The Evolution of Tendon — Morphology and Material Properties૾

Comparative Biochemistry and Physiology Part A 133 (2002) 1159–1170

Review The evolution of tendon — morphology and material properties૾

Adam P. Summersa, *, Thomas J. Koobb

aEcology and Evolutionary Biology, 321 Steinhaus Hall, University of California, Irvine, CA 92697-2525, USA bShriners Hospital for Children, 12502 North Pine Drive, Tampa, FL 33612, USA

Received 25 February 2002; received in revised form 19 August 2002; accepted 19 August 2002

Abstract

Phylogenetically, tendinous tissue first appears in the invertebrate chordate Branchiostoma as myosepta. This two- dimensional array of collagen fibers is highly organized, with fibers running along two primary axes. In hagfish the first linear tendons appear and the myosepta have developed specialized regions with unidirectional fiber orientation—a linear tendon within the flat sheet of myoseptum. Tendons react to compressive load by first forming a fibrocartilaginous pad, and under severe stress, sesamoid bones. Evidence for this ability to react to load first arises in the cartilaginous fish, here documented in a tendon from the jaw of a hard-prey crushing stingray. Sesamoid bones are common in bony fish and also in tetrapods. Tendons will also calcify under tensile loads in some groups of birds, and this reaction to load is seen in no other vertebrates. We conclude that the evolutionary history of tendon gives us insight into the use of model systems for investigating tendon biology. Using mammal and fish models may be more appropriate than avian models because of the apparent evolution of a novel reaction to tensile loads in birds. ᮊ 2002 Elsevier Science Inc. All rights reserved.

Keywords: Stress; Strain; Tensile; Collagen; Hagfish; Agnathans; Strength; Stiffness; Morphology; Material properties; Model systems; Connective tissue; Evolutionary transitions; Vertebrata

muscle to bone, but this definition does not begin ‘‘Tendons, forming the attachment of many muscles, to account for the varied forms of tendinous consist of bundles of connective tissue fibers’’ tissue—even within a single organism—its adap- Alfred S. Romer. tation to load, or the form that it takes in lower 1. Introduction vertebrates. In order to understand the evolution of the musculoskeletal system in vertebrates it is Tendon is most often thought of as the bright important to understand the evolutionary history white, parallel fibered connective tissue that joins of tendon as a tissue. Our understanding of tendon has lagged behind that of bone and cartilage, both ૾ This paper was presented at ‘Tendon – Bridging the Gap’, a symposium at the 2002 Society of Integrative and Compar- of which have been placed in an evolutionary ative Biology. Participation was funded by SICB, The Shriners context (Moss and Moss-Salentijn, 1983; Person, Hospitals for Children, and the National Science Foundation 1983; Smith and Hall, 1990). In fact, comparative (IBN-0127260). research on tendon is so rare that this project may *Corresponding. Tel.: q1-949-824-9359; fax: q1-510-315- 3106. be premature. Nevertheless, we attempt in the next E-mail addresses: [email protected] (A.P. Summers), few pages to synthesize tendon research in an [email protected] (T.J. Koob). evolutionary context, if for no other purpose than

1095-6433/02/$ - see front matter ᮊ 2002 Elsevier Science Inc. All rights reserved. PII: S1095-6433Ž02.00241-6 1160 A.P. Summers, T.J. Koob / Comparative Biochemistry and Physiology Part A 133 (2002) 1159–1170 to point out those areas that sorely need further those taxa that exhibit novel morphology relative investigation. to this ‘ancestral’ state. We consider tendon to be a tissue, and will refer to it as such, though at times we will use ‘tendi- 2.1. Urochordates nous tissue’ to make clear the distinction between the tissue and a particular tendinous organ (i.e. The most well known group of urochordates, digital flexor tendon). Our working definition of the ascidians or sea-squirts, are sessile as adults, tendon is an amalgam of functional and composi- but as larvae they may be free-swimming ‘tad- tional definitions: a dense, highly organized tissue poles’ propelling themselves along a helical path that transmits force, and is composed predomi- with undulations of their tail (Gans et al., 1996; nantly of type I collagen with fibril associated McHenry, 2001). The muscles that drive this loco- proteoglycans. motion are not divided by collagenous myosepta, and the muscle itself more closely resembles car- 2. Morphology diac than striated muscle (Cloney and Burighel, 1991). The only hint of tendinous tissue is in a Tendon is most familiar as the densely packed, series of collagenous, connective tissue leaflets linearly-arrayed, collagenous tissue seen in flexor that issue from the notochordal sheath but do not and extensor tendons in tetrapod limbs. However, appear to be attached to muscle (Cloney, 1964). it should be recognized that there are other collag- At present there is no evidence for tendinous enous connective tissues that perform the same structures in urochordates. functional task, that of transferring force generated by muscle from the muscle end to a target. These 2.2. Cephalochordates include the dense, well-organized arrays of connective tissue in the myosepta of lower vertebrates, The undulatory locomotion of the lancelets is as well as aponeuroses. powered by myotomal muscle divided by collag- The body musculature of vertebrates is arranged enous myosepta (Fig. 1)(Weitbrecht, 2000),a in serially homologous myomeres, each separated feature that is clearly seen in several fossil forms from the next by a collagenous myoseptum. In including Pikaia from the Burgess Shale. humans one of the few vestiges of this segmenta- There is scant evidence of any linear tendons in tion is the ‘six-pack’ of the abdominal muscles, lancelets, the only possible exception being struc- but as anyone who has eaten a fish fillet can attest, tures that Ruppert (1991) refers to as ‘micro- blocky myomeres are far more obvious in lower ligaments’. These are connective tissue projections vertebrates. Myosepta are not mats of disorganized that join the myomeric muscle to the body wall, collagen but rather highly organized structures with however, they are quite thin (1–5 mm) and there collagen organized in uni- or bi-directional sheets is no evidence that they are collagenous. We infer (Liem et al., 2000; Vogel and Gemballa, 2000). that well-organized and functional fibrous myosep- Furthermore, it should be recognized that simple ta appear for the first time in the chordate lineage myosepta and linearly-arrayed tendon are extremes in Cephalochordates. in a continuum. There are numerous examples from fish and tetrapods of aponeuroses that grade 2.3. Agnathans into tendon (Liem et al., 2000), and, within the myosepta of fish there are collagen fibers with The jawless fish, lampreys and hagfish use preferred orientation that form linear tendon struc- myomeric muscle to power undulatory locomotion, tures (Westneat et al., 1993; Vogel and Gemballa, and according to the well preserved fossils of 2000; Gemballa and Vogel, 2002). Haikouichthys and Myllokunmingia, this has been In this section we will examine morphological the case since the Lower Cambrian (490–540 innovations in these dense, collagenous tissues that MYA)(Chen et al., 1999; Shu et al., 1999). The serve to transmit the force of muscles across an myosepta are collagenous sheets with evidence for array of chordate taxa. In the interest of brevity the local specializations that form linearly arrayed we will establish a plesiomorphic condition for tendons in bony fish (Vogel and Gemballa, 2001). tendinous tissue and then specifically treat only Hagfish also have an interesting hydrostatic tongue A.P. Summers, T.J. Koob / Comparative Biochemistry and Physiology Part A 133 (2002) 1159–1170 1161

2.4. Cartilaginous and bony fish

Cartilaginous and bony fish have tendinous myosepta between the blocks of body musculature as well as linear tendons associated with jaw and pharyngeal muscles. The former appear quite similar to the myosepta in agnathans with some specialized regions that are linear in orientation (Hagen et al., 2001). The linear tendons found in the feeding apparatus resemble those of mammals and some individual tendons are likely homologs of mammalian tendons (i.e. an adductor mandibularis tendonstemporalis tendon)(Liem et al., 2000). Furthermore, the cartilaginous fish show tendon specializations that have previously only been reported in tetrapods. Tendons are normally subjected to tensile loads, however when one makes a sharp turn around a corner it is also subjected to compressive and shear loading in the region of the bend. This compressive loading leads to the formation of a fibrocartilaginous pad along the inner surface of the bend (Vogel and Koob, 1989; Benjamin and Ralphs, 1998). Some stingrays eat hard prey almost exclusively, and have several specializations of their jaws that reinforce their mandibular cartilage and increase the effective force of their jaw adductors (Sum- mers et al., 1998; Summers, 2000). The ventral intermandibular tendon of one of these specialists, the cownose ray (Rhinoptera bonasus), makes a sharp turn as it passes dorsally around the corner Fig. 1. A light micrograph of a single myseptum from Bran- of the jaws. We found a fibrocartilaginous pad chiostoma lanceolatum shows the organization of the collagen associated with the tendon along the inner edge of fibers into a two-dimensional array. The inscribed lines are to ( ) indicate the two primary directions of the collagen fibers (mod- this sharp bend Fig. 4a . Histologically it appears ified with permission from Weitbrecht, 2000). similar to fibrocartilage from mammals (Fig. 4b) and we believe this is the phylogenetically earliest protrusion and retraction mechanism that involves example of tendon’s ability to adapt to compres- two pennate muscles and two linear tendons (Fig. sive load. The ability of tendon to respond to 2)(Coles, 1905, 1907, 1914). We have prepared compressive load by forming a fibrocartilaginous histological sections (10 mm paraffin) of one of pad has been confirmed in amphibians (Carvalho the tongue retractor tendons (M. retractor mandi- and Vidal, 1994, 1995), archosaurs (Felisbino and buli tendon). The tendon is superficially quite Carvalho, 1999), and mammals (for review see similar in appearance to that of mammals, having Benjamin and Ralphs, 1998). the characteristic bright white color, clearly orient- A further adaptation to compressive load is the ed fibrous material, and discrete edges. However, formation of sesamoid bones in regions of tendon it appears to lack the organization into primary that bend over a bony prominence (for review see and secondary bundles, as well as the epitenon Sarin et al., 1999). These bones arise within the and paratenon seen in mammals (Kastelic et al., tendon and may be encapsulated in a synovial 1978). The only indication of this hierarchical sheath. In mammals there is evidence that sesa- organization is that there is an inner ‘core’ tendon moid formation can be induced by load, however wrapped with an outer ‘sheath’ tendon (Fig. 3). some sesamoids form regardless of force regime 1162 A.P. Summers, T.J. Koob / Comparative Biochemistry and Physiology Part A 133 (2002) 1159–1170

Fig. 2. Panels 1–4show the retraction of the toothy tongue of Myxine glutinosa accomplished by manually pulling on the retractor tendon. Scale bars5 mm. The lower panel shows the anatomy of the teeth, the supporting cartilage and the two tendons that protract and retract the tooth plate (modified from Coles, 1907).

(i.e. the patella). There are no sesamoids in carti- 2.5. Archosaurs laginous fish, but they are prominent in bony fish. The urohyal, the bone that supports the tongue, In addition to the aforementioned response to a may be the most well known example, though compressive load there are indications that tendon other bones of the branchial arches are also formed will respond to tensile loads by mineralizing (for in tendon and are clear in fossil and recent taxa review see Landis, 2002). These mineralizations (Patterson, 1977; Arratia and Schultze, 1990; Liem are quite different from sesamoid bone, in that et al., 2000). Sesamoids are widespread in other they never become encapsulated in a synovial vertebrates including amphibians (Olson, 2000; envelope, they do not have the histology of bone, Trueb et al., 2000), squamate reptiles (Maisano, and they are not associated with tendons passing 2001), archosaurs (Sych, 2001; Hutchinson, over bony prominences. Rather these mineraliza- 2002), and mammals. tions usually arise when a tendon bifurcates, lead- A.P. Summers, T.J. Koob / Comparative Biochemistry and Physiology Part A 133 (2002) 1159–1170 1163

3. Material properties

There are two principal difficulties in synthesiz- ing an evolutionary perspective on the material properties of tendon: firstly, there is no accepted standard protocol for testing, so results of different studies are difficult to compare; second, there are few literature values for the mechanical properties of tendon from lower vertebrates, and none at all from cartilaginous fish or agnathans. To address the first issue we present a range of representative published values for several biomechanically important measures of the response of tendon to applied force. To provide a broader evolutionary picture we also present original data from our own tests on a relatively obscure, linearly arrayed tendon from the hagfish described above. Biological structures are notoriously difficult to characterize with the standard material properties, such as strength and stiffness, used for manufac- tured solids. The reasons for this fall into two categories—technical problems that have their basis in the inconvenient sizes and shapes of living tissue; and difficulties that arise from the heterogeneous make-up and visco-elasticity of natural materials (Vogel, 1988; Niklas, 1992; Martin et al., 1998). Tendons present special technical chal- Fig. 3. (a) An alcian blue stained longitudinal section through lenges from the point of view of clamping and the tongue retractor tendon approximately midway along its preconditioning, and are certainly heterogeneous, length. The gaps in the dense connective tissue separate the inner ‘core’ tendon from the outer ‘sheath’ tendon and are the viscoelastic materials, nevertheless there is an only indication of tendon organization. Scale bars200 mm. (b) extensive literature on the tensile properties of An hemotoxylin and eosin stained section showing the rela- mammalian tendon (i.e. Bennett et al., 1986; tively high cellularity of the gap region compared to the ten- Pollock and Shadwick, 1994b; de Zee et al., 2000). dinous region. There are few tenocytes evident, as is often the case in mammalian tendon. Scale bars125 mm. 3.1. Hagfish tendon ing to a higher load in the two smaller tendons We dissected 14, fresh, frozen hagfish (Myxine than there is in the conjoined tendons. They appear ) to have arisen in the non-avian dinosaurs (Hutch- glutinosa heads, removing the complete retractor inson, 2002), but as far as we can tell are found mandibuli tendon from its origin on a thin carti- in no other group of chordates. laginous rod at the posterior end of the tongue retractor muscle to the insertion on the cartilagi- 2.6. Mammals nous tooth plate (for relevant anatomy see Coles, 1907). Tendons were kept moist with hagfish Aside from the hierarchical organization of Ringers (0.53 M NaCl, 7 mM KCl, 4.5 mM CaCl, ( ) mammalian tendon Kastelic et al., 1978 , there 12 mM MgCl224 , 0.9 mM Na SO , 25 mM Tris at are no morphological characters of tendon that we pH 7.95)(Riegel, 1978) for the brief time between do not see in other vertebrate groups. A possible dissection and testing. Material properties were exception may be in the morphology of the tendon determined with a tensile test to failure using an entheses, the insertion of the tendon onto the bone, MTS Mini Bionix with a 500-g load cell at a but there are no comparative data from other taxa strain rate of 2 mmys. Approximately 1 cm of (Benjamin et al., 2002). each end of the tendon was held between the 1164 A.P. Summers, T.J. Koob / Comparative Biochemistry and Physiology Part A 133 (2002) 1159–1170

Fig. 4. (a) A ventral view of the upper and lower jaws of a cownose ray (Rhinoptera bonasus) showing the arrangement of the adductor mandibularis medialis (AMM) muscle and the associated tendon. (b) Masson’s trichrome stained paraffin section (10 mm thick) of the fibrocartilaginous pad from the AMM tendon showing regions of proteoglycan matrix (blue) and organized fibrous areas (red). Scale bars100 mm. (c) Section of the fibrocartilaginous region of a calf meniscus showing similar morphology to the stingray tendon. Scale bars100 mm serrate jaws of standard tensile grips. Grips were calipers to the nearest tenth of a millimeter. Stress then cooled by manual application of dry ice vs. strain curves were generated from the MTS (–78 8C) until the tissue inside the grips was data and used to calculate ultimate strength, stiff- visibly affected. Tissue between the grips (8–15 ness, and failure strain. mm) was checked with forceps to ensure that it The strength of the hagfish tongue retractor had not frozen. In spite of freeze clamping, the tendon was 47.8"3.5 MPa, and from the samples tendon shifted in the grips in 6 of 14tests resulting that did not slip in the clamps (ns8) we calculated in slippage artifacts that prevented us from using the strain at failure to be 22"2%. This value is these samples in calculating the maximum strain well beyond any reliable estimate of maximum of the specimen (Fig. 5). The diameter of the strain in mammalian tendon (-10%). The stiff- unstretched, cylindrical tendon was measured with ness of the tendon was 290"29 MPa. These values A.P. Summers, T.J. Koob / Comparative Biochemistry and Physiology Part A 133 (2002) 1159–1170 1165

Fig. 5. Stress vs. strain curves for the hagfish (Myxine glutinosa) tongue retractor tendon. The ranges of values for strength and breaking strain in mammalian tendon are indicated by the bars. are similar to values reported for some mammalian records for the limbless and enigmatic caecilians, tendons (Fig. 5). and a single record for salamanders—Azizi et al. (2002) found a maximum stiffness of 7.1 MPa for 3.2. Bony and cartilaginous fish the sheet-like tendinous myosepta of the siren (Siren lacertina). Although frogs are important Cartilaginous fish have few linearly arrayed model systems for the study of muscle only a few tendons (Liem and Summers, 1999), and there has studies address tendon mechanics, and those only been no assessment of their material properties, report values for stiffness (Lieber et al., 1991; nor the properties of the aponeurotic tendons. The Trestik and Lieber, 1993). Gastrocnemius tendon literature for bony fish contains just two data (Es1.5 GPa) is similar to mammals, but the points. In this volume Shadwick et al. (2002) semitendinosus (0.2 GPa) is only as stiff as hagfish report that the tail tendons of albacore and yellow- tendon. fin tuna, fast swimming scombrid fish, are quite stiff (1.19–1.43 GPa), and they estimate a break- 3.4. Archosaurs ing strength near 30 MPa. Of the two extant groups of archosaurs, the birds 3.3. Amphibians and the crocodilians, there are data only from the former, though the latter have prominent, function- Of the three extant groups of lissamphibians ally important tendons. Some groups of birds (and (frogs, salamanders, and caecilians) only frog ten- some extinct non-avian dinosaurs; Hutchinson, dons have been tested in depth. There are no 2002) mineralize their tendons, which has a pro- 1166 A.P. Summers, T.J. Koob / Comparative Biochemistry and Physiology Part A 133 (2002) 1159–1170

1994b; Pike et al., 2000). From a functional point of view mammalian tendons fall into two categories, those that act as springs, such as the Achilles and digital flexor tendons of quadrupedal mammals, and those that simply transmit muscle force without storing significant energy, as in the digital extensors and biceps tendon (Alexander, 1984; Biewener and Blickhan, 1988; Biewener, 1998). Oddly, though these two functions might best be addressed by varied material properties, it seems that natural selection has not led to significant differences between them (Pollock and Shadwick, 1994b). In other words, while it would seem logical that the amount of strain energy stored in a tendon could be ‘tuned’ by varying the stiffness and resilience, in fact these properties are relatively invariant across a wide variety of tendons. Rather than rehash these studies, or a subset of them, we would like to point out the high and low values that have been reported for several properties and present scattergrams that summarize a synoptic review of the literature (Fig. 6). Fig. 6. Scattergram showing values for (a) stiffness and (b) strength of tendon from several chordate taxa. The values for 4. Discussion hagfish (Myxine glutinosa) are from this paper. Data for fish (Shadwick et al., 2002), amphibians (Lieber et al., 1991, 2000; Though there is too little evidence from non- Trestik and Lieber, 1993), birds (Bennett and Stafford, 1988; mammalian taxa to be completely confident in an Leonard et al., 1976), and mammals (Bennett et al., 1986; Itoi et al., 1995; Kondo et al., 1998; Pollock and Shadwick, 1994b; evolutionary scenario, we would propose the fol- Wren et al., 2001) were gathered from literature sources. lowing hypotheses (Figs. 7 and 8). The first appearance of tendinous tissue is as myosepta, thin found effect on their properties (Bennett and Staf- ford, 1988). Indeed in some cases the stiffness of calcified tendon can approach that of bone (Leon- ard et al., 1976; Bennett and Stafford, 1988). Here we are interested in the unmineralized tendon’s behavior under load, which has been measured in the usual tensometer devices as well as in vivo, and in vitro using disparate techniques such as sonomicrometry, force buckles, and ultrasound (Biewener et al., 1992; Mohamed et al., 1995; Buchanan and Marsh, 2001). The stiffness of avian tendons (mineralized and unmineralized) ranged from 0.9 to 13 GPa, and the strength from 54to 117 MPa.

3.5. Mammals Fig. 7. Cladogram of the chordates (modified from Liem et al., There is a vast body of literature on the tech- 2000) showing the evolutionary transitions of tendon: (1) niques of testing mammalian tendon (i.e. Riemers- ‘leaflets’ of connective tissue emanating from the notochord sheath; (2) an organized array of collagen forms myosepta; (3) ma and Schamhardt, 1982; Martin et al., 1998; linear tendon; specializations in the myosepta; (4) tendon Ker et al., 2000), and on the properties of tendon responds to compressive loading with a fibrocartilaginous pad; (i.e. Bennett et al., 1986; Pollock and Shadwick, and (5) sesamoid bones in areas of high compressive loading. A.P. Summers, T.J. Koob / Comparative Biochemistry and Physiology Part A 133 (2002) 1159–1170 1167

an indication that tendon has not undergone any major evolutionary transitions in the mammals. This implies that some non-mammals, and even non-tetrapods, may be used as model systems for studying tendon development, physiology, morphology, and repair. It is important to note that birds may not be a good model system for mammalian tendon biology, as avian tendon appears to have evolved a novel response to tensile stress (Fig. 8). On the evolution of material properties there is little we can be sure of, but we would speculate that the high strength of linear tendon is primitive on the basis of our hagfish data. Stiffness may have increased over evolutionary time in the line- Fig. 8. Cladogram of the vertebrates (modified from Liem et ages that gave rise to fish and tetrapods, but al., 2000) showing the evolutionary transition of tendon: (1) strength arose early and has been little changed tendon responds to compressive loading with a fibrocartilagi- through evolutionary time. We require a more nous pad; (2) sesamoid bones in areas of high compressive loading; and (3) tendons in tension calcify in response to load. extensive survey of material properties in fish and lower tetrapods to generate further hypotheses. Clearly, we have woefully little knowledge of sheets of connective tissue with collagen fibers non-mammalian tendon. Among the significant organized to resist tension from several directions. groups for which there are little or no data are the As body plans became more adapted for high- squamate reptiles, turtles, and cartilaginous fish. speed undulatory locomotion the myosepta became This is particularly troubling given the interesting specialized, with some regions being composed transition that apparently takes place between the almost entirely of unidirectional collagen fibers— agnathans and the tetrapods—tendon becomes a linear tendon within the flat sheet of the myosep- stiffer, it gains an epitenon, and becomes integrated tal tendon. This is supported by the work of into the locomotor system as a spring. We cannot Gemballa’s group on Branchiostoma, agnathans, understand the current character states in mammals and fish (Vogel and Gemballa, 2001; Weitbrecht without learning the evolutionary trajectory that and Gemballa, 2001; Gemballa and Vogel, 2002). they traversed in getting there. Linear tendons appear in the agnathans (Acrania) In the area of material properties there are before the advent of vertebrates, and before the several topics that would be quite interesting to evolution of endochondral bone (Smith and Hall, know more about. The reported values for resil- 1990). This renders the textbook definition of ience, that is the efficiency of energy storage, for tendon as a tissue that connects muscle to bone mammalian and fish tendon are quite high—on somewhat problematic. the order of 90% (Alexander, 1984; Pollock and Sometime in or before the Silurian (440 to 410 Shadwick, 1994a; Shadwick et al., 2002). The fish mya) tendon acquired the ability to adapt to tendons and mammalian tendons that have been compressive loads by forming fibrocartilage, and tested are of similar stiffness (Fig. 6). From the by the Devonian, bony fish have formed sesamoid scant comparative data it is clear that there are bones (Patterson, 1977; Arratia and Schultze, tendons of far lesser stiffness in both frogs and 1990). This is supported by our own work on the hagfish. It would be interesting to know if the fibrocartilage of a cartilaginous fish (see preceding high resilience is linked to high stiffness or wheth- section) and by the fossil record of fish (Long, er these traits are independent. 1995). The ability to calcify tendon in response to The lack of an epitenon in the hagfish tongue tensile loads is not certainly present until the tendon may represent a primitive, less hierarchical evolution of birds in the Jurassic period (208 to structure. Comparative morphological data from 146 mya)(Padian, 1997). The uniformity in mate- bony and cartilaginous fish, amphibians and rep- rial properties and the lack of novel responses to tiles would settle the question of where the mam- loading in eutherian and metatherian mammals is malian architecture of tendon arose (Kastelic et 1168 A.P. Summers, T.J. Koob / Comparative Biochemistry and Physiology Part A 133 (2002) 1159–1170 al., 1978; Rowe, 1985), and concomitantly might Biewener, A.A., 1998. Muscle–tendon stresses and elastic show whether the increased stiffness of mamma- energy storage during locomotion in the horse. Comp. lian tendon relative to hagfish tendon is related to Biochem. Physiol. 120A, 73–87. Biewener, A.A., Blickhan, R., 1988. Kangaroo rat locomotion: this organization. design for elastic energy storage or acceleration? J. Exp. Perhaps the most exciting area in tendon Biol. 140, 243–255. mechanics is that of the viscoelastic properties and Biewener, A.A., Dial, K.P., Goslow, G.E., 1992. Pectoralis fatigue quality (Ker et al., 2000; Ker, 2002). With muscle force and power output during flight in the starling. only a few data from sheep and kangaroos, there J. Exp. Biol. 164, 1–18. remains a gap in our understanding of the evolu- Buchanan, C.I., Marsh, R.L., 2001. Effects of long-term exercise on the biomechanical properties of the Achilles tion of time-dependent responses to steady and tendon of guinea fowl. J. Appl. Physiol. 90, 164–171. cyclic loading. This lack of knowledge is particu- Carvalho, H.F.D., Vidal, B.D.C., 1994. Structure and histo- larly troubling given the wide range of locomotor chemistry of a pressure-bearing tendon of the frog. Ann. behaviors and novel stress regimes´ that appear in Anat. 176, 161–170. the tetrapod lineage. The evolutionary history of Carvalho, H.F.D., Vidal, B.D.C., 1995. The elastic system of fatigue quality and creep responses may be linked a pressure-bearing tendon of the bullfrog Rana catesbeiana. Ann. 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