browridges? We believe the answer to this question is that ontogenetic and interspecific variation in the position of the orbital apertures relative to the anterior cranial vault underlies the extent of anthropoid browridge formation (Moss and Young, 1960; Ravosa, 1988, 1991a,b; Shea, 1986). We argue that the data employed by Bookstein et al. (1999) can provide neither support for, nor a refutation of, their claim regarding the masticatory determinants of variation in the thickness of the walls of primate supraorbital tori. Second: work on recent Melanesians shows that variation in adult human browridge proportions is also correlated with spatial and allometric (Hylander and Ravosa, 1992; Ravosa, 1988, 1991a,b) factors, which in turn indicates the hominid pattern of supraorbital torus development is similar to that of other anthropoids (Vinyard, 1994). The human analyses further demonstrate that, controlling for browridge size, frontal sinus pneumatization varies considerably across adults (Vinyard and Smith, 1997), a pattern which is opposite to Bookstein et al.'s (1999) putative link between supraorbital torus and frontal sinus development. The very low correlation levels between intraspecific variability in hominid frontal sinus proportions and browridge thickness (Vinyard and Smith, 1997) instead suggest that neither of these features is functionally related to variation in masticatory loads. As the primate circumorbital region experiences uniformly low strains and therefore correspondingly higher safety factors for masticatory stresses, it is more likely that (1) supraorbital tori develop to bridge the structural gap between neurocranial and orbital components of the skull, (2) the relative thickness of browridge walls (and calvarium) is a structural adaptation to counter accidental loads and (3) an extensive frontal sinus can reduce the use of a metabolically costly tissue such as bone. Of course, it is always possible to argue that, in contrast to the consistently low circumorbital strain levels observed during chewing and biting in a wide variety of non-human primates, the circumorbital region of extinct hominids experienced relatively higher masticatory stresses. One obvious drawback of such an explanation is that it is not directly testable. In addition to being less parsimonious and unfalsifiable as an hypothesis, it seems highly improbable that masticatory forces in a hominid that cooked its food (if only occasionally) regularly exceeded those of non-human primates that routinely process and ingest tough and/or hard items in the wild. In conclusion, a consideration of primate bone-strain data clearly indicate that circumorbital bone mass could be reduced considerably without inducing structural failure of the browridges during normal chewing and biting behaviors (Bouvier and Hylander, 1996a,b; Hylander and Johnson, 1992, 1997; Hylander et al., 1991a,b, 1998; Hylander and Ravosa, 1992; Ravosa et al., 2000a,b; Ross and Hylander, 1996). This finding is contrary to persistent claims that supraorbital torus development is an adaptation to resist masticatory forces (Bookstein et al., 1999; Lahr and Wright, 1996; Tattersall, 1995; Wolpoff, 1996). Moreover, the in vivo analyses, especially work on the primate zygomatic arch (Hylander and Johnson, 1997), demonstrate that gross morphology alone cannot be used to infer levels of masticatory stress and strain. Lastly, we suggest that Bookstein et al.'s (1999) data on hominoid browridge and frontal sinus proportions further support the hypothesis that ontogenetic and interspecific variation in primate circumorbital form is correlated directly and/or indirectly with variation in cranial size and neural-orbital disjunction (Hylander and Ravosa, 1992; Moss and Young, 1960; Ravosa, 1988, 1991a,b; Ravosa et al., 2000a,b; Ross and Hylander, 1996; Shea, 1986; Vinyard, 1994; Vinyard and Smith, 1997). B. Shea and A. Hogue offered helpful comments and suggestions. Personal research discussed herein was funded by the NIH, NSF, Northwestern University and Duke University. Dr. Ravosa is an associate professor in the Dept. of Cell and Molecular Biology at Northwestern University Medical School, and a research associate in the Dept. of Zoology, Mammals Division, at the Field Museum of Natural History. He is interested in the biomechanics, development, and ecomorphology of the mammalian skull, particularly as it relates to major morphological transformations during the origin of higher clades. Dr. Vinyard is a research associate, and Dr. Hylander is a professor, in the Dept. of Biological Anthropology and Anatomy at Duke University Medical Center. Dr. Vinyard is interested in morphological integration in the primate skull, and how covariation in craniofacial structures is related to the functional morphology and evolutionary history of this anatomical complex. Dr. Hylander studies the functional morphology and biomechanics of the vertebrate cranium, especially in primates. Over the past 25 years his laboratory has pioneered the development and application of in vivo bone-strain and jaw-muscle EMG investigations of the masticatory apparatus.