Three toes and three modes: Dynamics of terrestrial, suspensory, and vertical locomotion in brown-throated three-toed sloths (Bradypodidae, Xenarthra).


Journal

Journal of experimental zoology. Part A, Ecological and integrative physiology
ISSN: 2471-5646
Titre abrégé: J Exp Zool A Ecol Integr Physiol
Pays: United States
ID NLM: 101710204

Informations de publication

Date de publication:
05 2023
Historique:
revised: 13 01 2023
received: 11 09 2022
accepted: 15 01 2023
medline: 11 4 2023
pubmed: 8 2 2023
entrez: 7 2 2023
Statut: ppublish

Résumé

Living sloths exhibit numerous anatomical specializations towards inverted quadrupedalism, however, previous studies have noted a more varied locomotor repertoire than previously anticipated. In this study, we present spatiotemporal gait characteristics and triaxial kinetic data from the brown-throated three-toed sloth (Bradypus variegatus) across three locomotor modes: terrestrial quadrupedal "crawling", suspensory walking, and vertical climbing. Compared to quadrupedal crawling and suspensory walking, B. variegatus adopted longer contact times and stride durations, larger duty factors, and greater speed during vertical climbing. Net fore-aft impulses were significantly greater during vertical climbing in both limb pairs than in quadrupedal crawling and suspensory walking. Functionally, during quadrupedal crawling and vertical climbing, both limb pairs served propulsive roles, while differentiation between a propulsive forelimb and braking hindlimb was observed during suspension. Net tangential forces differentiated vertical climbing kinetics from the other modes of locomotion, with the introduction of bidirectional pulling and pushing forces in the forelimb and hindlimb, respectively. The net mediolateral impulses were similar in vertical climbing and quadrupedal crawling as both limb pairs directed forces in one direction, whereas during suspensory walking, the laterally dominant forelimb was opposed by the medially dominant hindlimb. In total, this study provides novel data on the diverse locomotor dynamics in a slow-moving arboreal tetrapod and posits new testable hypotheses about the neuroplasticity and ease of transitioning between locomotor behaviors. The strikingly similar kinetic profiles of quadrupedal crawling and suspensory walking compared to vertical climbing suggest shared neuromuscular and mechanical demands between these mirrored locomotor modes.

Identifiants

pubmed: 36747379
doi: 10.1002/jez.2684
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

383-397

Informations de copyright

© 2023 Wiley Periodicals LLC.

Références

Alfieri, F., Nyakatura, J. A., & Amson, E. (2021). Evolution of bone cortical compactness in slow arboreal mammals. Evolution, 75, 542-554.
Anderson, R. P., & Handley, C. O. (2001). A new species of three-toed sloth (Mammalia: Xenarthra) from Panama, with a review of the genus Bradypus. Proceedings-Biological Society of Washington, 114, 1-33.
Autumn, K., Hsieh, S. T., Dudek, D. M., Chen, J., Chitaphan, C., & Full, R. J. (2006). Dynamics of geckos running vertically. Journal of Experimental Biology, 209, 260-272.
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1-48. https://doi.org/10.18637/jss.v067.i01
Beebe, W. (1926). The three-toed sloth Bradypus cuculliger cuculliger Wagler. Zoologica, 7(1), 67.
Berger, S. E., & Adolph, K. E. (2007). Learning and development in infant locomotion. In C. Hofsten & K. Rosander (Eds.), Progress in brain research. From action to cognition (Vol. 164, pp. 237-255). Elsevier. https://www.sciencedirect.com/science/article/pii/S0079612307640138
Bishop, P. J., Graham, D. F., Lamas, L. P., Hutchinson, J. R., Rubenson, J., Hancock, J. A., Wilson, R. S., Hocknull, S. A., Barrett, R. S., Lloyd, D. G., & Clemente, C. J. (2018). The influence of speed and size on avian terrestrial locomotor biomechanics: Predicting locomotion in extinct theropod dinosaurs. PLoS One, 13, e0192172.
Bodnarchuk, J. L., & Eaton, W. O. (2004). Can parent reports be trusted? Journal of Applied Developmental Psychology, 25, 481-490.
Carlson, K. J., Demes, B., & Franz, T. M. (2005). Mediolateral forces associated with quadrupedal gaits of lemurids. Journal of Zoology, 266, 261-273.
Carrillo, E., Fuller, T. K., & Saenz, J. C. (2009). Jaguar (Panthera onca) hunting activity: Effects of prey distribution and availability. Journal of Tropical Ecology, 25, 563-567.
Cartmill, M., Brown, K., Atkinson, C., Cartmill, E. A., Findley, E., Gonzalez-Socoloske, D., Hartstone-Rose, A., & Mueller, J. (2020). The gaits of marsupials and the evolution of diagonal-sequence walking in primates. American Journal of Physical Anthropology, 171, 182-197.
Carvalho, C. de (1960). Notes on the three-toed sloth, Bradypus tridactylus. Mammalia, 24, 155-156.
Chang, Y. H., Bertram, J. E. A., & Lee, D. V. (2000). External forces and torques generated by the brachiating white-handed gibbon (Hylobates lar). American Journal of Physical Anthropology, 113, 201-216.
Demes, B., Larson, S. G., Stern, J. T., Jungers, W. L., Biknevicius, A. R., & Schmitt, D. (1994). The kinetics of primate quadrupedalism: “Hindlimb drive” reconsidered. Journal of Human Evolution, 26, 353-374.
Dickinson, E., Young, M. W., & Granatosky, M. C. (2022). Testing mechanisms for weight support distribution during inverted quadrupedalism in primates. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 337, 699-708.
Fish, F. E., Sheehan, M. J., Adams, D. S., Tennett, K. A., & Gough, W. T. (2021). A 60:40 split: Differential mass support in dogs. The Anatomical Record, 304, 78-89.
Fujiwara, S., Endo, H., & Hutchinson, J. R. (2011). Topsy-turvy locomotion: Biomechanical specializations of the elbow in suspended quadrupeds reflect inverted gravitational constraints. Journal of Anatomy, 219, 176-191.
Garcés-Restrepo, M. F., Pauli, J. N., & Peery, M. Z. (2018). Natal dispersal of tree sloths in a human-dominated landscape: Implications for tropical biodiversity conservation. Journal of Applied Ecology, 55, 2253-2262.
Gonzalez, C. L. R., & Sacrey, L.-A. R. (2018). Chapter 9 - The development of the motor system. In R. Gibb, & B. Kolb (Eds.), The neurobiology of brain and behavioral development (pp. 235-256). Academic Press. https://www.sciencedirect.com/science/article/pii/B9780128040362000091
Gorvet, M. A., Wakeling, J. M., Morgan, D. M., Hidalgo Segura, D., Avey-Arroyo, J., & Butcher, M. T. (2020). Keep calm and hang on: EMG activation in the forelimb musculature of three-toed sloths (Bradypus variegatus). Journal of Experimental Biology, 223, jeb218370.
Granatosky, M. C. (2016). A mechanical analysis of suspensory locomotion in primates and other mammals (Dissertations). Duke University.
Granatosky, M. C. (2018). Forelimb and hindlimb loading patterns during quadrupedal locomotion in the large flying fox (Pteropus vampyrus) and common vampire bat (Desmodus rotundus). Journal of Zoology, 305, 63-72.
Granatosky, M. C., Amanat, S., Panyutina, A. A., & Youlatos, D. (2021). Gait mechanics of a blind echolocating rodent: Implications for the locomotion of small arboreal mammals and proto-bats. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 335, 436-453.
Granatosky, M. C., Fitzsimons, A., Zeininger, A., & Schmitt, D. (2018a). Mechanisms for the functional differentiation of the propulsive and braking roles of the forelimbs and hindlimbs during quadrupedal walking in primates and felines. Journal of Experimental Biology, 221, 1-11.
Granatosky, M. C., Karantanis, N. E., Rychlik, L., & Youlatos, D. (2018b). A suspensory way of life: integrating locomotion, postures, limb movements, and forces in two-toed sloths Choloepus didactylus (Megalonychidae, Folivora, Pilosa). Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 329, 570-588.
Granatosky, M. C., & McElroy, E. J. (2022). Stride frequency or length? A phylogenetic approach to understand how animals regulate locomotor speed. Journal of Experimental Biology, 225, jeb243231.
Granatosky, M. C., McElroy, E. J., Laird, M. F., Iriarte-Diaz, J., Reilly, S. M., Taylor, A. B., & Ross, C. F. (2019a). Joint angular excursions during cyclical behaviors differ between tetrapod feeding and locomotor systems. Journal of Experimental Biology, 222, jeb200451.
Granatosky, M. C., McElroy, E. J., Lemelin, P., Reilly, S. M., Nyakatura, J. A., Andrada, E., Kilbourne, B. M., Allen, V. R., Butcher, M. T., Blob, R. W., & Ross, C. F. (2020). Variation in limb loading magnitude and timing in tetrapods. The Journal of Experimental Biology, 223.
Granatosky, M. C., & Schmitt, D. (2017). Forelimb and hind limb loading patterns during below branch quadrupedal locomotion in the two-toed sloth. Journal of Zoology, 302, 271-278.
Granatosky, M. C., & Schmitt, D. (2019). The mechanical origins of arm-swinging. Journal of Human Evolution, 130, 61-71.
Granatosky, M. C., Schmitt, D., & Hanna, J. (2019b). Comparison of spatiotemporal gait characteristics between vertical climbing and horizontal walking in primates. Journal of Experimental Biology, 222, jeb185702.
Gray, J. (1944). Studies in the mechanics of the tetrapod skeleton. Journal of Experimental Biology, 20, 88-116.
Hanna, C. S., Alihosseini, C., Fischer, H. M., Davoli, E. C., & Granatosky, M. C. (2022). Are they arboreal? Climbing abilities and mechanics in the red-backed salamander (Plethodon cinereus). Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 337, 238-249.
Hanna, J. B., Granatosky, M. C., Rana, P., & Schmitt, D. (2017). The evolution of vertical climbing in primates: Evidence from reaction forces. Journal of Experimental Biology, 220, 3039-3052.
Herrel, A., Tolley, K. A., Measey, G. J., da Silva, J. M., Potgieter, D. F., Boller, E., Boistel, R., & Vanhooydonck, B. (2013). Slow but tenacious: An analysis of running and gripping performance in chameleons. The Journal of Experimental Biology, 216, 1025-1030.
Hirasaki, E., Kumakura, H., & Matano, S. (1993). Kinesiological characteristics of vertical climbing in Ateles geoffroyi and Macaca fuscata. Folia Primatologica, 61, 148-156.
Hirasaki, E., Kumakura, H., & Matano, S. (2000). Biomechanical analysis of vertical climbing in the spider monkey and the Japanese macaque. American Journal of Physical Anthropology, 113, 455-472.
Ishida, H., Jouffroy, F., & Nakano, Y. (1990). Comparative dynamics of pronograde and upside down horizontal quadrupedalism in the slow loris (Nycticebus coucang). In F. Jouffroy, M. Stack, & C. Niemitz (Eds.), Gravity, posture and locomotion in primates. Firenze, Il Sedicesimo (pp. 209-220. http://scholar.google.com/scholar?q=ishida%2Bloris&btnG=&hl=en&as_sdt=0,34#0
Jouffroy, F., & Stern, J. (1990). Telemetered EMG study of the antigravity versus propulsive actions of knee and elbow muscles in the slow loris (Nycticebus coucang). Gravity, posture and locomotion in primates, 221-236. http://scholar.google.com/scholar?q=jouffroy%2Bloris&btnG=&hl=en&as_sdt=0,34#1
Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. B. (2017). Lmer test package: Tests in linear mixed effects models. Journal of Statistical Software, 82(13), 1-26. https://doi.org/10.18637/jss.v082.i13
Karantanis, N.-E., Rychlik, L., Herrel, A., & Youlatos, D. (2017a). Arboreal gaits in three sympatric rodents Apodemus agrarius, Apodemus flavicollis (Rodentia, Muridae) and Myodes glareolus (Rodentia, Cricetidae). Mammalian Biology - Zeitschrift für Säugetierkunde, 83, 51-63.
Karantanis, N.-E., Rychlik, L., Herrel, A., & Youlatos, D. (2017b). Comparing the arboreal gaits of Muscardinus avellanarius and Glis glis (Gliridae, Rodentia): A first quantitative analysis. Mammal Study, 42, 161-172.
Kimura, T. (1979). Kinesiological characteristics of primate walking. In H. Morbeck, H. Preuschoft, & N. Gomberg (Eds.), Environment, behavior, and morphology: Dynamic interactions in primates (pp. 297-311). G. Fischer.
Larson, S. G., & Demes, B. (2011). Weight support distribution during quadrupedal walking in Ateles and Cebus. American Journal of Physical Anthropology, 144, 633-642.
Larson, S. G., Schmitt, D., Lemelin, P., & Hamrick, M. (2001). Limb excursion during quadrupedal walking: How do primates compare to other mammals? Journal of Zoology, 255, 353-365.
Larson, S. G., & Stern, J. T. (2009). Hip extensor EMG and forelimb/hind limb weight support asymmetry in primate quadrupeds. American Journal of Physical Anthropology, 138, 343-355.
Massor, A. M., Young, J. W., & Butcher, M. T. (2022). Does a suspensory lifestyle result in increased tensile strength? Organ-level material properties of sloth limb bones. Journal of Experimental Biology, 225(5), jeb242866. https://doi.org/10.1242/jeb.242866
Marshall, S. K., Spainhower, K. B., Sinn, B. T., Diggins, T. P., & Butcher, M. T. (2021). Hind limb bone proportions reveal unexpected morphofunctional diversification in Xenarthrans. Journal of Mammalian Evolution, 28, 599-619.
Mendel, F. C. (1979). The wrist joint of two-toed sloths and its relevance to brachiating adaptations in the hominoidea. Journal of Morphology, 162, 413-424.
Mendel, F. C. (1981). Use of hands and feet of two-toed sloths (Choloepus hoffmanni) during climbing and terrestrial locomotion. Journal of Mammalogy, 62, 413-421.
Mendel, F. C. (1985a). Use of hands and feet of three-toed sloths (Bradypus variegatus) during climbing and terrestrial locomotion. Journal of Mammalogy, 66, 359-366. https://doi.org/10.2307/1381249
Mendel, F. C. (1985b). Adaptations for suspensory behavior in the limbs of two-toed sloths. In G. G. Montgomery (Ed.), The evolution and ecology of armadillos, sloths, and vermilinguas (pp. 151-162). Smithsonian Institution Press.
Miller, R. A. (1935). Functional adaptations in the forelimb of the sloths. Journal of Mammalogy, 16, 38-51.
Montañez-Rivera, I., Nyakatura, J. A., & Amson, E. (2018). Bone cortical compactness in ‘tree sloths’ reflects convergent evolution. Journal of Anatomy, 233, 580-591.
Nyakatura, J. A. (2012). The convergent evolution of suspensory posture and locomotion in tree sloths. Journal of Mammalian Evolution, 19, 225-234.
Nyakatura, J. A., Andrada, E., Curth, S., & Fischer, M. S. (2014). Bridging “Romer's Gap”: Limb mechanics of an extant belly-dragging lizard inform debate on tetrapod locomotion during the early carboniferous. Journal of Evolutionary Biology, 41, 175-190.
Nyakatura, J. A., & Fischer, M. S. (2011). Functional morphology of the muscular sling at the pectoral girdle in tree sloths: Convergent morphological solutions to new functional demands? Journal of Anatomy, 219, 360-374.
Nyakatura, J. A., Petrovitch, A., & Fischer, M. S. (2010). Limb kinematics during locomotion in the two-toed sloth (Choloepus didactylus, Xenarthra) and its implications for the evolution of the sloth locomotor apparatus. Zoology, 113, 221-234.
Nyakatura, J. A., & Andrada, E. A. (2013). A mechanical link model of two-toed sloths: No pendular mechanics during suspensory locomotion. Acta Theriologica, 58, 83-93. https://doi.org/10.1007/s13364-012-0099-4
Olson, R. A., Glenn, Z. D., Cliffe, R. N., & Butcher, M. T. (2018). Architectural properties of sloth forelimb muscles (Pilosa: Bradypodidae). Journal of Mammalian Evolution, 25, 573-588.
Preuschoft, H. (2002). What does “arboreal locomotion” mean exactly and what are the relationships between “climbing”, environment and morphology? Zeitschrift für Morphologie und Anthropologie, 83, 171-188.
Raichlen, D. A., Pontzer, H., Shapiro, L. J., & Sockol, M. D. (2009). Understanding hind limb weight support in chimpanzees with implications for the evolution of primate locomotion. American Journal of Physical Anthropology, 138, 395-402.
Reynolds, T. R. (1985). Mechanics of increased support of weight by the hindlimbs in primates. American Journal of Physical Anthropology, 67, 335-349.
Schmitt, D. (2003). Mediolateral reaction forces and forelimb anatomy in quadrupedal primates: Implications for interpreting locomotor behavior in fossil primates. Journal of Human Evolution, 44, 47-58.
Schmitt, D., & Lemelin, P. (2002). Origins of primate locomotion: Gait mechanics of the woolly opossum. American Journal of Physical Anthropology, 118, 231-238.
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671-675.
Sokal, R. R., & Braumann, C. A. (1980). Significance tests for coefficients of variation and variability profiles. Systematic Biology, 29(1), 50-66. https://doi.org/10.1093/sysbio/29.1.50
Sokal, R. R., & Rohlf, F. J. (2012). Biometry: The principles and practice of statistics in biological research (6th ed.). Freeman & Company.
Spainhower, K. B., Cliffe, R. N., Metz, A. K., Barkett, E. M., Kiraly, P. M., Thomas, D. R., Kennedy, S. J., Avey-Arroyo, J. A., & Butcher, M. T. (2018). Cheap labor: Myosin fiber type expression and enzyme activity in the forelimb musculature of sloths (Pilosa: Xenarthra). Journal of Applied Physiology, 125, 799-811.
Spainhower, K. B., Metz, A. K., Yusuf, A.-R. S., Johnson, L. E., Avey-Arroyo, J. A., & Butcher, M. T. (2021). Coming to grips with life upside down: How myosin fiber type and metabolic properties of sloth hindlimb muscles contribute to suspensory function. Journal of Comparative Physiology B, 191, 207-224.
Sunquist, M. E., & Montgomery, G. G. (1973). Activity patterns and rates of movement of two-toed and three-toed sloths (Choloepus hoffmanni and Bradypus infuscatus). Journal of Mammalogy, 54, 946-954.
Thomas, P., Pouydebat, E., Brazidec, M. L., Aujard, F., & Herrel, A. (2016). Determinants of pull strength in captive grey mouse lemurs. Journal of Zoology, 298, 77-81.
Urbani, B., & Bosque, C. (2007). Feeding ecology and postural behaviour of the three-toed sloth (Bradypus variegatus flaccidus) in Northern Venezuela. Mammalian Biology, 72, 321-329.
Winter, B. (2013). Linear models and linear mixed effects models in R with linguistic applications. arXiv. http://arxiv.org/pdf/1308.5499.pdf
Wang, Z., Dai, Z., Ji, A., Ren, L., Xing, Q., & Dai, L. (2015). Biomechanics of gecko locomotion: The patterns of reaction forces on inverted, vertical and horizontal substrates. Bioinspiration & Biomimetics, 10, 016019.
Wislocki, G. B. (1928). Observations on the gross and microscopic anatomy of the sloths (Bradypus griseus griseus Gray and Choloepus hoffmanni Peters). Journal of Morphology, 46, 317-397.
Young, M. W., Dickinson, E., Flaim, N. D., & Granatosky, M. C. (2022). Overcoming a “forbidden phenotype”: The parrot's head supports, propels and powers tripedal locomotion. Proceedings of the Royal Society B: Biological Sciences, 289, 20220245.

Auteurs

Melody W Young (MW)

Department of Anatomy, New York Institute of Technology College of Osteopathic Medicine, Old Westbury, New York, USA.

Andrew J McKamy (AJ)

Department of Biological Sciences, Youngstown State University, Youngstown, Ohio, USA.

Edwin Dickinson (E)

Department of Anatomy, New York Institute of Technology College of Osteopathic Medicine, Old Westbury, New York, USA.

Johnathan Yarbro (J)

New York Institute of Technology College of Osteopathic Medicine, Jonesboro, Arkansas, USA.

Ashwin Ragupathi (A)

New York Institute of Technology College of Osteopathic Medicine, Old Westbury, New York, USA.

Navjot Guru (N)

New York Institute of Technology College of Osteopathic Medicine, Old Westbury, New York, USA.

Judy A Avey-Arroyo (JA)

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

Michael T Butcher (MT)

Department of Biological Sciences, Youngstown State University, Youngstown, Ohio, USA.

Michael C Granatosky (MC)

Department of Anatomy, New York Institute of Technology College of Osteopathic Medicine, Old Westbury, New York, USA.
Center for Biomedical Innovation, New York Institute of Technology College of Osteopathic Medicine, Old Westbury, New York, USA.

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