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Architectural Properties of Sloth Forelimb Muscles (Pilosa: Bradypodidae)

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Abstract

Tree sloths have reduced skeletal muscle mass, and yet they are able to perform suspensory behaviors that require both strength and fatigue resistance to suspend their body mass for extended periods of time. The muscle architecture of sloths is hypothesized to be modified in ways that will enhance force production to compensate for this reduction in limb muscle mass. Our objective is to test this hypothesis by quantifying architecture properties in the forelimb musculature of the brown-throated three-toed sloth (Bradypus variegatus: N = 4). We evaluated architecture from 52 forelimb muscles by measuring muscle moment arm (r m), muscle mass (MM), belly length (ML), fascicle length (LF), pennation angle (θ), and physiological cross-sectional area (PCSA), and these metrics were used to estimate isometric force, joint torque, and power. Overall, the musculature becomes progressively more pennate from the extrinsic to intrinsic regions of the forelimb, and the flexors are more well developed than the extensors as predicted. However, most muscles are indicative of a mechanical design for fast joint rotational velocity instead of large joint torque (i.e., strength), although certain large, parallel-fibered shoulder (e.g., m. latissimus dorsi) and elbow (e.g., m. brachioradialis) flexors are capable of producing appreciable torques by having elongated moment arms. This type of functional tradeoff between joint rotational velocity and mechanical advantage is further exemplified by muscle gearing in Bradypus that pairs synergistic muscles with opposing LF/r m ratios in each functional group. These properties are suggested to facilitate the slow, controlled movements in sloths. In addition, the carpal/digital flexors have variable architectural properties, but their collective PCSA and joint torque indicates the capability for maintaining grip force and carpal stability while distributing load from the manus to the shoulder. The observed specializations provide a basis for understanding sustained suspension in sloths.

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Acknowledgments

We sincerely thank Judy Avey-Arroyo and Gerald Richardson for their research partnership with The Sloth Sanctuary of Costa Rica and access to frozen sloth specimens. We also thank the entire staff at The Sloth Sanctuary for making us very comfortable during our stay. A very special thanks to Regan Falin for the anatomical illustrations. Thanks to Sarah Kennedy and Dylan Thomas for assistance with data collection and photography. Support by the American Society of Mammalogists (ASM) Grants-in-Aid of Research (GIAR) funding to RA Olson. The YSU College of STEM also provided travel funding to ZD Glenn (current address: Ohio University College of Osteopathic Medicine). The YSU Department of Biological Sciences, Ohio University Department of Biological Sciences, and Swansea University Department of Biosciences are also gratefully acknowledged.

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Authors and Affiliations

  1. Department of Biological Sciences, Ohio University, Athens, OH, USA

    Rachel A. Olson

  2. Department of Biological Sciences, Youngstown State University, 4013 Ward Beecher Science Hall, Youngstown, OH, 44555, USA

    Zachary D. Glenn & Michael T. Butcher

  3. Department of Biosciences, Swansea University, Wales, UK

    Rebecca N. Cliffe

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  1. Rachel A. Olson
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Correspondence to Michael T. Butcher.

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Supplemental Fig 1

Mean summed physiological cross-sectional area (PCSA) distribution across selected functional muscle groups in the forelimb of B. variegatus. Data shown are only for adult individuals. The functional muscle groups are bracketed by their actions at each major limb joint and include the total summed PCSA (in cm2) for each subgroup. Bars are means ± SD (N = 3). (GIF 71 kb)

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Olson, R.A., Glenn, Z.D., Cliffe, R.N. et al. Architectural Properties of Sloth Forelimb Muscles (Pilosa: Bradypodidae). J Mammal Evol 25, 573–588 (2018). https://doi.org/10.1007/s10914-017-9411-z

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