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Coming to grips with life upside down: how myosin fiber type and metabolic properties of sloth hindlimb muscles contribute to suspensory function

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Abstract

Sloths exhibit almost obligatory suspensory locomotion and posture. These behaviors require both strength and fatigue resistance, although we previously found muscle fiber type characteristics in the forelimbs of sloths that belied these initial expectations. Based on locomotor roles of the forelimbs versus hindlimbs in propulsion and braking, respectively, sloth hindlimb musculature should be adapted for force production and energy savings by a near homogeneous expression of slow myosin heavy chain (MHC) fibers. This hypothesis was tested by determining MHC fiber type (%) distribution and energy metabolism in the hindlimbs of three-toed (B. variegatus, N = 5) and two-toed (C. hoffmanni, N = 3) sloths. A primary expression of the slow MHC-1 isoform was found in the hindlimbs of both species. Slow MHC fiber type (%) was significantly greater in the flexors of B. variegatus, whereas expression of fast MHC-2A fibers was significantly greater in the extensors of C. hoffmannni. MHC-1 fibers were largest in cross-sectional area (CSA) and comprised the greatest %CSA in each muscle sampled from both species. Enzyme assays showed elevated activity for anaerobic enzymes (CK and LDH) compared with low-to-moderate activity for aerobic enzymes (3-HAD and CS), and only CK activity was related to body size. These findings emphasize a joint stabilization role by the hindlimbs during suspension, especially in smaller three-toed sloths, and suggest that larger two-toed sloths could have muscles further modified for greater power output and/or prolonged arboreal maneuvering. Moreover, modifications to muscle metabolism rather than MHC expression may be more reflective of functional adaptation in sloth limbs.

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Abbreviations

3-HAD:

3-Hydroxyacetyl Co A dehydrogenase

CK:

Creatine kinase

CS:

Citrate synthase

CSA:

Cross-sectional area

LDH:

Lactate dehydrogenase

MHC:

Myosin heavy chain

PFK:

Phosphofructokinase-1

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Acknowledgements

We sincerely thank Gerald Richardson (Dallas World Aquarium) for coordinating the research partnership with The Sloth Sanctuary of Costa Rica. A very special thanks to R. Cliffe (Sloth Conservation Foundation) for coordinating research permits in Costa Rica. Thanks to T. Diggins for assistance with multivariate statistics and M. Womble for editorial suggestions on the original draft, as well as two anonymous reviewers for critical comments that improved this manuscript. We thank B. Chadwell for assistance with dissection; D. Thomas for gel electrophoresis; A. Svenson and T. Rogers for data collection/analysis; and two reviewers for comments on the manuscript draft. Portions of this work were submitted as Masters Thesis by KB Spainhower. Support by Choose Ohio First and University Research Council (URC) funding to MT Butcher. The YSU Office of Research and Department of Biological Sciences provided travel funding to KBS. A Cushwa/Commercial Shearing Fellowship also provided a graduate assistantship (2017–2018) to KBS. Current address for KB Spainhower is the Case Comprehensive Cancer Center, Case Western Reserve University. The YSU Department of Biological Sciences and Choose Ohio First Scholarships Program are also gratefully acknowledged.

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Authors and Affiliations

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

    Kyle B. Spainhower, Allan K. Metz, Abdel-Ruhman S. Yusuf, Lydia E. Johnson & Michael T. Butcher

  2. The Sloth Sanctuary of Costa Rica, Penshurst, Limon, Costa Rica

    Judy A. Avey-Arroyo

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  1. Kyle B. Spainhower
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Contributions

MTB and KBS conception and study design; KBS, AKM, A-R SY, LEJ, and JA A-A performed data collection; KBS, AKM, A-R SY, LEJ, and MTB data analysis and interpretation; KBS and MTB prepared figures; KBS and MTB drafted manuscript: KBS, AKM, A-R SY, LEJ, JA A-A., and MTB edited and revised manuscript; All authors approved the final version of the manuscript. All authors gave final approval of the published version and agree to be accountable for all content therein.

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Correspondence to Michael T. Butcher.

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Communicated by H.V. Carey.

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Spainhower, K.B., Metz, A.K., Yusuf, AR.S. et al. Coming to grips with life upside down: how myosin fiber type and metabolic properties of sloth hindlimb muscles contribute to suspensory function. J Comp Physiol B 191, 207–224 (2021). https://doi.org/10.1007/s00360-020-01325-x

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