Skip to main content
NCBI home page
Integrative Organismal Biology logoLink to Integrative Organismal Biology
. 2020 Oct 26;2(1):obaa032. doi: 10.1093/iob/obaa032

A Horse of a Different Color?: Tensile Strength and Elasticity of Sloth Flexor Tendons

A M Mossor 1, B L Austin 1, J A Avey-Arroyo 2, M T Butcher 1,✉
PMCID: PMC7715270  PMID: 33796818

Abstract

Tendons must be able to withstand the tensile forces generated by muscles to provide support while avoiding failure. The properties of tendons in mammal limbs must therefore be appropriate to accommodate a range of locomotor habits and posture. Tendon collagen composition provides resistance to loading that contributes to tissue strength which could, however, be modified to not exclusively confer large strength and stiffness for elastic energy storage/recovery. For example, sloths are nearly obligate suspenders and cannot run, and due to their combined low metabolic rate, body temperature, and rate of digestion, they have an extreme need to conserve energy. It is possible that sloths have a tendon “suspensory apparatus” functionally analogous to that in upright ungulates, thus allowing for largely passive support of their body weight below-branch, while concurrently minimizing muscle contractile energy expenditure. The digital flexor tendons from the fore- and hindlimbs of two-toed (Choloepus hoffmanni) and three-toed (Bradypus variegatus) sloths were loaded in tension until failure to test this hypothesis. Overall, tensile strength and elastic (Young’s) modulus of sloth tendons were low, and these material properties were remarkably similar to those of equine suspensory “ligaments.” The results also help explain previous findings in sloths showing relatively low levels of muscle activation in the digital flexors during postural suspension and suspensory walking.

Introduction

Tendons are specialized connective tissue structures that can withstand large tensile forces that are generated during locomotor activities (Bennett et al. 1986; Ker et al. 1988). Consequently, tendons need to be strong and stiff (and tough) enough to withstand such forces, as well as have a reasonable safety factor for body weight support (Shadwick 1990). Strength is the maximum amount of tensile stress that a tendon can withstand before failure, while stiffness is the ability of tendon to resist deformation (i.e., strain) and toughness indicates the total amount of energy a tendon can absorb before rupture. Distal limb tendons in some terrestrial mammals are known to function as appropriately stiff elastic elements for joint position control and/or as efficient biological springs during locomotion to conserve energy (Alexander 1984, 1988; Alexander and Dimery 1985). For example, muscle-tendon units (MTUs) of ungulates, kangaroos, and wallabies are extremely modified in this aspect by having long, thin tendons capable of undergoing large strains for substantial elastic strain energy storage and recovery (Dimery and Alexander 1985; Dimery et al. 1986; Biewener and Baudinette 1995; Biewener 1998; Butcher et al. 2009).

Strain in MTU may also occur with little-to-no muscle activation for static body weight support, thus the resisting force is largely passive tension during postural behavior (Lieber 2002; Hodson-Tole et al. 2016). This type of MTU function is typical in the distal limbs of upright ungulates during grazing. Notably, horses have a weight-bearing suspensory apparatus (Hildebrand 1960, 1987) which allows them to remain standing for long periods of time without fatigue (Hermanson and Cobb 1992). As a part of their suspensory apparatus, composed mainly of the suspensory “ligament” (i.e., m. interosseous medius) and collateral ligaments about metacarpo-metatarsophalangeal joints, the digital flexor tendons act in parallel with these ligamentous structures that are more immediate to the support of the digits during standing (Hildebrand 1960; Dyce et al. 1996; Butcher et al. 2006), in addition to the tendons resisting substantial load during the mid-stance portion of locomotion. The specializations in digital flexor MTU structure-function of equids substantially reduce metabolic energy expenditure that would otherwise need to be supplied by muscle work (Biewener 1998; Butcher et al. 2007), which is critical for both postural and locomotor activity of all mammals. Thus, it is possible that similar specializations are also present in the distal limbs of taxa not adapted for cursorial habit, including sloths, because they are capable of suspending below tree branches by pairs of limbs for extended periods of time, an ability that is functionally analogous to ungulates standing upright for many hours grazing.

Tree sloths (an uncommon model system) are some of the rare mammals that demonstrate nearly obligatory suspensory habits as part of their arboreal lifestyle (Hayssen 2010, 2011; Granatosky et al. 2018b), and accordingly, they have exceptionally modified distal limb morphology as a representation of their suspensory adaptations (Mendel 1981a, 1981b, 1985;Nyakatura et al. 2010;Olson et al. 2018). Sloths do not use pronograde (above-branch) locomotion as do their primate counterparts that are also adapted for suspensory habits, and although sloths can perform both arboreal (suspensory) and terrestrial (crouched-crawl) locomotion, they are incapable of a running gait for either mode of transport ( Mendel 1981a,1985). Moreover, sloths do not utilize pendulum-like energy exchanges when suspensory walking (Nyakatura and Andrada 2013), and with no necessity to bounce below-branch, their flexor tendons serve no functional role as biological springs like those in upright quadrupeds. Therefore, energy conservation is extraordinarily critical to sloths, and akin to other mammals, they can be expected to have one or several mechanisms to offset the cost of force production during locomotor and postural behaviors. The need to conserve metabolic energy is further compounded by a combination of extremely low basal metabolism (Pauli et al. 2016) and low body temperatures (Cliffe et al. 2018), as well as an energy poor diet (Montgomery and Sunquist 1978) and low rates of digestion (Cliffe et al. 2015). It is hypothesized that the distal limbs of sloths may effectively demonstrate a suspensory apparatus to supplement offset metabolic energy expenditure during periods of suspensory activity.

The objective of this study is to evaluate the material/mechanical properties of sloth deep digital flexor tendons. Based on previous data (Gorvet et al. 2020) indicating that small, fast-contracting fibers (and/or motor units) in the distal flexor musculature are activated at low levels during suspensory walking and posture, the low muscle activation observed in sloth digital flexors may provide a similar low level of force; a magnitude adequate to counteract strain in their flexor tendons (i.e., modulating stiffness), such that a large portion of the body weight in sloths is supported by tensile loading of their robust flexor tendons. Such a mechanism would save sloths energy during suspension (see Fig. 1) and additional evidence on the tendon strength and elasticity as key components of their tensile limb system could also help validate a previous hypothesis of entirely passive support provided by strong “locking” flexor tendons (Mendel 1981a, 1981b, 1981c). Last, the expected combination of large tensile strength and modest elasticity for sloth flexor tendons may also account for necessary selected advantages of sloths having an unusually low metabolism for placental mammals and the slow, deliberate movement patterns associated with their arboreal lifestyle.

Fig. 1.

Fig. 1

Open in a new tab

Proposed integrated model of system function for counteracting tensile forces acting on sloth limbs during suspension. Sloth image was redrawn and modified from that originally published in Granatosky and Schmitt (2017).

Materials and methods

Tensile testing was performed on m. flexor digitorum profundus (FDP) tendons from sub-adult/adult Choloepus hoffmanni (N = 6, 5.47 ± 1.14 kg) and Bradypus variegatus (N = 5, 3.36 ± 1.37 kg). As a comparator dataset, we tested the deep flexor tendons from the forelimbs of vervet monkeys, Chlorocebus aethiops (N = 3, 4.20 ± 2.00 kg), a semi-arboreal primate, using the following protocol. Tendons were loaded in tension using a uniaxial Instron machine (Instron, Norwood, MA, USA) and photographs of the loading chain are shown in Fig. 2. Two custom grips, one on the machine base (aluminum clamp block) and the other on the load cell attached to the crosshead (screw-tensioned clamp) were used to hold the tendon test specimen in place. Prior to enclosing the tendons in the grips, each end of the tendon was secured between four 2.5 cm × 2.5 cm pieces of 100 grit adhesive-backed sandpaper, such that two pieces were adhered to each other leaving the grit sides exposed to both the tendon and grip. Tendons were further secured to the sandpaper by using veterinary grade tissue glue (3 M) and then photographed on a 1 cm × 1 cm measurement grid. Once the tissue adhesive cured (quick drying), one end of the tendon was clamped in the top grip followed by the clamping between the base grip when the tendon test sample was vertically aligned within the testing frame (Fig. 2). Tendon tissue was kept hydrated with PBS during this entire process.

Fig. 2.

Fig. 2

Open in a new tab

(A–D) Photographs of the Instron load chain for material property testing on sloth flexor tendons. Shown sequentially is a robust digital flexor tendon gripped for initial measurement using upper and lower custom grips, undergoing a tensile test, and ultimately under maximum load near failure.

Initial tendon length (L0) between the grips was standardized to 15–20 mm (specifically, for sloth tendons) and set using digital calipers. Also, measurements of tendon width and depth were measured at three locations (top grip, middle tendon, and bottom grip) along L0 with the test tendon clamped in place. These measurements were used to input specimen dimensions into Instron software for reference, as well as for the computation of elastic (Young’s) Modulus. Still, photographs in two dimensions were also taken prior to testing to upload into SolidWorks® software (v. 25: Dassault Systèmes, Waltham, MA, USA) for more accurate digital measurement of resting tendon dimensions for calculations of material properties. All tendons were loaded to failure in tension at a crosshead displacement (strain rate: 10 mm min−1; ∼1% strain per min: Javidi et al. 2019). Force and extension were continuously recorded during testing and output from the load cells (250 N load cell) to Instron data acquisition software (v. 2.25: Instron). After each test, tendons were removed from the testing rig and once again photographed on the measurement grid to assess any patterns of differential strain throughout tendon length leading to its permanent deformation and/or rupture. All recorded data were exported as .csv files to MS Excel (Microsoft Corp., Redmond, WA, USA) for computation of material properties. Stress (in MPa) and strain (%) were calculated from the records of force and extension using digitally calculated values of tendon cross-sectional area (CSA) and L0, respectively, and plotted as a normalized stress-strain curve (Fig. 3). The following material properties were measured/calculated from the linear elastic regions of either raw force-extension or normalized stress-strain data: elastic (Young’s) Modulus (E), ultimate tensile strength, stiffness (in N/mm), extensibility (in mm), toughness (in J/mm3), elastic strain energy (in mJ), and safety factors.

Fig. 3.

Fig. 3

Open in a new tab

Representative normalized stress-strain curve of sloth digital flexor tendons. Diagrammed are measurements of material properties taken from the elastic loading region: ultimate tensile strength, elastic (Young’s) modulus (E), toughness, and extensibility.

Multivariate analysis of variance (MANOVA) performed in SPSS (version 20.0: IBM, Armonk, NY, USA) was used to test for differences in tendon material properties for the a priori factors species (Choloepus vs. Bradypus) and limbs (forelimb vs. hindlimb). A non-significant finding for both factors then allowed for a similar MANOVA test among forelimb tendon properties between sloths and vervet monkeys. ANOVA (in SPSS) was used to test for differences in elastic (Young’s) modulus and ultimate tensile strength among limb tendons based on the following locomotor habit (substrate preference) categorizations: terrestrial, semi-arboreal, and arboreal. Data for these tests included rat calcaneal tendon (terrestrial) from the literature (LaCroix et al. 2013), in addition to those values from vervet monkeys (semi-arboreal) and sloths (arboreal) sampled in this study.

Results

Means ± SD of measured and calculated material properties are shown in Fig. 4. Overall, tensile strength was lower than expected and as was elasticity, while tendon stiffness was moderate. Despite some mean variation between species, especially in tendon safety factors (Table 1), tendon properties did not vary (P = 0.950) between two-toed (Cho. hoffmanni) and three-toed (B. variegatus) sloths or between fore- and hindlimb pairs (P = 0.907). Comparisons among the material properties of flexor tendons from semi-arboreal vervet monkeys (Chl. aethiops) versus those from sloth limbs showed that only extensibility (P = 0.030) and elastic strain energy (P = 0.041) differed significantly, with greater values for extensibility in sloths and the inverse for elastic strain energy storage capacity in monkeys. Significant differences in tensile strength and elastic (Young’s) modulus were also found in relation to locomotor habit and/or substrate preference as shown in Fig. 5. Overall, tensile strength (P = 0.006) and elastic modulus (P = 0.001) were greater in rat (calcaneal) tendons than in sloth flexor tendons (Fig. 5A), whereas only tendon elastic modulus (P = 0.024) was greater in rats over that in vervet monkeys (Fig. 5B).

Fig. 4.

Fig. 4

Open in a new tab

(A–F) Bar charts of tendon material properties for the fore- and hindlimbs of Cho. hoffmanni and B. variegatus. Shown are mean ± SD. Forelimbs (blue or red) are indicated by solid bars while hindlimbs (orange or yellow) are dashed bars.

Table 1.

Safety factors (SF) for fore– and hindlimb flexor tendons for Choloepus, Bradypus, and Chlorocebus

Species Tendon SF (single limb support)
 Tendon SF (three limb support)
Forelimb Hindlimb Forelimb Hindlimb
Choloepus hoffmanni 3.16 2.49 9.21 6.70
Bradypus variegatus 3.99 4.21 8.81 10.1
Chlorocebus aethiops a 2.00 — 6.00 —
Open in a new tab
a

Data for forelimbs only.

Safety factors are estimated as the ratio maximum tensile load to body weight. Three limb support for sloths is most common during suspensory locomotor support.

Fig. 5.

Fig. 5

Open in a new tab

Bar charts (mean ± SD) comparing (A) ultimate tensile strength and (B) elastic (Young’s) modulus across substrate preference (or locomotor habits): arboreal (sloths, black), semi-arboreal (vervet monkeys, white), and generalists (rats, gray). Rat calcaneal tendon data are adapted from LaCroix et al. (2013) and references therein.

Discussion

To our know knowledge, this study is the first to determine material properties of flexor tendons in an obligate suspensory (tensile) limb system. Despite differences in adult body mass (Grand 1978), distal limb form (Mendel 1981a, 1981b), and frequency of suspensory locomotion and posture (Sunquist and Montgomery 1973; Urbani and Bosque 2007), tendon strength, elasticity, and stiffness are the same for Cho. hoffmanni and B. variegatus. This major finding may not be surprising due to the remarkable breadth of evolutionary convergence for suspensory habits observed between two-toed and three-toed forms (Gaudin 2004; Nyakatura 2012; Montanez-Rivera et al. 2018; Spainhower et al. 2018). In particular, peak vertical substrate reaction forces (SRFs) do not differ between the fore- and hindlimbs during suspensory walking in Choloepus (Granatosky and Schmitt 2017), thus both limb pairs play an equal role for body weight support (Granatosky et al. 2018b) necessitating that limb tendon properties remain consistent. Future work with Bradypus aims to demonstrate similar locomotor mechanics to determine if there is a universal lack of body weight shifting during suspensory locomotion in sloths. Moreover, we initially expected that safety factors might be elevated in the flexor tendons of Choloepus, which tends to spend more time in postural suspension than Bradypus, as well as having greater active time incorporating longer bouts of suspensory walking (Urbani and Bosque 2007). These behavioral differences, which correspond with the ecological preferences of Cho. hoffmanni (Hayssen 2011), suggest that lower safety factors for the tendons of two-toed sloths may result from them operating at longer lengths during suspension. Nonetheless, elevated safety factors in B. variegatus coupled with its less active lifestyle bears no statistical difference, further signifying functional convergence in sloths.

Tendon safety factors estimated for sloths are higher than those typically found for the tendons from upright mammals (Alexander 1981). The species of two- and three-toed sloths studied have an average body mass of nearly 4–6 kg as adults (Grand 1978; Spainhower et al. 2018). At worst, when supported by only one limb in suspension, the flexor tendons can sustain 2.5–4.2 times the body weight of sloths. While these values are within the typical range of safety factors for mammalian tendons, sloths rarely employ single limb postural support and walk with a lateral sequence diagonal couplet gait (Mendel 1985; Nyakatura et al. 2010; Gorvet et al. 2020) where three limb support is most common. When supported by three limbs, safety factors increase substantially (Table 1), ranging upwards of 7–10 for sloths, although we caution that our estimates are calculated with the assumption that the tendons alone are supporting the body mass (i.e., functional load) with no assistance from muscle activation. Nevertheless, despite lacking large tensile strength as we originally expected, the flexor tendons of sloths appear to be “overbuilt” for the usual loads that they must resist, consistent with an important role in suspension. It is also likely that the robustness of sloth tendons belies the large strength and stiffness properties typical of thick tendons (Ker et al. 1988). The relative composition of proteoglycans (ground substance) versus Type I collagen, as well as the orientation of the collagen fibers in the flexor tendons of Choloepus and Bradypus are not known. Future studies of tendon histology seek to overcome this limitation to our present interpretation. In particular, such evaluations should test the hypothesis that the relationship between tissue composition and function in limb tendons is a possible plesiomorphic trait in sloths.

Similar to ungulates, which have relatively long, thin tendons and suspensory “ligaments” for their large size, as well as elongated distal limb length, the digital flexor tendons of Choloepus (Mendel 1981b, 1981c) and Bradypus (Olson et al. 2018) are equally impressive and also paired with elongate skeletal elements of the feet. Moreover, sloths have long, re-curved claws and the combination of a hook-like shape to their feet and robust tendon (volar) tunnels have additionally been argued to be features acquired independently for suspensory habits (Mendel 1981a, 1981b). Based on the observed morphology, it was previously proposed (Mendel 1985) that the body weight of sloths was supported by passive tension in the digital flexor tendons that “locked” in a fixed position to confirm grip on the substrate by the feet/claws. Support for this functional hypothesis depends on the relative stiffness versus compliance of the tendons, and by having both low tendon tensile strength and elasticity, some form of suspensory modification to sloth digital flexor tendons is indicated. However, it is not clear how these tendons would “lock” into place or how they would be latched and released by their well-developed volar tunnels. Moreover, sloth digital flexor tendons may be too compliant for strictly passive support, often displaying strains approximating 20–25% in the linear elastic region. This finding suggests a potential reduction in collagen fiber content corresponding with modifications of both reduced skeletal mass and skeletal muscle mass in sloths (Grand 1978).

Grip on the substrate is critical to the ability of sloths to remain in suspension and distal flexor muscles are in series with flexor tendons for joint position control (Biewener and Roberts 2000). It is the integrated function of an MTU that determines a role in support and/or energy savings and we speculate that the compliance observed in sloth flexor tendons may allow fascicles of the FDP to modulate tendon stiffness by undergoing minimal length changes during tensile loading of the MTU. Patterns of low muscle activation observed for the FDP in B. variegatus during suspensory hanging (Gorvet et al. 2020) match this expectation and conceivably serve to lower muscle contractile energy expenditure. By this mechanism, the FDP would produce limited force but enough to counterbalance tensile loading of its four tendon slips to sustain flexion of the digits/claws, all while minimizing muscle activation, thus allowing the digital flexors of sloths to act as important anti-gravity muscles (Fig. 1). EMG recordings from the digital flexors and forelimb extensors of horses support our interpretations by also showing minimal activation during standing (Jansen et al. 1998; Butcher et al. 2009; Harrison et al. 2012). The action of postural muscles to stabilize joints saves horses appreciable amounts of metabolic energy (Biewener 1998). In addition, the m. interosseous medius provides largely passive support to the metacarpophalangeal joints in horses for standing (Hildebrand 1960); however, activation of its extremely short muscle fibers stiffens this highly modified flexor muscle in accordance with dynamic body weight support needs of the animal (Soffler and Hermanson 2006). Again, we anticipate analogous functional modulations in the distal limbs of sloths.

Beyond the material properties of the flexor tendons, the structure/function of the muscle bellies of sloth digital flexors is similar to those participating in the suspensory apparatus of upright ungulates (Hildebrand 1960; Butcher et al. 2007, 2010). Specifically, the digital flexor complex (FDP and m. flexor digitorum superficialis) is correspondingly the most massive (intrinsic) muscle functional group in the forelimb of B. variegatus and each muscle belly has pennate fascicles with appreciable PCSA (Olson et al. 2018) as seen in horse forelimbs (Hermanson and Cobb 1992; Butcher et al. 2010). Other observations indicate that the FDP in sloths may have appreciable tendinous fibers throughout its cross-section (Spainhower et al. 2018), which suggests that active contractile muscle mass could be sacrificed for enhanced intramuscular tendon for suspensory function without increasing the cost of force production. This type of tissue exchange may also contribute to the reduced skeletal muscle mass in sloths (Grand 1978). Overall, functional tradeoffs between tendon compliance and stiffness appear to be an energetically economical means to support body weight while still providing the ability of joint position control for a strong grip on the substrate. That is, sloths may maintain the minimal amount of tendon tissue necessary for suspensory support (vertical SRF = 0.7 BM: Granatosky and Schmitt 2017) and rely on muscle force when greater tendon stiffness is needed.

Re-evaluation of mammalian tendon properties

Figure 6 shows values of ultimate tensile strength and elastic (Young’s) modulus (E) for mammalian tendons taken from the literature and grouped by locomotor habits (e.g., saltatorial, cursorial, generalist, etc.). Contrary to the persisting dogma that emphasizes high strength and elasticity in distal limb tendons for elastic strain energy storage and recovery (Alexander 1984; Bennett et al. 1986; Biewener 1998), sloth digital flexor tendons are characterized by both low strength and elasticity, and these data group completely opposite to that of tendons with cursorial and saltatorial specialization. Moreover, similar data for equine suspensory “ligaments” (SL) match well with the material properties measured from sloth flexor tendons, albeit the values for E that we extrapolated for the SL (Jansen et al. 1998) are minimal. While methods of data acquisition might have been different from some studies for which values were taken from the literature, we are confident in our analysis and propose that this combination of tendon properties observed from sloths represents a simplification for suspensorial habits, thus providing the most direct support to our hypothesis that sloth FDP tendons have the ability to function analogous to an ungulate suspensory apparatus for energy conservation.

Fig. 6.

Fig. 6

Open in a new tab

Relationship between ultimate tensile strength (in MPa) and elastic (Young’s) modulus (in MPa) across mammals. Line of unity has a slope equal to 1.0. Experimental data were assembled from numerous sources in the literature (wallaby calcaneal tendon: Bennett et al. 1986; horse suspensory ligament: Jansen et al. 1998; horse superficial/deep digital flexor tendons: Biewener 1998; LaCroix et al. 2013; human and rat calcaneal tendons: LaCroix et al. 2013; kangaroo rat gastrocnemius/plantaris tendons: Javidi et al. 2019). Sloth and monkey data are from this study. Ellipses show functional categorizations of tendon properties based on locomotor habits (substrate use). Data grouped by the rectangle near the origin are placed in the proposed “suspensorial” functional grouping by emphasizing low-to-modest tensile strength and/or elastic modulus in “simplified” tendon tissue from these taxa.

Recognizing that distal limb tendons from mammals with diverse locomotor behaviors can be modified (or “simplified”) in their material properties is not necessarily novel (Alexander and Dimery 1985; Dimery and Alexander 1985; Bennett et al. 1986; Dimery et al. 1986; Ker et al. 1988; Biewener 1998; Biewener and Roberts 2000), but the extent to which functional adaptation influences tendon performance has been overlooked until recently. Javidi et al. (2019) showed that large tensile strength and elastic modulus are decoupled in the long, thin hindlimb (calcaneal and plantaris) tendons of kangaroo rats, which perform ricochetal jumping without reliance on elastic energy storage/recovery. Strength and elastic modulus of tendons do not have to correlate as they are observed for numerous other mammals that are typically studied, including rats, humans, horses, and various domesticated species (LaCroix et al. 2013). And while exceptional tendon performance in kangaroo rat limb warrants further study for understanding mechanisms or microstructure that drive differential adaptation in tendon mechanical properties, sloth tendons are just as extraordinary, but for their lack of tendon strength and elasticity despite their robustness. Again, our broad interpretation of tendon structure and function is limited by the comparative lack of studies on tendon histology and tissue composition. Moreover, flexor vs. extensor tendons (e.g., calcaneal, quadriceps, and digital flexor tendons) with predicted major roles in limb loading patterns are too often the target of functional studies. It also may be insightful to study the material properties of tendons with a lesser role in weight-bearing support to address questions about universal investment in and maintenance of tendon tissue.

Across mammals, tendon strength and elasticity are broadly reflective of generalized substrate use. Thus, our comparative analysis shows that, overall, material properties are part of a continuum independent of body size (Fig. 6), and areas of overlap between the differing locomotor habits could be interpreted as functional trade-offs in tendon performance. For example, there are modifications in tendon material properties among arboreal, semi-arboreal, and generalized mammals where elastic modulus differs significantly between the selected taxa, whereas tensile strength is only different for the extremes of arboreal and generalized habits (Fig. 5). A comparison between sloths and rats emphasizes obligate (anti-pronograde) suspension in an arboreal mammal that requires greater tendon compliance versus greater strength and stiffness needed for translation of joint power during pronograde terrestrial locomotion. These results may also point to differences in functional roles between fore- and hindlimb pairs in suspensorial vs. terrestrial taxa.

Interestingly, data from the forelimb digital flexor tendons of vervet monkeys coincide with those from two- and three-toed sloths warranting their placement in our suspensorial data grouping. The species Chl. aethiops is semi-arboreal and is limited in its use of suspensory modes of locomotion and posture. However, whereas primates often bear more weight on their hindlimbs than forelimbs during terrestrial and pronograde arboreal locomotion (Schmitt and Hanna 2004; Granatosky et al. 2016a, 2016b), they shift body weight to their forelimbs as the main supports for suspension (Granatosky et al. 2018a) and this compensatory behavior may account for the similarity in primate and sloth flexor tendon properties. We speculate that there may be additional undiscovered functional trade-offs in the strength/stiffness and elastic properties of both tendon and bone tissue across arboreal mammals that routinely load their limbs in tension. Available evidence suggests that there are indeed multiple similarities in forelimb bone shape (Patel et al. 2013) and microstructural properties such as bone density (Patel and Carlson 2008) and trabecular architecture (Amson et al. 2017) between sloths and suspensory primates associated with functional adaptations for suspensory habits. Our future research aims to further understand modifications of tensile limb systems in primates and if the presence of a tendon suspensory apparatus is strictly adapted for near obligatory suspension or do tendon properties represent additional compromises (or simplifications) relating to various modes of arboreal locomotion. This work will also test the hypothesis that compressive versus tensile bone strength in mammals (Currey 1970, 1987, 1990; Biewener 1982; Erickson et al. 2002) is more plastic than previously considered, and the forelimb skeletal elements from sloths and arboreal primates will be our main models.

Data availability

Tendon loading data are available from the corresponding author upon reasonable request. All other data generated or analyzed during this study are included in this published article in adherence to disclosure policy of the Journal.

Acknowledgments

We sincerely thank Gerald Richardson (Dallas World Aquarium) for coordinating the research partnership with The Sloth Sanctuary of Costa Rica. Special thanks to Jesse Young (NEOMED) and Hazel Marie (YSU) for providing access to and assistance with use of the Instron machines. We thank Michael Granatosky (NYIT) for providing vervet monkey specimens. Thank you to two anonymous reviewers for very helpful comments. Thanks to Lydia Johnson, Abdel Yusuf, Branson Brownfield, Dakota Morgan, and Joshua Schlueter for assistance with data collection and analysis. Portions of the work will be submitted as a Master Thesis by A.M.M. with a Cushwa/Commercial Shearing Fellowship providing support during AY 2019–2020. The YSU College of STEM, Office of Research, and Departments of Biological Sciences and Mechanical Engineering are acknowledged for their support of graduate student research. The Department of Neurobiology and Anatomy at NEOMED is also gratefully acknowledged.

Authors’ contributions

A.M.M. developed the concepts and experimental approach, collected and analyzed data, and drafted the manuscript; B.L.A. performed data collection and analysis; J.A.A.-A. developed the concepts and provided sloth specimens; M.T.B. developed the concepts and experimental approach, performed data collection, and drafted and revised the manuscript. All authors contributed to manuscript editing.

References

  1. Alexander RM.  1984. Elastic energy stores in running vertebrates. Am Zool 24:85–94. [Google Scholar]
  2. Alexander RM.  1981. Factors of safety in the structure of animals. Sci Prog  67:109–30. [PubMed] [Google Scholar]
  3. Alexander RM.  1985. Body support, scaling, and allometry In: Bramble DM, Liem KF, Wake DB, editors. Functional vertebrate morphology. Cambridge (MA: ): Harvard University Press; p. 26–37. [Google Scholar]
  4. Alexander RM.  1988. Elastic mechanisms in animal movement. Cambridge: Cambridge University Press. [Google Scholar]
  5. Alexander RM, Dimery NJ.  1985. Elastic properties of the forefoot of the Donkey, Equus asinus. J Zool  205:511–24. [Google Scholar]
  6. Amson E, Arnold P, van Heteren AH, Canoville A, Nyakatura JA.  2017. Trabecular architecture in the forelimb epiphyses of extant xenarthrans (Mammalia). Front Zool  14:52. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bennett MB, Ker RF, Imery NJ, Alexander RM.  1986. Mechanical properties of various mammalian tendons. J Zool  209:537–48. [Google Scholar]
  8. Biewener AA, Baudinette R.  1995. In vivo muscle force and elastic energy storage during steady-speed hopping of tammar wallabies (Macropus eugenii). J Exp Biol  198:1829–41. [DOI] [PubMed] [Google Scholar]
  9. Biewener AA, Roberts TJ.  2000. Muscle and tendon contributions to force, work, and elastic energy savings: a comparative perspective. Exerc Sport Sci Rev  3:99–107. [PubMed] [Google Scholar]
  10. Biewener AA.  1982. Bone strength in small mammals and bipedal birds: do safety factors change with body size?. J Exp Biol  98:289–301. [DOI] [PubMed] [Google Scholar]
  11. Biewener AA.  1998. Muscle-tendon stresses and elastic energy storage during locomotion in the horse. Comp Biochem Physiol  120:73–87. [DOI] [PubMed] [Google Scholar]
  12. Butcher MT, Bertram JEA, Benzuidenhout AJ.  2006. Collateral ligaments of the distal sesamoid bone in the digit of Equus: re-evaluating midstance function. J Morphol  267:1177–85. [DOI] [PubMed] [Google Scholar]
  13. Butcher MT, Hermanson JW, Ducharme NG, Mitchell LM, Soderholm LV, Bertram JEA.  2007. Superficial digital flexor tendon lesions in racehorses as a sequela to muscle fatigue: a preliminary study. Equine Vet J  39:540–5. [DOI] [PubMed] [Google Scholar]
  14. Butcher MT, Hermanson JW, Ducharme NG, Mitchell LM, Soderholm LV, Bertram JEA.  2009. Contractile behavior of the forelimb digital flexors during steady-state locomotion in horses (Equus caballus): an initial test of muscle architectural hypotheses about in vivo function. Comp Biochem Physiol B Biochem Mol Biol  152:100–14. [DOI] [PubMed] [Google Scholar]
  15. Butcher MT, Chase PB, Herman son 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 Regul Integr Comp Physiol  299:996–1005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Cliffe RN, Scantlebury DM, Kennedy SJ, Avey-Arroyo J, Mindich D, Wilson RP.  2018. The metabolic response of the Bradypus sloth to temperature. PeerJ  6:e5600. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Currey JD.  1970. The mechanical properties of bone. Clin Orthop Relat Res  73:210–31. [PubMed] [Google Scholar]
  19. Currey JD.  1987. The evolution of the mechanical properties of amniote bone. J Biomech  20:1035–44. [DOI] [PubMed] [Google Scholar]
  20. Currey JD.  1990. Physical characteristics affecting the tensile failure properties of compact bone. J Biomech  23:837–44. [DOI] [PubMed] [Google Scholar]
  21. Dimery NJ, Alexander RM.  1985. Elastic properties of the hind foot of the Donkey, Equus asinus. J Zool  207:9–20. [Google Scholar]
  22. Dimery NJ, Ker RF, Alexander RM.  1986. Elastic properties of the feet of deer (Cervidae). J Zool  208:161–9. [Google Scholar]
  23. Dyce KM, Sack WO, Wensing CJG.  1996. The forelimb of the horse In:  Textbook of veterinary anatomy. 2nd ed Philadelphia (PA: ): W.M. Saunders Co; p. 573–609. [Google Scholar]
  24. Erickson GM, Catanese JII, Keaveny TM.  2002. Evolution of the biomechanical material properties of the femur. Anat Rec  268:115–24. [DOI] [PubMed] [Google Scholar]
  25. Gaudin TJ.  2004. Phylogenetic relationships among sloths (Mammalia, Xenarthra, Tardigrada): the craniodental evidence. Zool J Linn Soc  140:255–305. [Google Scholar]
  26. Gorvet MA, et al.  2020. Keep calm and hang on: EMG activation in the forelimb musculature of three-toed sloths. J Exp Biol  223 (doi:10.1242/jeb.218370). [DOI] [PubMed] [Google Scholar]
  27. Granatosky MC, Fitzsimons A, Zeininger A, Schmitt D.  2018. a. Mechanisms for the functional differentiation of the propulsive and braking roles of the forelimbs and hindlimbs during quadrupedal walking in primates and feline. J Exp Biol  221:1–11. [DOI] [PubMed] [Google Scholar]
  28. Granatosky MC, Karantanis NE, Rychlik L, Youlatos D.  2018. b. A suspensory way of life: integrating locomotion, postures, limb movements, and forces in two-toed sloths Choloepus didactylus (Megalonychidae, Folivora, Pilosa). J Exp Zool  329:570–88. [DOI] [PubMed] [Google Scholar]
  29. Granatosky MC, Schmitt D.  2017. Forelimb and hindlimb loading patterns during below branch quadrupedal locomotion in the two-toed sloth. J Zool  302:271–8. [Google Scholar]
  30. Granatosky MC, Tripp CH, Fabre AC, Schmitt D.  2016. a. Patterns of quadrupedal locomotion in a vertical clinging and leaping primate (Propithecus coquereli) with implications for understanding the functional demands of primate quadrupedal locomotion. Am J Phys Anthropol  160:644–52. [DOI] [PubMed] [Google Scholar]
  31. Granatosky MC, Tripp CH, Schmitt D.  2016. b. Gait kinetics of above- and below branch quadrupedal locomotion in lemurid primates. J Exp Biol  219:53–63. [DOI] [PubMed] [Google Scholar]
  32. Grand TI.  1978. Adaptations of tissue and limb segments to facilitate moving and feeding in arboreal folivores In: Montgomery GG, editor. The ecology of arboreal folivores. Washington (DC: ): Smithsonian Press; p. 231–41. [Google Scholar]
  33. Harrison SM, Whitton RC, King M, Haussler KK, Kawcak CE, Stover SM, Pandy MG.  2012. Forelimb muscle activity during equine locomotion. J Exp Biol  215:2980–91. [DOI] [PubMed] [Google Scholar]
  34. Hayssen V.  2010. Bradypus variegatus (Pilosa: Bradypodidae). Mamm Spec  42:19–32. [Google Scholar]
  35. Hayssen V.  2011. Choloepus hoffmanni (Pilosa: Megalonychidae). Mamm Spec  43:37–55. [Google Scholar]
  36. Hermanson JW, Cobb MA.  1992. Four forearm flexor muscles of the horse, Equus caballus: anatomy and histochemistry. J Morph  212:269–80. [DOI] [PubMed] [Google Scholar]
  37. Hildebrand M.  1960. How animals run. Sci Am  202:148–57. [DOI] [PubMed] [Google Scholar]
  38. Hildebrand M.  1987. The mechanics of horse legs. Am Sci  75:594–601. [Google Scholar]
  39. Hodson-Tole EF, Wakeling JM, Dick TJM.  2016. Passive muscle-tendon unit gearing is joint dependent in human medial gastrocnemius. Front Physiol  7:1–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Jansen MO, Schamhardt HC, van den Bogert AJ, Hartman W.  1998. Mechanical properties of the tendinous equine interosseus muscle are affected by in vivo transducer implantation. J Biomech  31:485–90. [DOI] [PubMed] [Google Scholar]
  41. Javidi M, McGowan CP, Schiele NR, Lin DC.  2019. Tendons from kangaroo rats are exceptionally strong and tough. Nature  98196:1–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Ker RF, Alexander RM, Bennett MB.  1988. Why are mammalian tendons so thick?  J Zool  216:309–24. [Google Scholar]
  43. LaCroix AS, Duenwald-Kuehl SE, Lakes RS, Vanderby R.  2013. Relationship between tendon stiffness and failure: a metaanalysis. J Appl Physiol  115:43–51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Lieber RL.  2002. Skeletal muscle structure, function, and plasticity (ed. T. Julet).  Baltimore (MD: ): Lippincott Williams & Wilkins. [Google Scholar]
  45. Mendel FC.  1981a. Use of hands and feet of two-toed sloths (Choloepus hoffmanni) during climbing and terrestrial locomotion. J Mamm  62:413–21. [Google Scholar]
  46. Mendel FC.  1981b. The hand of two-toed sloths (Choloepus): its anatomy and potential uses relative to size of support. J Morphol  169:1–19. [DOI] [PubMed] [Google Scholar]
  47. Mendel FC.  1981. c. Use of hands and feet of two-toed sloths (Choloepus hoffmanni) during climbing and terrestrial locomotion. J Mamm  62:413–21. [Google Scholar]
  48. Mendel FC.  1985. Use of hands and feet of three-toed sloths (Bradypus variegatus) during climbing and terrestrial locomotion. J Mamm  66:359–66. [Google Scholar]
  49. Montanez-Rivera I, Nyakatura JA, Amson E.  2018. Bone cortical compactness in tree sloth reflects convergent evolution. J Anat  233:580–91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Montgomery GG, Sunquist ME.  1978. Habitat selection and use by two-toed and three-toed sloths In: Montgomery GG, editor. The ecology of arboreal folivores.  Washington (DC: ): Smithsonian University Press; p. 329–59. [Google Scholar]
  51. Nyakatura JA.  2012. The convergent evolution of suspensory posture and locomotion in tree sloths. J Mamm Evol  19:225–34. [Google Scholar]
  52. Nyakatura JA, Andrada E.  2013. A mechanical link model of two-toed sloths: no pendular mechanics during suspensory locomotion. Acta Theriol  58:83–93. [Google Scholar]
  53. 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. J Zool  113:221–34. [DOI] [PubMed] [Google Scholar]
  54. Olson RA, Glenn ZD, Cliffe RN, Butcher MT.  2018. Architectural properties of sloth forelimb muscles (Pilosa: Bradypodidae). J Mamm Evol  25:573–88. [Google Scholar]
  55. Patel BA, Carlson KJ.  2008. Apparent density patterns in subchondral bone of the sloth and anteater forelimb. Biol Lett  4:486–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Patel BA, Ruff CB, Simons ELR, Organ JM.  2013. Humeral cross-sectional shape in suspensory primates and sloths. Anat Rec  296:545–56. [DOI] [PubMed] [Google Scholar]
  57. Pauli JN, Peery MZ, Fountain ED, Karasov WH.  2016. Arboreal folivores limit their energetic output, all the way to slothfulness. Am Nat  188:196–204. [DOI] [PubMed] [Google Scholar]
  58. Schmitt D, Hanna JB.  2004. Substrate alters forelimb to hindlimb peak force ratios in primates. J Hum Evol  46:237–52. [DOI] [PubMed] [Google Scholar]
  59. Shadwick RE.  1990. Elastic energy storage in tendons: mechanical differences related to function and age. J Appl Physiol  68:1033–40. [DOI] [PubMed] [Google Scholar]
  60. Soffler C, Hermanson JW.  2006. Muscular design in the equine interosseus muscle. J Morph  267:696–704. [DOI] [PubMed] [Google Scholar]
  61. 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. [DOI] [PubMed] [Google Scholar]
  62. Sunquist ME, Montgomery GG.  1973. Activity patterns and rates of movement of two-toed and three-toed sloths (Choloepus hoffmanni and Bradypus infuscatus). J Mamm  54:946–54. [PubMed] [Google Scholar]
  63. Urbani B, Bosque C.  2007. Feeding ecology and postural behavior of the three-toed sloth (Bradypus variegatus flaccidus) in northern Venezuela. Mamm Biol  72:321–9. [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

Tendon loading data are available from the corresponding author upon reasonable request. All other data generated or analyzed during this study are included in this published article in adherence to disclosure policy of the Journal.

Articles from Integrative Organismal Biology are provided here courtesy of Oxford University Press

RESOURCES