An official website of the United States government
Abstract Carnivorans represent extreme ecomorphological diversity, encompassing remarkable variation in form, habitat, and diet. The relationship between the masticatory musculature and dietary ecology has been explored in a number of carnivoran lineages, including felids and the superfamily Musteloidea. In this study, we present novel architectural data on two additional carnivoran families—Ursidae and Canidae—and supplement these previous studies with additional felid, musteloid, herpestid, hyaenid, and viverrid taxa (a total of 53 species across 10 families). Gross dissection data were collected following a standardized protocol—sharp dissection followed by chemical digestion. Summed jaw adductor forces were also transformed into bite force estimates (BF) using osteologically calculated leverages. All data were linearized, log‐transformed, and size‐adjusted using two proxies for each taxon—body mass (BM) and cranial geometric mean—to assess relative scaling trends. These architectural data were then analyzed in the context of dietary ecology to examine the impact of dietary size (DS) and dietary mechanical properties (DMP). Muscle mass, physiological cross‐sectional area, and BF scaled with isometry or positive allometry in all cases, whereas fascicle lengths (FLs) scaled with isometry or negative allometry. With respect to diet, BM‐adjusted FLs were strongly correlated with DS in musteloids, but not in any other lineage. The relationship between size‐adjusted BF and DMP was also significant within musteloids, and across the sample as a whole, but not within other individual lineages. This interfamilial trend may reflect the increased morphological and dietary diversity of musteloids relative to other carnivoran groups.
more »
« less
Bite Force and Masticatory Muscle Architecture Adaptations in the Dietarily Diverse Musteloidea (Carnivora)
ABSTRACT Dietary ecology and its relationship with both muscle architecture and bite force potential has been studied in many mammalian (and non‐mammalian) taxa. However, despite the diversity of dietary niches that characterizes the superfamily Musteloidea, the masticatory muscle fiber architecture of its members has yet to be investigated anatomically. In this study, we present myological data from the jaw adductors in combination with biomechanical data derived from craniomandibular measurements for 17 species representing all four families (Ailuridae, Mephitidae, Mustelidae, and Procyonidae) of Musteloid. These data are combined to calculate bite force potential at each of three bite points along the dental row. Across our sample as a whole, masticatory muscle mass scaled with isometry or slight positive allometry against both body mass and skull size (measured via a cranial geometric mean). Total jaw adductor physiological cross‐sectional area scaled with positive allometry against both body mass and skull size, while weighted fiber length scaled with negative allometry. From a dietary perspective, fiber length is strongly correlated with dietary size such that taxa that exploit larger foods demonstrated myological adaptations toward gape maximization. However, no consistent relationship between bite force potential and dietary mechanical resistance was observed. These trends confirm previous findings observed within the carnivoran family Felidae (as well as within primates), suggesting that the mechanisms by which masticatory anatomy adapts to dietary ecology may be more universally consistent than previously recognized. Anat Rec, 302:2287–2299, 2019. © 2019 American Association for Anatomy
more »
« less
- Award ID(s):
- 1557125
- PAR ID:
- 10671965
- Publisher / Repository:
- American Association for Anatomy
- Date Published:
- Journal Name:
- The Anatomical Record
- Volume:
- 302
- Issue:
- 12
- ISSN:
- 1932-8486
- Page Range / eLocation ID:
- 2287 to 2299
- Subject(s) / Keyword(s):
- Bite Force gape masseter temporalis pterygoids Masticatory muscles Muscle Architecture Diet Musteloidea Carnivora scaling PCSA fiber length mechanical advantage
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
ABSTRACT The masticatory apparatus has been the focus of many studies in comparative anatomy—especially analyses of skulls and teeth, but also of the mandibular adductor muscles which are responsible for the production of bite force and the movements of the mandible during food processing and transport. The fiber architecture of these muscles has been correlated to specific diets (e.g., prey size in felids) and modes of foraging (e.g., tree gouging in marmosets). Despite the well‐elucidated functional implications of this architecture, little is known about its ontogeny. To characterize age‐related myological changes, we studied the masticatory muscles in a large (n= 33) intraspecific sample of a small, Malagasy primate,Microcebus murinusincluding neonatal through geriatric individuals. We removed each of the mandibular adductors and recorded its mass as well as other linear measurements. We then chemically dissected each muscle to study its architecture—fascicle length and physiological cross‐sectional area (PCSA) which relate to stretch (gape) and force capabilities, respectively. We observed PCSA and muscle mass to increase rapidly and plateau in adulthood through senescence. Fascicle lengths remained relatively constant once maximal length was reached, which occurred early in life, suggesting that subsequent changes in PCSA are driven by changes in muscle mass. Quadratic curvilinear models of each of the architectural variables of all adductors combined as well as individual muscles regressed against age were all significant. Anat Rec, 303:1364–1373, 2020. © 2019 American Association for Anatomymore » « less
-
Abstract In carnivorans, bite force is a critical and ecologically informative variable that has been correlated with multiple morphological, behavioral, and environmental attributes. Whereas in vivo measures of biting performance are difficult to obtain in many taxa—and impossible in extinct species—numerous osteological proxies exist for estimating masticatory muscle size and force. These proxies include both volumetric approximations of muscle dimensions and direct measurements of muscular attachment sites. In this study, we compare three cranial osteological techniques for estimating muscle size (including 2D‐photographic and 3D‐surface data approaches) against dissection‐derived muscle weights and physiological cross‐sectional area (PCSA) within the jaw adductor musculature of 40 carnivoran taxa spanning eight families, four orders of magnitude in body size, and the full dietary spectrum of the order. Our results indicate that 3D‐approaches provide more accurate estimates of muscle size than do surfaces measured from 2D‐lateral photographs. However, estimates of a muscle's maximum cross‐sectional area are more closely correlated with muscle mass and PCSA than any estimates derived from muscle attachment areas. These findings highlight the importance of accounting for muscle thickness in osteological estimations of the masticatory musculature; as muscles become volumetrically larger, their larger cross‐sectional area does not appear to be associated with a proportional increase in the attachment site area. Though volumetric approaches approximate muscle dimensions well across the order as a whole, caution should be exercised when applying any single method as a predictor across diverse phylogenies.more » « less
-
Abstract In 1974, Sue Herring described the relationship between two important performance variables in the feeding system, bite force and gape. These variables are inversely related, such that, without specific muscular adaptations, most animals cannot produce high bite forces at large gapes for a given sized muscle. Despite the importance of these variables for feeding biomechanics and functional ecology, the paucity of in vivo bite force data in primates has led to bite forces largely being estimated through ex vivo methods. Here, we quantify and compare in vivo bite forces and gapes with output from simulated musculoskeletal models in two craniofacially distinct strepsirrhines:Eulemur, which has a shorter jaw and slower chewing cycle durations relative to jaw length and body mass compared toVarecia. Bite forces were collected across a range of linear gapes from 16 adult lemurs (suborder Strepsirrhini) at the Duke Lemur Center in Durham, North Carolina representing three species:Eulemur flavifrons(n = 6; 3F, 3M),Varecia variegata(n = 5; 3F, 2M), andVarecia rubra(n = 5; 5F). Maximum linear and angular gapes were significantly higher forVareciacompared toEulemur(p = .01) but there were no significant differences in recorded maximum in vivo bite forces (p = .88). Simulated muscle models using architectural data for these taxa suggest this approach is an accurate method of estimating bite force‐gape tradeoffs in addition to variables such as fiber length, fiber operating range, and gapes associated with maximum force. Our in vivo and modeling data suggestVareciahas reduced bite force capacities in favor of absolutely wider gapes compared toEulemurin relation to their longer jaws. Importantly, our comparisons validate the simulated muscle approach for estimating bite force as a function of gape in extant and fossil primates.more » « less
-
ABSTRACT Relative to all other primates, the aye‐aye (Daubentonia madagascariensis) exists at the extremes of both morphology and behavior. Its specialized anatomy—which includes hypselodont incisors and highly derived manual digits—reflects a dietary niche, unique among primates, which combines tap‐foraging with gouging to locate and extract wood‐boring larvae. Here, we explore the impact of this extreme dietary ecology upon the masticatory musculature of this taxon with reference to a second, similarly sized but highly generalist lemuriform—the mongoose lemur (Eulemur mongoz). Using non‐destructive, high‐resolution diffusible iodine‐based contrast‐enhanced computed tomography techniques, we reconstruct the three‐dimensional volumes of eight masticatory muscles, and, for the first time in strepsirrhines, isolate and visualize their constituent muscle fasciclesin situand in three dimensions. Using these data, we report muscle volumes, forces, and fascicle lengths from each muscle portion, as well as their orientation relative to two standardized anatomical planes. Our findings demonstrate the overbuilt nature of the aye‐aye's masticatory apparatus, in which each muscle possesses an absolutely and relatively larger muscle volume and PCSA than its counterpart in the mongoose lemur. Likewise, for several adductor muscles, aye‐ayes also possess relatively greater fascicle lengths. Finally, we note several unusual features within the lateral pterygoid of the aye‐aye—the muscle most responsible for jaw protrusion—that relate to force maximization and reorientation. As this jaw motion is critical to gouging, we interpret these differences to reflect highly specific specializations that facilitate the aye‐aye's extreme subsistence strategy. Anat Rec, 2019. © 2019 American Association for Anatomy Anat Rec, 303:282–294, 2020. © 2019 American Association for Anatomymore » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Journal Article:
- https://doi.org/10.1002/ar.24233
