Tree Gouging Research Articles

The Ontogeny of Masticatory Muscle Architecture in Microcebus murinus

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 murinus including 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 Anatomy.

The Ontogeny of Masticatory Muscle Architecture in Microcebus murinus

Many studies pertaining to the masticatory apparatus have focused on the mandibular adductors (the temporalis, masseter, and medial pterygoid) ‐ the muscles that work cooperatively to produce bite force. Specifically, the architectural properties of these muscles have been correlated with diet. For instance, felids that eat relatively large prey have relatively longer fascicles to allow for the necessary gape. Primate diet also correlates with muscle architecture and, in some instances (e.g., tree gouging in Callithrix), the mode of foraging. However, there is little known about the ontogenetic development of these muscles. To characterize age‐related changes, we used an intraspecific sample of 28 specimens from a captive colony, spanning the entire lifespan of the small Malagasy primate, Microcebus murinus.We dissected each of the jaw adductors and obtained their masses as well as linear morphometrics. We then chemically dissected them using 35% nitric acid for 15–30 hours until their constituent fascicles could be separated. Then the reaction was neutralized in 50% glycerol and fascicles were photographed and measured using ImageJ (NIH) and all logged variables were statistically analyzed in JMP (SAS).A quadratic curvilinear model is significant when muscle mass is regressed against age with p‐values <0.01 for each adductor. The trends demonstrate that the muscle mass of the adductors peak during early to mid‐adulthood with a point of inflection occurring at late adulthood to early senescence. When physiological cross‐sectional area (PCSA) is scaled against age, a quadratic model represents the data significantly better for the masseter and medial pterygoid with p‐values <0.01. However, a linear model is more appropriate when characterizing changes in the PCSA of temporalis as the quadratic model was found to be insignificant. The general trend for changes in PCSA for masseter and medial pterygoid are consistent with the patterns observed in muscle mass, but temporalis PCSA does not appear to atrophy significantly with age. When fiber length is scaled against age for each mandibular adductor, the curvilinear relationship was observed to be a good fit with p‐values <0.05. However, for the temporalis and medial pterygoid this trend appears to be driven by the inclusion of a low outlier. When this specimen is excluded, the trend line is horizontal suggesting that, once fiber length reaches maximum length early in life, it remains relatively constant. The trend for medial pterygoid also suggests that fiber length peaks early in life; however, it also indicates a point of inflection occurring in early adulthood.From these results, representing the most complete ontogenetic sample of primate masticatory muscle architecture, we have successfully characterized myological changes across the lifespan of M. murinus. Our findings suggest that the changes in PCSA are driven mostly by changes in muscle mass including growth through early adulthood and slight but clear reduction into senescence, while masticatory fascicle lengths remain surprisingly constant throughout life.Support or Funding InformationThis project was supported by the NSF (IOS‐15‐57125 and BCS‐14‐40599).This abstract is from the Experimental Biology 2019 Meeting. There is no full text article associated with this abstract published in The FASEB Journal.

Accessing foods can exert multiple distinct, and potentially competing, selective pressures on feeding in common marmoset monkeys

AbstractAnimals must overcome the physical properties protecting foods to obtain nutrition. While animals can experience selection for traits that facilitate resource exploitation, specific feeding behaviors may entail multiple, different mechanical challenges with each potentially eliciting distinct selection pressures. Tree gouging by common marmosets (Primates: Callithrix jacchus) provides an illustrative case for studying these distinct mechanical challenges and their correlated behaviors and morphologies. We test the hypothesis that marmosets respond differently to three sequential mechanical stages of bark removal: (1) indentation; (2) crack initiation; (3) crack propagation. By surveying trees gouged by free‐ranging marmosets in Pernambuco, Brazil, we found that mechanical variables related to crack initiation (fracture toughness, critical strain energy release rate and elastic modulus) were inversely correlated with measures of gouging intensity, with less mechanically challenging trees being gouged more intensely. Because crack initiation is likely the most mechanically challenging aspect of tree gouging, behavioral preference for less challenging resources likely allows marmosets to reduce costs and potential risks associated with accessing exudates. Variables related to bark indentation (hardness and friction) showed no relationship to the intensity of gouging behavior. Contrary to our prediction, trees with greater mechanical challenges for crack propagation (work to peel) were gouged more intensely. We attribute this pattern of gouging trees requiring greater effort in crack propagation to an inverse correlation between work to peel and fracture toughness in our tree sample. Importantly, marmosets exhibit morphological specializations of the feeding apparatus that facilitate indentation and crack propagation, potentially mitigating the need for behavioral choice. Here we show that extracting a single food resource can exert a series of distinct, potentially competing, selective forces during resource acquisition. This study illustrates how animals combine behaviors and morphological specializations to competently overcome distinct mechanical challenges, emphasizing the need for holistic approaches in understanding feeding adaptations.

The functional morphology of the anterior masticatory apparatus in tree‐gouging marmosets (cebidae, primates)

Although all genera of Callitrichinae feed on tree exudates, marmosets (Callithrix and Cebuella) use specialized anterior teeth to gouge holes in trees and actively stimulate exudate flow. Behavioral studies demonstrate that marmosets use large jaw gapes but do not appear to generate large bite forces (relative to maximal ability) during gouging. Nonetheless, the anterior teeth of marmosets likely experience different loads during gouging compared to nongouging platyrrhines. We use histological data from sectioned teeth, μCTs of jaws and teeth, and in vitro tests of symphyseal strength to compare the anterior masticatory apparatus in Callithrix to nongouging tamarins (Saguinus) and other cebids. We test the hypotheses that (1) marmoset anterior teeth are adapted to accommodate relatively high stresses linked to dissipating gouging forces and (2) the mandibular symphysis does not provide increased load resistance ability compared with closely related nongouging platyrrhines. Differences in decussation between Callithrix and Saguinus are greatest in the anterior teeth, suggesting an increased load resistance ability specifically in incisor and canine enamel of Callithrix. Callithrix lower incisor crowns are labiolingually thicker suggesting increased bending resistance in this plane and improved wedging ability compared with Saguinus. Anterior tooth roots are larger relative to symphyseal bone volume in Callithrix. Anterior tooth root surface areas also are larger in marmosets for their symphyseal volume, but it remains unclear whether this relative increase is an adaptation for dissipating dental stresses versus a growth-related byproduct of relatively elongated incisors. Finally, simulated jaw loading suggests a reduced ability to withstand external forces in the Callithrix symphysis. The contrast between increased load resistance ability in the anterior dentition versus relatively reduced symphyseal strength (1) suggests a complex loading environment during gouging, (2) highlights the possibility of distinct loading patterns in the anterior teeth versus the symphysis, and (3) points to a potential mosaic pattern of dentofacial adaptations to tree gouging.

Does nonnutritive tree gouging in a rainforest‐dwelling lemur convey resource ownership as does loud calling in a dry forest‐dwelling lemur?

Nonhuman primates may defend crucial resources using acoustic or chemical signals. When essential resources are limited, ownership display for a resource may be enhanced. Defending resources may depend on population density and habitat characteristics. Using the Milne Edwards' sportive lemurs (Lepilemur edwardsi) and weasel sportive lemurs (L. mustelinus) as models, we tested whether two cryptic nocturnal lemur species differing in population density and habitat show differences in their vocal and chemical communication for signaling ownership of resources. L. edwardsi inhabits a western dry deciduous forest in a high-density population, whereas L. mustelinus is found in an eastern rainforest in low density. We followed ten L. edwardsi (six males and four females) and nine L. mustelinus (four males and five females) for 215 hr during the early evening (06:00-10:00 p.m.) and the early morning (02:00-05:00 a.m.) and recorded their behavior using focal animal sampling. We found that both species differed in their vocal and chemical communication. L. edwardsi was highly vocal and displayed loud calling in the mornings and evenings while feeding or in the vicinity of resting places. In contrast, L. mustelinus never vocalized during observations, but displayed tree-gouging behavior that was never observed in L. edwardsi. Tree gouging occurred more often during early evening sessions than early morning sessions. Subjects gouged trees after leaving their sleeping hole and before moving around. We suggest that, in weasel sportive lemurs, non-nutritive tree gouging is used as a scent-marking behavior in order to display ownership of sleeping sites. Altogether, our findings provide first empirical evidence on the evolution of different communication systems in two cryptic nocturnal primate species contrasting in habitat quality and population density. Further investigations are needed to provide more insight into the underlying mechanisms.

The functional correlates of jaw‐muscle fiber architecture in primates

The jaw muscles are responsible for generating jaw forces and movements yet surprisingly little is known about the architecture of these muscles in primates. To better understand the relationship among jaw‐muscle fiber architecture, feeding behavior, and diet, we evaluated and compared masseter and temporalis fiber architecture in marmosets (Callithrix jacchus, Cebuella pygmaea), tamarins (Saguinus oedipus), capuchins (Cebus sp), and large‐bodied hominoids. Muscles were removed en masse from the skull, weighed, and whole muscle and fiber lengths measured. We computed pinnation angles and physiologic cross‐sectional areas (PCSAs). In some cases, fiber architecture differences can be predictably linked to functional and adaptive differences in feeding behavior. Thus, the relatively longer, less pinnate‐fibered muscles in tree‐gouging marmosets compared to nongouging tamarins can be functionally linked to the production of relatively wide jaw gapes during tree gouging. Likewise, C. apella displays relatively larger PCSAs compared to other capuchins, consistent with their occasional exploitation of exceptionally resistant foods. Fiber architecture, however, fails to predict differences in feeding behavior and diet among hominoids. We discuss the implications for reconstructing feeding behavior and diet in extinct taxa. Grant sponsor: NSF; Grant numbers: BCS‐0452160, BCS‐0094666, BCS‐0412153; Grant sponsor: NIH; Grant number: R24 HD050837; Grant sponsor: Duke Undergraduate Research Support and the Biology Research Forum of Trinity College.

The morphology of the masticatory apparatus facilitates muscle force production at wide jaw gapes in tree-gouging common marmosets (Callithrix jacchus)

Common marmosets (Callithrix jacchus) generate wide jaw gapes when gouging trees with their anterior teeth to elicit tree exudate flow. Closely related cotton-top tamarins (Saguinus oedipus) do not gouge trees but share similar diets including exudates. Maximizing jaw opening theoretically compromises the bite forces that marmosets can generate during gouging. To investigate how jaw-muscle architecture and craniofacial position impact muscle performance during gouging, we combine skull and jaw-muscle architectural features to model muscle force production across a range of jaw gapes in these two species. We incorporate joint mechanics, resting sarcomere length and muscle architecture estimates from the masseter and temporalis to model muscle excursion, sarcomere length and relative tension as a function of joint angle. Muscle excursion from occlusion to an estimated maximum functional gape of 55 deg. was smaller in all regions of the masseter and temporalis of C. jacchus compared with S. oedipus except the posterior temporalis. As a consequence of reduced muscle excursion distributed over more sarcomeres in series (i.e. longer fibers), sarcomere length operating ranges are smaller in C. jacchus jaw muscles across this range of gapes. This configuration allows C. jacchus to act on a more favorable portion of the length-tension curve at larger gapes and thereby generate relatively greater tension in these muscles compared with S. oedipus. Our results suggest that biting performance during tree gouging in common marmosets is improved by a musculoskeletal configuration that reduces muscle stretch at wide gapes while simultaneously facilitating comparatively large muscle forces at the extremes of jaw opening.

The functional correlates of jaw‐muscle fiber architecture in tree‐gouging and nongouging callitrichid monkeys

Common (Callithrix jacchus) and pygmy (Cebuella pygmaea) marmosets and cotton-top tamarins (Saguinus oedipus) share broadly similar diets of fruits, insects, and tree exudates. Marmosets, however, differ from tamarins in actively gouging trees with their anterior dentition to elicit tree exudates flow. Tree gouging in common marmosets involves the generation of relatively wide jaw gapes, but not necessarily relatively large bite forces. We compared fiber architecture of the masseter and temporalis muscles in C. jacchus (N = 18), C. pygmaea (N = 5), and S. oedipus (N = 13). We tested the hypothesis that tree-gouging marmosets would exhibit relatively longer fibers and other architectural variables that facilitate muscle stretch. As an architectural trade-off between maximizing muscle excursion/contraction velocity and muscle force, we also tested the hypothesis that marmosets would exhibit relatively less pinnate fibers, smaller physiologic cross-sectional areas (PCSA), and lower priority indices (I) for force. As predicted, marmosets display relatively longer-fibered muscles, a higher ratio of fiber length to muscle mass, and a relatively greater potential excursion of the distal tendon attachments, all of which favor muscle stretch. Marmosets further display relatively smaller PCSAs and other features that reflect a reduced capacity for force generation. The longer fibers and attendant higher contraction velocities likely facilitate the production of relatively wide jaw gapes and the capacity to generate more power from their jaw muscles during gouging. The observed functional trade-off between muscle excursion/contraction velocity and muscle force suggests that primate jaw-muscle architecture reflects evolutionary changes related to jaw movements as one of a number of functional demands imposed on the masticatory apparatus.

Cross-sectional Bone Distribution in the Mandibles of Gouging and Non-gouging Platyrrhini

Recent morphometric analyses have led to dissimilar conclusions about whether the jaws of tree-gouging primates are designed to resist the purportedly large forces generated during this biting behavior. We further address this question by comparing the cross-sectional geometry of the mandibular corpus and symphysis in tree-gouging common marmosets (Callithrix jacchus) to nongouging saddleback tamarins (Saguinus fuscicollis) and squirrel monkeys (Saimiri sciureus). As might be expected, based on size, squirrel monkeys tend to have absolutely larger cross-sectional areas at each tooth location sampled, while saddleback tamarins are intermediate, followed by the smaller common marmosets. Similarly, the amount and distribution of cortical bone in squirrel monkey jaws provides them with increased ability to resist sagittal bending (I xx ) and torsion (K) in the corpus as well as coronal bending (I xx ) and shearing in the symphysis. However, when the biomechanical parameters are scaled to respective load arm estimates, there are few significant differences in relative resistance abilities among the 3 species. A power analysis indicates that we cannot statistically rule out subtle changes in marmoset jaw form linked to resisting loads during gouging. Nevertheless, our results correspond to studies in vivo of jaw loading, field data, and other comparative analyses suggesting that common marmosets do not generate relatively large bite forces during tree gouging. The 3 species are like most other anthropoids in having thinner bone on the lingual than on the buccal side of the mandibular corpus at M1. The similarity in corporal shape across anthropoids supports a hypothesized stereotypical pattern of jaw loading during chewing and may indicate a conserved pattern of mandibular growth for the suborder. Despite the overall similarity, platyrrhines may differ slightly from catarrhines in the details of their cortical bone distribution.

Comparative functional analysis of skull morphology of tree-gouging primates.

Many primates habitually feed on tree exudates such as gums and saps. Among these exudate feeders, Cebuella pygmaea, Callithrix spp., Phaner furcifer, and most likely Euoticus elegantulus elicit exudate flow by biting into trees with their anterior dentition. We define this behavior as gouging. Beyond the recent publication by Dumont ([1997] Am J Phys Anthropol 102:187-202), there have been few attempts to address whether any aspect of skull form in gouging primates relates to this specialized feeding behavior. However, many researchers have proposed that tree gouging results in larger bite force, larger internal skull loads, and larger jaw gapes in comparison to other chewing and biting behaviors. If true, then we might expect primate gougers to exhibit skull modifications that provide increased abilities to produce bite forces at the incisors, withstand loads in the skull, and/or generate large gapes for gouging. We develop 13 morphological predictions based on the expectation that gouging involves relatively large jaw forces and/or jaw gapes. We compare skull shapes for P. furcifer to five cheirogaleid taxa, E. elegantulus to six galagid species, and C. jacchus to two tamarin species, so as to assess whether gouging primates exhibit these predicted morphological shapes. Our results show little morphological evidence for increased force-production or load-resistance abilities in the skulls of these gouging primates. Conversely, these gougers tend to have skull shapes that are advantageous for creating large gapes. For example, all three gouging species have significantly lower condylar heights relative to the toothrow at a given mandibular length in comparison with closely related, nongouging taxa. Lowering the height of the condyle relative to the mandibular toothrow should reduce the stretching of the masseters and medial pterygoids during jaw opening, as well as position the mandibular incisors more anteriorly at wide jaw gapes. In other words, the lower incisors will follow a more vertical trajectory during both jaw opening and closing. We predict, based on these findings, that tree-gouging primates do not generate unusually large forces, but that they do use relatively large gapes during gouging. Of course, in vivo data on jaw forces and jaw gapes are required to reliably assess skull functions during gouging.

Vertical clinging, small body size, and the evolution of feeding adaptations in the Callitrichinae.

Primates of the subfamily Callitrichinae (Callimico, Callithrix, Leontopithecus, and Saguinus) are small-bodied New World monkeys (105-700 g) possessing clawlike nails on all manual and pedal digits excluding the hallux. Specialized nails in these genera serve a critical function in feeding by enabling tamarins and marmosets to cling to trunks and other large vertical supports while exploiting food resources. Within the subfamily, there is evidence of at least four distinct large-branch feeding patterns. These include (1) seasonal exudate feeding and occasional trunk foraging (many Saguinus spp.); (2) exploitation of bark surface insects and the use of trunks as a platform to locate terrestrial prey (Saguinus fuscicollis, S. nigricollis, and Callimico); (3) manipulative foraging and bark stripping to locate concealed insects and small vertebrates (Leontopithecus); and (4) tree gouging and year-round exudate feeding (many Callithrix). Large-branch feeding and the use of vertical clinging postures appear to be a primary adaptation among virtually all callitrichines, distinguishing them ecologically from other platyrrhine taxa. Given the anatomy and behavior of extant callitrichines, Saguinus appears to be the most ecologically generalized member of this subfamily, and species of this genus may provide useful models for reconstructing the feeding and foraging adaptations of early callitrichines.