Coming to grips with life upside down: how myosin fiber type and metabolic properties of sloth hindlimb muscles contribute to suspensory function.
Arboreal
Metabolism
Muscle
Myosin heavy chain
Suspension
Journal
Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology
ISSN: 1432-136X
Titre abrégé: J Comp Physiol B
Pays: Germany
ID NLM: 8413200
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
24
06
2019
accepted:
28
10
2020
revised:
15
09
2020
pubmed:
20
11
2020
medline:
29
10
2021
entrez:
19
11
2020
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 33211164
doi: 10.1007/s00360-020-01325-x
pii: 10.1007/s00360-020-01325-x
doi:
Substances chimiques
Myosin Heavy Chains
EC 3.6.4.1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
207-224Références
Anapol FC, Jungers WL (1986) Architectural and histochemical diversity within the quadriceps femoris of brown lemur (Lemur fulvus). Am J Phys Anthropol 69:355–375
pubmed: 3706515
Ariano MA, Armstrong RB, Edgerton VR (1973) Hindlimb muscle fiber populations of five mammals. J Histochem 21:51–55
Armstrong RB, Phelps RO (1984) Muscle fiber type composition of the rat hindlimb. Am J Anat 171:259–272
pubmed: 6517030
Britton WS (1941) Form and function in the sloth (concluded). Quart Rev Biol 16:190–207
Butcher MT, Chase PG, Hermanson JW, Clark AN, Brunet NM, Bertram JEA (2010) Contractile properties of muscle fibers from the forelimb deep and superficial digital flexors of horses. Am J Physiol Reg Integr Comp Physiol 299:R996–R1005
Carillo E, Fuller TK, Saenz JC (2009) Jaguar (Panthera onca) hunting activity: effects of prey distribution and availability. J Trop Ecol 25:563–567
Cliffe RN, Haupt RJ, Avey-Arroyo JA, Wilson RP (2015) Sloths like it hot: ambient temperature modulates food intake in the brown-throated sloth (Bradypus variegatus). PeerJ 3:e875-889
pubmed: 25861559
pmcid: 4389270
Cliffe RN, Scantlebury MD, Kennedy SJ, Avey-Arroyo JA, Mindich D, Wilson RP (2018) The metabolic response of the Bradypus sloth to temperature. PeerJ 6:e5600
pubmed: 30258712
pmcid: 6151113
De Moura Filho AG, Huggins SE, Lines SG (1983) Sleep and waking in the three-toed sloth, Bradypus tridactylus. Comp Biochem Physiol A 76:345–355
pubmed: 6139209
Engelmann GF (1985) The phylogeny of the Xenarthra. In: Montgomery GG (ed) The evolution and ecology of armadillos, sloths, and Vermilinguas. Smithsonian Institution Press, Washington, pp 51–64
Goffart M (1971) Function and form in the sloth. Pergamon Press, Fairview Park
Gorvet MA, Wakeling JM, Morgan DM, Hidalgo Segura D, Avey-Arroyo JA, Butcher MT (2020) Keep calm and hang on: EMG activation in the forelimb musculature of three-toed sloths. J Exp Biol. https://doi.org/10.1242/jeb.218370
doi: 10.1242/jeb.218370
pubmed: 32527958
Granatosky MC, Schmitt D (2017) Forelimb and hind limb loading patterns during below branch quadrupedal locomotion in the two-toed sloth. J Zool 302:271–278
Granatosky MC, Karantanis NE, Rychlik L, Youlatos D (2018) A suspensory way of life: integrating locomotion, postures, limb movements, and forces in two-toed sloths Choloepus didactylus (Megalonychidae, Folivora, Pilosa). J Exp Zool 329:570–588
Grand TI (1978) Adaptations of tissue and limb segments to facilitate moving and feeding in arboreal folivores. In: Montgomery GG (ed) The ecology of arboreal folivores. Smithsonian Press, Washington DC, pp 231–241
Hanna JB, Schmitt D, Griffin TM (2008) The energetic cost of climbing in primates. Science 320:898
pubmed: 18487185
Hazimihalis PJ, Gorvet MA, Butcher MT (2013) Myosin isoform fiber type and fiber size in the tail of the Virginia opossum (Didelphis virginiana). Anat Rec 296:96–107
Hesse B, Fischer MS, Schilling N (2010) Distribution pattern of muscle fiber types in the perivertebral musculature of two different sized species of mice. Anat Rec 293:446–463
Jouffroy FK, Medina MF (2004) Comparative fiber-type composition and size in the antigravity muscles of primate limbs. In: Anapol F, German RZ, Jablonski NG (eds) Shaping primate evolution form, function, and behavior. Cambridge University Press, Cambridge, pp 134–161
Jouffroy FK, Stern JT Jr (1990) Telemetered EMG study of the antigravity versus propulsive actions of knee and elbow muscles in the slow loris (Nycticebus coucang). In: Jouffroy FK, Stack MH, Niemitz C (eds) Gravity, posture and locomotion in primates. Il Sedicesimo, Florence, pp 221–236
Jouffroy FK, Stern JT Jr, Medina MF, Larson SG (1999) Function and cytochemical characteristics of postural limb muscles of the rhesus monkey: a telemetered EMG and immunofluorescence study. Folia Primatol 70:235–253
Kohn TA (2014) Insights into the skeletal muscles characteristics of three southern African antelope species. J Exp Biol 3:1037–1044
Kohn TA, Myburgh KH (2007) Regional specialization of rat quadriceps myosin heavy chain isoforms occurring in distal to proximal parts of middle and deep regions is not mirrored by citrate synthase activity. J Anat 210:8–18
pubmed: 17229279
pmcid: 2100260
Kohn TA, Burroughs R, Hartman MJ, Noakes TD (2011) Fiber type and metabolic characteristics of lion (Panthera leo), caracal (Caracal caracal), and human skeletal muscle. Comp Biochem Physiol A 159:125–133
Kohn TA, Curry JW, Noakes TD (2011) Black wildebeest skeletal muscle exhibits high oxidative capacity and a high proportion of type IIx fibres. J Exp Biol 214:4041–4047
pubmed: 22071196
Lieber RL (2009) Skeletal muscle, structure, function, and plasticity, 3rd edn. Lippincott Williams & Wilkins Baltimore, Philadelphia, p 369
McDonald HG, De Iuliis G (2008) Fossil history of sloths. In: Vizcaíno SF, Loughry WJ (eds) The biology of the Xenarthra. University Press of Florida, Gainesville, pp 39–55
Mendel FC (1981a) The hand of two-toed sloths (Choloepus): its anatomy and potential uses relative to size of support. J Morphol 169:1–19
pubmed: 30139204
Mendel FC (1981b) Foot of two-toed sloths: its anatomy and potential uses relative to size of support. J Morphol 170:357–372
pubmed: 30119592
Mendel FC (1985) Use of hands and feet of three-toed sloths (Bradypus variegatus) during climbing and terrestrial locomotion. J Mammal 66:359–366
Mendel FC (1987) Adaptations for suspensory behavior in the limbs of two-toed sloths. In: Montgomery GG (ed) The ecology and evolution of armadillos, sloths, and Vermilinguas. Smithsonian Institute Press, Washington, pp 151–162
Meyers RA, Hermanson JW (2006) Horse soleus muscle: postural sensor or vestigial structure? Anat Rec 288A:1068–1076
Montgomery GG, Sunquist ME (1975) Impact of sloths on neotropical forest energy flow and nutrient cycling. In: Golley FB, Medina E (eds) Tropical ecological systems: trends in terrestrial and aquatic research. Springer-Verlag, New York, pp 69–98
Moreno RS, Kays RW, Samudio O Jr (2006) Competitive release in diets of ocelot (Leopardus pardalis) and puma (Puma concolor) after jaguar (Panthera onca) decline. J Mammal 87:808–816
Nyakatura JA (2012) The convergent evolution of suspensory posture and locomotion in tree sloths. J Mammal Evol 19:225–234
Nyakatura JA, Andrada E (2013) A mechanical link model of two-toed sloths: no pendular mechanics during suspensory locomotion. Acta Theriol 58:83–93
Nyakatura JA, Petrovitch A, Fischer MS (2010) Limb kinematics during locomotion in the two-toed sloth (Choloepus didactylus, Xenarthra) and its implications for the evolution of the sloth locomotor apparatus. Zool 113:221–234
Olson RA, Glenn ZD, Cliffe RN, Butcher MT (2018) Architectural properties of sloth forelimb muscles (Pilosa: Bradypodidae). J Mammal Evol 25:573–588
Pauli JN, Peery MZ, Fountain ED, Karasov WH (2016) Arboreal folivores limit their energetic output, all the way to slothfulness. Amer Nat 188:196–204
Rupert JE, Schmidt EC, Moriera-Soto A, Rodriguez Herrera BR, Vandeberg JL, Butcher MT (2014) Myosin isoform expression in the prehensile tails of didelphid marsupials: functional differences between arboreal and terrestrial opossums. Anat Rec 297:1364–1376
Rupert JE, Rose JA, Organ JM, Butcher MT (2015) Forelimb muscle architecture and myosin isoform composition in the groundhog (Marmota monax). J Exp Biol 218:194–205
pubmed: 25452499
Schiaffino S, Reggiani C (2011) Fiber types in mammalian skeletal muscles. Physiol Rev 91:1447–1531
pubmed: 22013216
Sickles DW, Pinkstaff CA (1981a) Comparative histochemical study of prosimian primate hindlimb muscles. I. Muscle fiber types. Am J Anat 160:175–186
pubmed: 6455915
Sickles DW, Pinkstaff CA (1981b) Comparative histochemical study of prosimian primate hindlimb muscles. II. Populations of fiber types. Am J Anat 160:187–194
pubmed: 6791489
Spainhower KB, Cliffe RN, Metz AK, Barkett EM, Kiraly PM, Thomas DR, Kennedy SJ, Avey-Arroyo JA, Butcher MT (2018) Cheap labor: Myosin fiber type expression and enzyme activity in the forelimb musculature of sloths (Pilosa: Xenarthra). J Appl Physiol 125:799–811
pubmed: 29722617
Stewart JM, Woods AK, Blakely JA (2005) Maximal enzyme activities, and myoglobin and glutathione concentrations in heart, liver and skeletal muscle of the Northern Short-tailed shrew (Blarina brevicauda; Insectivora: Soricidae). Comp Biochem Physiol B 141:267–273
pubmed: 15914053
Sunquist ME, Montgomery GG (1973) Activity patterns and rates of movement of two-toed and three-toed sloths (Choloepus hoffmanni and Bradypus infuscatus). J Mammal 54:946–954
pubmed: 4761371
Thomas DR, Chadwell BA, Walker GR, Budde JE, Vandeberg JL, Butcher MT (2017) Ontogeny of myosin isoform expression and prehensile function in the tail of the gray short-tailed opossum (Monodelphis domestica). J Appl Physiol 123:513–525
pubmed: 28522766
Urbani B, Bosque C (2007) Feeding ecology and postural behavior of the three-toed sloth (Bradypus variegatus flaccidus) in northern Venezuela. Mammal Biol 72:321–329
Wigston DJ, English AW (1992) Fiber-type proportions in mammalian soleus muscle during postnatal development. J Neurobiol 23:61–70
pubmed: 1564455
Williams TM, Dobson GP, Mathieu-Costello O, Morsbach D, Worley MB, Phillips JA (1997) Skeletal muscle histology and biochemistry of an elite sprinter, the African cheetah. J Comp Physiol B 167:527–535
pubmed: 9404014
Wislocki GB (1928) Observations on the gross and microscopic anatomy of the sloths (Bradypus griseus griseus Gray and Choloepus hoffmanni Peters). J Morphol Physiol 46:317–377