Michael C. Granatosky

Gait kinetics of above- and below-branch quadrupedal locomotion in lemurid primates

ABSTRACT For primates and other mammals moving on relatively thin branches, the ability to effectively adopt both above- and below-branch locomotion is seen as critical for successful arboreal locomotion, and has been considered an important step prior to the evolution of specialized suspensory locomotion within our Order. Yet, little information exists on the ways in which limb mechanics change when animals shift from above- to below-branch quadrupedal locomotion. This study tested the hypothesis that vertical force magnitude and distribution do not vary between locomotor modes, but that the propulsive and braking roles of the forelimb change when animals shift from above- to below-branch quadrupedal locomotion. We collected kinetic data on two lemur species (Varecia variegata and Lemur catta) walking above and below an instrumented arboreal runway. Values for peak vertical, braking and propulsive forces as well as horizontal impulses were collected for each limb. When walking below branch, both species demonstrated a significant shift in limb kinetics compared with above-branch movement. The forelimb became both the primary weight-bearing limb and propulsive organ, while the hindlimb reduced its weight-bearing role and became the primary braking limb. This shift in force distribution represents a shift toward mechanics associated with bimanual suspensory locomotion, a locomotor mode unusual to primates and central to human evolution. The ability to make this change is not accompanied by significant anatomical changes, and thus likely represents an underlying mechanical flexibility present in most primates. Highlighted Article: The mechanics of below-branch quadrupedal locomotion in primates is not simply a mirror of above-branch quadrupedal locomotion, but instead shows kinetic similarities that may be related to arm swinging.

Patterns of quadrupedal locomotion in a vertical clinging and leaping primate (Propithecus coquereli) with implications for understanding the functional demands of primate quadrupedal locomotion.

OBJECTIVES Many primates exhibit a suite of characteristics that distinguish their quadrupedal gaits from non-primate mammals including the use of a diagonal sequence gait, a relatively protracted humerus at touchdown, and relatively high peak vertical forces on the hindlimbs compared to the forelimbs. These characteristics are thought to have evolved together in early, small-bodied primates possibly in response to the mechanical demands of navigating and foraging in a complex arboreal environment. It remains unclear, however, whether primates that employ quadrupedalism only rarely demonstrate the common primate pattern of quadrupedalism or instead use the common non-primate pattern or an entirely different mechanical pattern from either group. MATERIALS AND METHODS This study compared the kinematics and kinetics of two habitually quadrupedal primates (Lemur catta and Varecia variegata) to those of a dedicated vertical clinger and leaper (Propithecus coquereli) during bouts of quadrupedal walking. RESULTS All three species employed diagonal sequence gaits almost exclusively, displayed similar degrees of humeral protraction, and exhibited lower vertical peak forces in the forelimbs compared to the hindlimb. DISCUSSION From the data in this study, it is possible to reject the idea that P. coquereli uses a non-primate pattern of quadrupedal walking mechanics. Nor do they use an entirely different mechanical pattern from either most primates or most non-primates during quadrupedal locomotion. These findings provide support for the idea that this suite of characteristics is adaptive for the challenges of arboreal locomotion in primates and that these features of primate locomotion may be basal to the order or evolved independently in multiple lineages including indriids. Am J Phys Anthropol 160:644-652, 2016.

Taxonomic assessment of Alligator Snapping Turtles (Chelydridae: Macrochelys), with the description of two new species from the southeastern United States.

The Alligator Snapping Turtle, Macrochelys temminckii, is a large, aquatic turtle limited to river systems that drain into the Gulf of Mexico. Previous molecular analyses using both mitochondrial and nuclear DNA suggested that Macrochelys exhibits significant genetic variation across its range that includes three distinct genetic assemblages (western, central, and eastern = Suwannee). However, no taxonomic revision or morphological analyses have been conducted previously. In this study, we test previous hypotheses of distinct geographic assemblages by examining morphology, reanalyzing phylogeographic genetic structure, and estimating divergence dating among lineages in a coalescent framework using Bayesian inference. We reviewed the fossil record and discuss phylogeographic and taxonomic implications of the existence of three distinct evolutionary lineages. We measured cranial (n=145) and post-cranial (n=104) material on field-captured individuals and museum specimens. We analyzed 420 base pairs (bp) of mitochondrial DNA sequence data for 158 Macrochelys. We examined fossil Macrochelys from ca. 15-16 million years ago (Ma) to the present to better assess historical distributions and evaluate named fossil taxa. The morphological and molecular data both indicate significant geographical variation and suggest three species-level breaks among genetic lineages that correspond to previously hypothesized genetic assemblages. The holotype of Macrochelys temminckii is from the western lineage. Therefore, we describe two new species as Macrochelys apalachicolae sp. nov. from the central lineage and Macrochelys suwanniensis sp. nov. from the eastern lineage (Suwannee River drainage). Our estimates of divergence times suggest that the most recent common ancestor (MRCA) of M. temminckii (western) and M. apalachicolae (central) existed 3.2-8.9 Ma during the late Miocene to late Pliocene, whereas M. temminckii-M. apalachicolae and M. suwanniensis last shared a MRCA 5.5-13.4 Ma during the mid-Miocene to early Pliocene. Examination of fossil material revealed that the fossil taxon M. floridana is actually a large Chelydra. Our taxonomic revision of Macrochelys has conservation and management implications in Florida, Georgia, and Alabama.

The evolution of vertical climbing in primates: evidence from reaction forces

ABSTRACT Vertical climbing is an essential behavior for arboreal animals, yet limb mechanics during climbing are poorly understood and rarely compared with those observed during horizontal walking. Primates commonly engage in both arboreal walking and vertical climbing, and this makes them an ideal taxa in which to compare these locomotor forms. Additionally, primates exhibit unusual limb mechanics compared with most other quadrupeds, with weight distribution biased towards the hindlimbs, a pattern that is argued to have evolved in response to the challenges of arboreal walking. Here we test an alternative hypothesis that functional differentiation between the limbs evolved initially as a response to climbing. Eight primate species were recorded locomoting on instrumented vertical and horizontal simulated arboreal runways. Forces along the axis of, and normal to, the support were recorded. During walking, all primates displayed forelimbs that were net braking, and hindlimbs that were net propulsive. In contrast, both limbs served a propulsive role during climbing. In all species, except the lorisids, the hindlimbs produced greater propulsive forces than the forelimbs during climbing. During climbing, the hindlimbs tends to support compressive loads, while the forelimb forces tend to be primarily tensile. This functional disparity appears to be body-size dependent. The tensile loading of the forelimbs versus the compressive loading of the hindlimbs observed during climbing may have important evolutionary implications for primates, and it may be the case that hindlimb-biased weight support exhibited during quadrupedal walking in primates may be derived from their basal condition of climbing thin branches. Summary: A comparison of force profiles during walking and climbing across a range of body sizes in primates indicates that as body size increases, a greater functional differentiation of the limbs is exhibited.

Distinct functional roles of primate grasping hands and feet during arboreal quadrupedal locomotion

It has long been thought that quadrupedal primates successfully occupy arboreal environments, in part, by relying on their grasping feet to control balance and propulsion, which frees their hands to test unstable branches and forage. If this interlimb decoupling of function is real, there should be discernible differences in forelimb versus hind limb musculoskeletal control, specifically in how manual and pedal digital flexor muscles are recruited to grasp during arboreal locomotion. New electromyography data from extrinsic flexor muscles in red ruffed lemurs (Varecia rubra) walking on a simulated arboreal substrate reveal that toe flexors are activated at relatively higher levels and for longer durations than finger flexors during stance phase. This demonstrates that the extremities of primates indeed have different functional roles during arboreal locomotion, with the feet emphasizing maintenance of secure grips. When this dichotomous muscle activity pattern between the forelimbs and hind limbs is coupled with other features of primate quadrupedal locomotion, including greater hind limb weight support and the use of diagonal-sequence footfall patterns, a complex suite of biomechanical characters emerges in primates that allow for the co-option of hands toward non-locomotor roles. Early selection for limb functional differentiation in primates probably aided the evolution of fine manipulation capabilities in the hands of bipedal humans.

Functional and Evolutionary Aspects of Axial Stability in Euarchontans and Other Mammals

The presence of a stable thoracolumbar region, found in many arboreal mammals, is considered advantageous for bridging and cantilevering between discontinuous branches. However, no study has directly explored the link between osteological features cited as enhancing axial stability and the frequency of cantilevering and bridging behaviors in a terminal branch environment. To fill this gap, we collected metric data on costal and vertebral morphology of primate and nonprimate mammals known to cantilever and bridge frequently and those that do not. We also quantified the frequency and duration of cantilevering and bridging behaviors using experimental setups for species that have been reported to show differences in use of small branches and back anatomy (Caluromys philander, Loris tardigradus, Monodelphis domestica, and Cheirogaleus medius). Phylogenetically corrected principal component analysis reveals that taxa employing frequent bridging and cantilevering (C. philander and lorises) also exhibit reduced intervertebral and intercostal spaces, which can serve to increase thoracolumbar stability, when compared to closely related species (M. domestica and C. medius). We observed C. philander cantilevering and bridging significantly more often than M. domestica, which never cantilevered or crossed any arboreal gaps. Although no difference in the frequency of cantilevering was observed between L. tardigradus and C. medius, the duration of cantilevering bouts was significantly greater in L. tardigradus. These data suggest that osteological features promoting axial rigidity may be part of a morpho‐behavioral complex that increases stability in mammals moving and foraging in a terminal branch environment. J. Morphol. 313–327, 2014.

Functional associations between support use and forelimb shape in strepsirrhines and their relevance to inferring locomotor behavior in early primates

The evolution of primates is intimately linked to their initial invasion of an arboreal environment. However, moving and foraging in this milieu creates significant mechanical challenges related to the presence of substrates differing in their size and orientation. It is widely assumed that primates are behaviorally and anatomically adapted to movement on specific substrates, but few explicit tests of this relationship in an evolutionary context have been conducted. Without direct tests of form-function relationships in living primates it is impossible to reliably infer behavior in fossil taxa. In this study, we test a hypothesis of co-variation between forelimb morphology and the type of substrates used by strepsirrhines. If associations between anatomy and substrate use exist, these can then be applied to better understand limb anatomy of extinct primates. The co-variation between each forelimb long bone and the type of substrate used was studied in a phylogenetic context. Our results show that despite the presence of significant phylogenetic signal for each long bone of the forelimb, clear support use associations are present. A strong co-variation was found between the type of substrate used and the shape of the radius, with and without taking phylogeny into account, whereas co-variation was significant for the ulna only when taking phylogeny into account. Species that use a thin branch milieu show radii that are gracile and straight and have a distal articular shape that allows for a wide range of movements. In contrast, extant species that commonly use large supports show a relatively robust and curved radius with an increased surface area available for forearm and hand muscles in pronated posture. These results, especially for the radius, support the idea that strepsirrhine primates exhibit specific skeletal adaptations associated with the supports that they habitually move on. With these robust associations in hand it will be possible to explore the same variables in extinct early primates and primate relatives and thus improve the reliability of inferences concerning substrate use in early primates.

Pliocene–Pleistocene lineage diversifications in the Eastern Indigo Snake (Drymarchon couperi) in the Southeastern United States

Indigo Snakes (Drymarchon; with five currently recognized species) occur from northern Argentina, northward to the United States in southern Texas and eastward in disjunct populations in Florida and Georgia. Based on this known allopatry and a difference in supralabial morphology the two United States taxa previously considered as subspecies within D. corais (Boie 1827), the Western Indigo Snake, D. melanurus erebennus (Cope 1860), and Eastern Indigo Snake, D. couperi (Holbrook 1842), are currently recognized as separate species. Drymarchon couperi is a Federally-designated Threatened species by the United States Fish and Wildlife Service under the Endangered Species Act, and currently being incorporated into a translocation program. This, combined with its disjunct distribution makes it a prime candidate for studying speciation and genetic divergence. In this study, we (1) test the hypothesis that D. m. erebennus and D. couperi are distinct lineages by analyzing 2411 base pairs (bp) of two mitochondrial (mtDNA) loci and one single copy nuclear (scnDNA) locus; (2) estimate the timing of speciation using a relaxed phylogenetics method to determine if Milankovitch cycles during the Pleistocene might have had an influence on lineage diversifications; (3) examine historical population demography to determine if identified lineages have undergone population declines, expansions, or remained stable during the most recent Milankovitch cycles; and (4) use this information to assist in an effective and scientifically sound translocation program. Our molecular data support the initial hypothesis that D. melanurus and D. couperi should be recognized as distinct species, but further illustrate that D. couperi is split into two distinct genetic lineages that correspond to historical biogeography and sea level changes in peninsular Florida. These two well-supported genetic lineages (herein termed Atlantic and Gulf lineages) illustrate a common biogeographic distributional break previously identified for other plants and animals, suggesting that these organisms might have shared a common evolutionary history related to historic sea level changes caused by Milankovitch cycles. Our estimated divergence times suggest that the most recent common ancestor (MRCA) between D. melanurus and southeastern United States Drymarchon occurred ca. 5.9Ma (95% HPD=2.5-9.8Ma; during the late Blancan of the Pleistocene through the Hemphillian of the Miocene), whereas the MRCA between the Atlantic and Gulf lineages in the southeastern United States occurred ca. 2.0Ma (95% HPD=0.7-3.7Ma; during the Irvingtonian of the Pleistocene through the Blancan of the Pliocene). During one or more glacial intervals within these times, these two lineages must have become separated and evolved independently. Despite numerous Milankovitch cycles along with associated forming of physical barriers (i.e., sea level fluctuations, high elevation sand ridges, clayey soils, and/or insufficient habitats) since their initial lineage diversification, these two lineages have likely come in and out of contact with each other many times, yet today they still illustrate near discrete geographic distributions. Although the Atlantic and Gulf lineages appear to be cryptic, a thorough study examining morphological characters should be conducted. We believe that our molecular data is crucial and should be incorporated in making conscious decisions in the management of a translocation program. We suggest that source populations for translocations include maintaining the integrity of the known genetic lineages found herein, as well as those coming from the closest areas that currently support sizable Drymarchon populations.

Ontogeny of material stiffness heterogeneity in the macaque mandibular corpus.

Evidence is accumulating that bone material stiffness increases during ontogeny, and the role of elastic modulus in conditioning attributes of strength and toughness is therefore a focus of ongoing investigation. Developmental changes in structural properties of the primate mandible have been documented, but comparatively little is known about changes in material heterogeneity and their impact on biomechanical behavior. We examine a cross-sectional sample of Macaca fascicularis (N = 14) to investigate a series of hypotheses that collectively evaluate whether the patterning of material stiffness (elastic modulus) heterogeneity in the mandible differs among juvenile, subadult and adult individuals. Because differences in age-related activity patterns are known to influence bone stiffness and strength, these data are potentially useful for understanding the relationship between feeding behavior on the one hand and material and structural properties of the mandible on the other. Elastic modulus is shown to be spatially dependent regardless of age, with this dependence being explicable primarily by differences in alveolar versus basal cortical bone. Elastic modulus does not differ consistently between buccal and lingual cortical plates, despite likely differences in the biomechanical milieu of these regions. Since we found only weak support for the hypothesis that the spatial patterning of heterogeneity becomes more predictable with age, accumulated load history may not account for regional differences in bone material properties in mature individuals with respect to the mandibular corpus.

Patterns, Variability, and Flexibility of Hand Posture During Locomotion in Primates

Primates are defined, in part, by the presence of a grasping hand that couples primitive anatomy with exceptional neuromuscular dexterity. This arrangement is maintained across the evolutionary history of primates, and is often seen as one of the key features that allow primates to make fluid transitions from one substrate to another, make kinematic adjustments with changes in speed and gait, and to make biomechanical adjustments throughout ontogeny. This chapter surveys the exceptional diversity of primate hand positions across locomotor modes, and provides a perspective on the organization of hand positioning based on underlying biomechanical similarities. Across primates, hand positions are highly variable, and multiple solutions to same locomotor challenges are observed. This mechanical flexibility appears to be an adaptive feature of the primate hand, and suggests much of the success of the primate radiation has to do with maintaining generalized ‘cheiridial compromise’ that allows locomotor versatility.