Mechanical and morphometric approaches to body mass estimation in rhesus macaques: A test of skeletal variables.

OBJECTIVES: Estimation of body mass from skeletal metrics can reveal important insights into the paleobiology of archeological or fossil remains. The standard approach constructs predictive equations from postcrania, but studies have questioned the reliability of traditional measures. Here, we examine several skeletal features to assess their accuracy in predicting body mass. MATERIALS AND METHODS: Antemortem mass measurements were compared with common skeletal dimensions from the same animals postmortem, using 115 rhesus macaques (male: n = 43; female: n = 72). Individuals were divided into training (n = 58) and test samples (n = 57) to build and assess Ordinary Least Squares or multivariate regressions by residual sum of squares (RSS) and AIC weights. A leave-one-out approach was implemented to formulate the best fit multivariate models, which were compared against a univariate and a previously published catarrhine body-mass estimation model. RESULTS: Femur circumference represented the best univariate model. The best model overall was composed of four variables (femur, tibia and fibula circumference and humerus length). By RSS and AICw, models built from rhesus macaque data (RSS = 26.91, AIC = -20.66) better predicted body mass than did the catarrhine model (RSS = 65.47, AIC = 20.24). CONCLUSION: Body mass in rhesus macaques is best predicted by a 4-variable equation composed of humerus length and hind limb midshaft circumferences. Comparison of models built from the macaque versus the catarrhine data highlight the importance of taxonomic specificity in predicting body mass. This paper provides a valuable dataset of combined somatic and skeletal data in a primate, which can be used to build body mass equations for fragmentary fossil evidence.

Quantifying the relationship between bone and soft tissue measures within the rhesus macaques of Cayo Santiago.

OBJECTIVES: Interpretations of the primate and human fossil record often rely on the estimation of somatic dimensions from bony measures. Both somatic and skeletal variation have been used to assess how primates respond to environmental change. However, it is unclear how well skeletal variation matches and predicts soft tissue. Here, we empirically test the relationship between tissues by comparing somatic and skeletal measures using paired measures of pre- and post-mortem rhesus macaques from Cayo Santiago, Puerto Rico. MATERIALS AND METHODS: Somatic measurements were matched with skeletal dimensions from 105 rhesus macaque individuals to investigate paired signals of variation (i.e., coefficients of variation, sexual dimorphism) and bivariate codependence (reduced major axis regression) in measures of: (1) limb length; (2) joint breadth; and (3) limb circumference. Predictive models for the estimation of soft tissue dimensions from skeletons were built from Ordinary Least Squares regressions. RESULTS: Somatic and skeletal measurements showed statistically equivalent coefficients of variation and sexual dimorphism as well as high epiphyses-present ordinary least square (OLS) correlations in limb lengths (R2 >0.78, 0.82), joint breadths (R2 >0.74, 0.83) and, to a lesser extent, limb circumference (R2 >0.53, 0.68). CONCLUSION: Skeletal measurements are good substitutions for somatic values based on population signals of variation. OLS regressions indicate that skeletal correlates are highly predictive of somatic dimensions. The protocols and regression equations established here provide a basis for reliable reconstruction of somatic dimension from catarrhine fossils and validate our ability to compare or combine results of studies based on population data of either hard or soft tissue proxies.

Skeletal age during hurricane impacts fluctuating asymmetry in Cayo Santiago rhesus macaques.

As natural disasters become more frequent due to climate change, understanding the biological impact of these ecological catastrophes on wild populations becomes increasingly pertinent. Fluctuating asymmetry (FA), or random deviations from bilateral symmetry, is reflective of developmental instability and has long been positively associated with increases in environmental stress. This study investigates craniofacial FA in a population of free-ranging rhesus macaques (Macaca mulatta) that has experienced multiple Category 3 hurricanes since the colony's inception on Cayo Santiago, including 275 individuals from ages 9 months to 31 years (F = 154; M = 121). Using geometric morphometrics to quantify FA and a linear mixed-effect model for analysis, we found that sex, age, and decade of birth did not influence the amount of FA in the individuals included in the study, but the developmental stage at which individuals experienced these catastrophic events greatly impacted the amount of FA exhibited (p = .001). Individuals that experienced these hurricanes during fetal life exhibited greater FA than any other post-natal developmental period. These results indicate that natural disasters can be associated with developmental disruption that results in long-term effects if occurring during the prenatal period, possibly due to increases in maternal stress-related hormones.

A medida que los desastres naturales se vuelven más frecuentes debido al cambio climático, entender el impacto biológico de estas catástrofes ecológicas en poblaciones silvestres va en aumento pertinente. La asimetría fluctuante (AF), o desviaciones aleatorias de simetría bilateral, es reflejo de inestabilidad durante el desarrollo y se ha asociado positivamente con incrementos en estrés ambiental durante mucho tiempo. Este estudio investiga AF craneofacial en una población de macacos rhesus (Macaca mulatta) en libertad que ha experimentado múltiples huracanes categoría 3 desde el inicio de la colonia en Cayo Santiago, e incluye 275 individuos de 9 meses a 31 años de edad (F = 154; M = 121). Usando morfometría geométrica para cuantificar AF y un modelo lineal de efectos mixtos para análisis, encontramos que el sexo, la edad y la década de nacimiento no influyeron en la cantidad de AF en los individuos incluidos en el estudio, pero la etapa de desarrollo en la que los individuos experimentaron estos eventos catastróficos impactó altamente la cantidad de AF exhibida (p = .001). Los individuos que experimentaron estos huracanes durante el período fetal exhibieron mayor AF que cualquier otro período de desarrollo posnatal. Estos resultados indican que los desastres naturales pueden asociarse con trastornos del desarrollo que tienen efectos a largo plazo si ocurren durante el período prenatal, posiblemente debido al aumento de hormonas maternas relacionadas con el estrés.

The ontogeny of sexual dimorphism in free-ranging rhesus macaques.

Objective: Reconstructing the social lives of extinct primates is possible only through an understanding of the interplay between morphology, sexual selection pressures, and social behavior in extant species. Somatic sexual dimorphism is an important variable in primate evolution, in part because of the clear relationship between the strength and mechanisms of sexual selection and the degree of dimorphism. Here, we examine body size dimorphism across ontogeny in male and female rhesus macaques to assess whether it is primarily achieved via bimaturism as predicted by a polygynandrous mating system, faster male growth indicating polygyny, or both. Methods: We measured body mass in a cross-sectional sample of 364 free-ranging rhesus macaques from Cayo Santiago, Puerto Rico to investigate size dimorphism: 1) across the lifespan; and 2) as an outcome of sex-specific growth strategies, including: a) age of maturation; b) growth rate; and c) total growth duration, using regression models fit to sex-specific developmental curves. Results: Significant body size dimorphism was observed by prime reproductive age with males 1.51 times the size of females. Larger male size resulted from a later age of maturation (males: 6.8-7.8 years versus females: 5.5-6.5 years; logistic model) and elevated growth velocity through the pre-prime period (LOESS model). Though males grew to larger sizes overall, females maintained adult size for longer before senescence (quadratic model). Discussion: The ontogeny of size dimorphism in rhesus macaques is achieved by bimaturism and a faster male growth rate. Our results provide new data for understanding the development and complexities of primate dimorphism.

Muscle attachment sites and behavioral reconstruction: An experimental test of muscle-bone structural response to habitual activity.

OBJECTIVE: Behavioral reconstruction from muscle attachment sites (entheses) is a common practice in anthropology. However, experimental evidence provides mixed support for the assumed association between enthesis size and shape with changes in habitual activity. In this study, a laboratory mouse model was used to experimentally test whether activity level and type alters muscle architecture and the underlying bone cross-sectional geometry of entheses in order to assess the underlying assumption that behavioral changes lead to quantifiable differences in both muscle and enthesis morphology. MATERIALS AND METHODS: Female wild-type mice were separated into one control group and two experimentally increased activity groups (running, climbing) over an 11-week study period. At the start of the experiment, half of the mice were 4 weeks and half were 7 weeks of age. The postmortem deltoideus and biceps brachii muscles were measured for potential force production (physiological cross-sectional area) and potential muscle excursion (fiber length). Bone cross-sectional geometry variables were measured from microCT scans of the humerus and radius at the enthesis and non-enthesis regions of interest across activity groups. RESULTS: Activity level and type altered potential force production and potential muscle excursion of both muscles in the younger cohort. We observed differences in cortical bone geometry in both the humerus enthesis and radius non-enthesis region driven exclusively among the younger wheel-running mice. DISCUSSION: These results indicate that in addition to muscle architectural changes, bone structural properties at the enthesis do show an adaptive response to increased activity, such as running but only during earlier development. However, further research is required in order to apply these findings to the reconstruction of living behavior from anthropological specimens.

Evaluating bony predictors of bite force across the order Carnivora.

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.

Elevated activity levels do not influence extrinsic fiber attachment morphology on the surface of muscle-attachment sites.

Extrinsic fibers (EFs) are a type of penetrating collagenous fiber, closely related to the periodontal ligament, which help anchor soft tissue into bone. These fibers are associated with muscle attachment sites (entheses). Their size and grouping patterns are thought to be indicative of the loading history of the muscle. EFs are of particular significance in anthropology as potential tools for the reconstruction of behavior from skeletal remains and, specifically, entheses. In this study, we used a mouse model to experimentally test how activity level alters the morphology of EF insertion sites on the bone surface of a fibrocartilaginous enthesis, the biceps brachii insertion. Further, we adapted surface metrological techniques from studies of dental wear to perform automated, quantitative and non-destructive analysis of bone surface histology. Our results show that experimentally increased activity had no significant effect on the quantity or density of EF insertions at the enthesis, nor on the size of those insertions. Although EF presence does indicate muscle attachment, activity did not have an observable effect on EF morphology.