Why are mammalian tendons so thick?

The maximum stresses to which a wide range of mammalian limb tendons could be subjected in life were estimated by considering the relative cross-sectional areas of each tendon and of the fibres of its muscle. These cross-sectional areas were derived from mass and length measurements on tendons and muscles assuming published values for the respective densities. The majority of the stresses are low. The distribution has a broad peak with maximum frequency at a stress of about 13 MPa, whereas the fracture stress for tendon in tension is about 100 MPa. Thus, the majority of tendons are far thicker than is necessary for adequate strength. Much higher stresses are found among those tendons which act as springs to store energy during locomotion. The acceptability of low safety factors in these tendons has been explained previously (Alexander, 1981). A new theory explains the thickness of the majority of tendons. The muscle with its tendon is considered as a combined system which delivers mechanical energy: the thickness of the tendon is optimized by minimizing the combined mass. A thinner tendon would stretch more. To take up this stretch, the muscle would require longer muscle fibres, which would increase the combined mass. The predicted maximum stress in a tendon of optimum thickness is about 10 MPa, which is within the main peak of the observed stress distribution. Individual variations from this value are to be expected and can be understood in terms of the functions of the various muscles.     

Rest length and compliance of non-immobilised and immobilised rabbit soleus muscle and tendon

The first aim of this study was to measure the contributions of muscle and tendon to the total compliance of resting muscle-tendon units. A second aim was to determine whether the decrease in muscle-tendon unit rest length produced by prolonged immobilisation in a shortened position is mediated primarily by adaptations of the muscle or tendon. One ankle joint from each of five rabbits was immobilised in a plantarflexed position for 14 days. The passive length-tension properties of soleus muscle fascicles and tendons from both hindlimbs were measured using a video-based tensile-testing system. In non-immobilised muscles, muscle fascicle strains exceeded tendon strains by up to four times. However, because the rest length of tendon was much greater than that of muscle fascicles, changes in tendon length accounted for nearly half of the total change in muscle-tendon unit length. The rest length of immobilised muscle-tendon units was less than that of non-immobilised muscle-tendon units from contralateral limbs. Most of this difference was attributable to a change in the rest length of the tendon; there was little change in the rest length of muscle fascicles. It is concluded that the tendon is responsible for a large part of the compliance of rabbit soleus muscle-tendon units at physiological resting tensions, and that adaptation of tendon rest length is the primary mechanism by which the rabbit soleus shortens in response to immobilisation at short lengths. Accepted: 7 May 1997     

The evolution of hindlimb tendons and muscles on the line to crown-group birds

The anatomy and functions of muscle-tendon complexes and their bony attachments in birds and their outgroups show how the major pelvic limb muscle groups evolved. Fossils reveal that most changes evolved after the divergence of archosaurs in the Triassic, particularly in the dinosaurian precursors to birds. Three-dimensional limb control became concentrated at the hip joint; more distal joints and muscles were restricted to flexion or extension early in dinosaur evolution. Hip extensors expanded even though the primary femoral retractor M. caudofemoralis longus was reduced. Hip flexors and two-joint "hamstring" muscles were simplified to a few large heads. Knee extensors increased their sizes and moment arms early in bipedal dinosaurs, but the patella and cranial cnemial crest evolved later in birds. Lower limb muscles expanded as ossifications such as the hypotarsus increased their moment arms. The ossification of lower limb tendons, particularly in extensors, is a recent novelty of birds. Muscles and tendons that develop large forces, stresses, and moments to stabilize or move the limbs became increasingly prominent on the line to birds. Locomotion evolved in a stepwise pattern that only recently produced the derived limb control mechanisms of crown-group birds, such as the strongly flexed hip and knee joints.     

Allometry of the leg muscles of birds

The musculoskeletal components of the hindlimbs of 20 species of birds, considered non-runners, were examined. Allometry was used to compare these data with previously published information on the limbs of running birds. In non-runners the digital flexor muscle and tendon areas scaled approximately isometrically, in contrast to running birds where tendon areas had a lower exponent. Non-running birds had muscle fibre areas approximately half that of runners of equal mass. In both groups, the muscle:tendon area ratio for m. gastrocnemius increased as M^0.13, suggesting factors other than elastic energy storage are important. Runners exhibited relatively longer tibiotarsi and tarsometatarsi and shorter toes. With very few exceptions, the linear dimensions of bones, tendon cross-sectional areas, and muscle masses and fibre areas in the legs of the non-running birds scaled closely according to the requirements for geometric similarity, but the confidence limits are often wide. Deviations from geometric similarity in birds reflect differences in locomotor behaviours and abilities.     

Ethnic differences in triceps surae muscle-tendon complex and walking economy

The purposes of this study were to (a) determine whether structural differences in triceps surae muscle-tendon complex and walking economy exist between 14 African American and 19 Caucasian sedentary women and (b) determine whether muscle-tendon parameters are associated with walking economy. African American and Caucasian subjects were matched on body weight, height, and body composition. Muscle-tendon parameters were determined by magnetic resonance imaging and walking economy was evaluated at 4.8 km.h(-1). Medial gastrocnemius and total triceps surae muscle shape were different across ethnicity despite no ethnic differences in plantar flexion strength or in maximal cross-sectional area for any triceps surae muscles. African American women had shorter gastrocnemius muscles and longer tendons and performed walking more economically. Tendon length was the only variable related to walking economy. No ethnic differences were observed in walking economy after adjusting for tendon length. Data show gastrocnemius tendon length is related to level walking and longer gastrocnemius tendons may partly explain more economical walking in African American women. These preliminary findings indicate the structure of the muscle-tendon complex could be a factor partially accounting for reported ethnic differences in certain types of athletic-related performance.     

Mechanical properties of collagen fascicles from the rabbit patellar tendon

Tensile and viscoelastic properties of collagen fascicles of approximately 300 microns in diameter, which were obtained from rabbit patellar tendons, were studied using a newly designed micro-tensile tester. Their cross-sectional areas were determined with a video dimension analyzer combined with a CCD camera and a low magnification microscope. There were no statistically significant differences in tensile properties among the fascicles obtained from six medial-to-lateral locations of the patellar tendon. Tangent modulus, tensile strength, and strain at failure of the fascicles determined at about 1.5 percent/s strain rate were 216 +/- 68 MPa, 17.2 +/- 4.1 MPa, and 10.9 +/- 1.6 percent (mean +/- S.D.), respectively. These properties were much different from those of bulk patellar tendons; for example, the tensile strength and strain at failure of these fascicles were 42 percent and 179 percent of those of bulk tendons, respectively. Tangent modulus and tensile strength of collagen fascicles determined at 1 percent/s strain rate were 35 percent larger than those at 0.01 percent/s. The strain at failure was independent of strain rate. Relaxation tests showed that the reduction of stress was approximately 25 percent at 300 seconds. These stress relaxation behavior and strain rate effects of collagen fascicles differed greatly from those of bulk tendons. The differences in tensile and viscoelastic properties between fascicles and bulk tendons may be attributable to ground substances, mechanical interaction between fascicles, and the difference of crimp structure of collagen fibrils.     

The variation of the cross-sectional shape in the long bones of birds and mammals

The transverse and sagittal diameters of the long bones were measured in a sample of 53 species of eutherian mammals and 36 species of birds. The scaling of the transverse and sagittal diameters of each bone to body mass was calculated. For each bone the ratio of sagittal/transverse diameter was calculated, as an expression of the cross-sectional shape of the bones. The distributions of the ratios were not significantly different from normality in all the avian bones and in the mammalian femur and tibia. In most cases, the mean of the distribution was significantly different from 1 (circular shape). The analysis shows that changes in the ratio can be caused by selective factors, considering the correlation predicted between the breaking moments and the radii, but at the same time the cross-sectional shape of mammalian and avian long bones may have a phylogenetic basis. Finally, the previous assumption of relationship between bone curvature and stress predictability, is also discussed.     

The legs of ostriches (Struthio) and moas (Pachyornis)

Ostriches were filmed running at maximum speed, and forces on the feet were calculated. Measurements were made of the principal structures in the legs of an ostrich. Hence peak stresses in muscles, tendons and bones were calculated. They lay within the range of stresses calculated for strenuous activities of other vertebrates. The ostrich makes substantial savings of energy in running, by elastic storage in stretched tendons. Pachyornis was a flightless bird, much heavier than ostriches and with massively thick leg bones. These bones are shorter than predicted for its estimated body mass, by extrapolation from allometric equations for flying birds. An attempt is made to calculate the stresses that acted in the leg bones in running, for all possible patterns of leg movement. The stresses were probably rather low, unless Pachyornis was capable of running fast. It is argued that the optimum factor of safety for moo leg bones may have been exceptionally high, as a consequence of the absence of predators.     

The force-length relationship of a muscle-tendon complex: experimental results and model calculations

Models are useful when studying how architectural and physiological properties of muscle-tendon complexes are related to function, because they allow for the simulation of the behaviour of such complexes during natural movements. In the construction of these models, evaluation of their accuracy is an important step. In the present study, a model was constructed to calculate the isometric force-length relationship of the rat extensor digitorum longus muscle-tendon complex. The model is based on the assumption that a muscle-tendon complex is a collection of independent units, each consisting of a muscle fibre in series with a tendon fibre. By intention, values for model parameters were derived indirectly, using only the measured maximal isometric tetanic force, the distance between origin and insertion at which it occurred (optimum lOI) and an estimate of muscle fibre optimal length. The accuracy of the calculated force-length relationship was subsequently evaluated by comparing it to the relationship measured in isometric tetanic contractions of a real complex in the rat. When the length of distal muscle fibres, measured during isometric contraction at optimal lOI of the whole complex, was used as an estimate for muscle fibre optimal length of all muscle fibre-tendon fibre units in the model, the calculated relationship was too narrow. That is, both on the ascending limb and on the descending limb the calculated tetanic force was lower than the measured tetanic force.(ABSTRACT TRUNCATED AT 250 WORDS)     

The effects of a calcium deficient diet on the mechanical properties and morphology of goose bone

A control group of geese (Anser anser) on a normal calcium diet for egg laying poultry was compared to egg laying geese on a calcium deficient diet. The ultimate compressive strength and modulus of elasticity of femoral cortical bone from each group were determined by compressing right circular cylinders which were 2.4 mm in height and 0.8 mm in diameter. The bending strength and bending modulus of elasticity of tibial cortical bone were determined by three point bend tests on rectangular prisms which were approximately 25 mm by 0.8 mm by 0.8 mm. Bone calcium content and eggshell calcium content were determined by atomic absorption spectrophotometry. Blood samples were analyzed for free calcium ion concentration. Histological observations included studies of cross-sectional microradiographs, examinations of cross sections stained by a modified Masson's technique, and a determination of fractional area of voids by quantitative microscopy. The average compressive modulus for the control birds was 12.0 GPa (S.D.: 6.2 GPa) while the ultimate compressive strength was 165 MPa (S.D.: 27 MPa). Calcium deprived birds showed slight, but not statistically significant, decreases in both the compressive modulus and compressive strength. The tibial three point bending modulus for the control birds was 16.5 GPa (S.D.: 2.6 GPa) while the ultimate bending strength was 256 MPa (S.D.: 58 MPa). Once again, slight though not statistically significant decreases in the bending modulus and strength were seen in the geese on the calcium deficient diet. The average calcium content (wt%) of the femora of the control birds was 20.5% (S.D.: 4.3%) and 20.6% (S.D.: 4.8%) for the tibiae. No significant differences were noted in the calcium deprived birds. The average fractional void area for the control bird femoral bone was 12.0% (S.D.: 2.6%) and 9.8% (S.D.: 1.8%) for the tibial bone. Significantly greater fractional void areas were noted in the calcium deficient birds as were profound changes in the macrocellular structure of these bones.     

Conservation planning and viability: problems associated with identifying priority sites in Swaziland using species list data

Conservation planning assessments based on species atlas data are known to select planning units containing ecotones because these areas are relatively species‐rich. However, this richness is often dependent on the presence of adjoining core habitat, so populations within these ecotones might not be viable. This suggests that atlas data may also fail to distinguish between planning units that are highly transformed by agriculture or urbanization with those from neighbouring untransformed units. These highly transformed units could also be identified as priority sites, based solely on the presence of species that require adjoining habitat patches to persist. This potential problem was investigated using bird and mammal atlas data from Swaziland and a landcover map and found that: (i) there was no correlation between planning unit species richness and proportion of natural landcover for both taxa; (ii) the priority areas that were identified for both birds and mammals were no less transformed than if the units had been chosen at random and (iii) an approach that aimed to meet conservation targets and minimize transformation levels failed to identify more viable priority areas. This third result probably arose because 4.8% of the bird species and 22% of the mammal species were recorded in only one planning unit, reducing the opportunity to choose between units when aiming to represent each species. Therefore, it is suggested that using species lists to design protected area networks at a fine spatial scale may not conserve species effectively unless population viability data are explicitly included in the analysis.     

Increased Serum and Musculotendinous Fibrogenic Proteins following Persistent Low-Grade Inflammation in a Rat Model of Long-Term Upper Extremity Overuse

We examined the relationship between grip strength declines and muscle-tendon responses induced by long-term performance of a high-repetition, low-force (HRLF) reaching task in rats. We hypothesized that grip strength declines would correlate with inflammation, fibrosis and degradation in flexor digitorum muscles and tendons. Grip strength declined after training, and further in weeks 18 and 24, in reach limbs of HRLF rats. Flexor digitorum tissues of reach limbs showed low-grade increases in inflammatory cytokines: IL-1β after training and in week 18, IL-1α in week 18, TNF-α and IL-6 after training and in week 24, and IL-10 in week 24, with greater increases in tendons than muscles. Similar cytokine increases were detected in serum with HRLF: IL-1α and IL-10 in week 18, and TNF-α and IL-6 in week 24. Grip strength correlated inversely with IL-6 in muscles, tendons and serum, and TNF-α in muscles and serum. Four fibrogenic proteins, TGFB1, CTGF, PDGFab and PDGFbb, and hydroxyproline, a marker of collagen synthesis, increased in serum in HRLF weeks 18 or 24, concomitant with epitendon thickening, increased muscle and tendon TGFB1 and CTGF. A collagenolytic gelatinase, MMP2, increased by week 18 in serum, tendons and muscles of HRLF rats. Grip strength correlated inversely with TGFB1 in muscles, tendons and serum; with CTGF-immunoreactive fibroblasts in tendons; and with MMP2 in tendons and serum. Thus, motor declines correlated with low-grade systemic and musculotendinous inflammation throughout task performance, and increased fibrogenic and degradative proteins with prolonged task performance. Serum TNF-α, IL-6, TGFB1, CTGF and MMP2 may serve as serum biomarkers of work-related musculoskeletal disorders, although further studies in humans are needed.     

Biomechanical studies of the rabbit patellar tendon after removal of its one-fourth or a half.

Effects of the overstressing induced by the harvest of grafts from the patellar tendon on the mechanical properties and morphometry of remaining tendon were studied using a rabbit model. The width of the patellar tendon was reduced by one-fourth or one-half equally removing the medial and lateral portions; by this surgery, the cross-sectional area was decreased by 25 or 50 percent from the original area. After all the rabbits were allowed unrestricted activities in cages for 3 to 12 weeks, their patellar tendons were harvested for mechanical and histological studies. The one-fourth removal induced no significant changes in the mechanical properties, but significantly increased the cross-sectional area. In the case of one-half removal, tensile strength and tangent modulus did not change in some tendons, although the cross-sectional area increased significantly. In the other central half tendons, mechanical strength decreased markedly, while the cross-sectional area increased; hypercellular areas and breakage of collagen bundles were observed in these tendons. These results indicate that the patellar tendon has an ability of functionally adapting to overstressing by changing the cross-sectional area, while keeping the mechanical properties unchanged, if the extent of overstressing is less than 30 percent.     

Development and validation of ultrasound speckle tracking to quantify tendon displacement

Ultrasound can be used to study tendon movement. However, measurement of tendon movement is mostly based on manual tracking of anatomical landmarks such as the musculo-tendinous junction, limiting the applicability to a small number of muscle-tendon units. The aim of this study was to quantify tendon displacement without anatomical landmarks using a speckle tracking algorithm optimized for tendons in long B-mode image sequences. A dedicated two-dimensional multi-kernel block-matching scheme with subpixel motion estimation was devised to handle large displacements over long sequences. The accuracy of the tracking on porcine tendons was evaluated during different displacements and velocities. Subsequently, the accuracy of tracking the flexor digitorum superficialis (FDS) of a human cadaver hand was evaluated. Finally, the in-vivo accuracy of the tendon tracking was determined by measuring the movement of the FDS at the wrist level. For the porcine experiment and the human cadaver arm experiment tracking errors were, on average, 0.08 and 0.05 mm, respectively (1.3% and 1.0%). For the in-vivo experiment the tracking error was, on average, 0.3 mm (1.6%). This study demonstrated that our dedicated speckle tracking can quantify tendon displacement at different physiological velocities without anatomical landmarks with high accuracy. The technique allows tracking over large displacements and in a wider range of tendons than by using anatomical landmarks.     

Viscous elements have little impact on measured passive length-tension properties of human gastrocnemius muscle-tendon units in vivo

Several studies have measured the elastic properties of a single human muscle-tendon unit in vivo. However the viscoelastic behavior of single human muscles has not been characterized. In this study, we adapted QLV theory to model the viscoelastic behavior of human gastrocnemius muscle-tendon units in vivo. We also determined the influence of viscoelasticity on passive length-tension properties of human gastrocnemius muscle-tendon units. Eight subjects participated in the experiment, which consisted of two parts. First, the stress relaxation response of human gastrocnemius muscle-tendon units was determined at a range of knee and ankle angles. Subsequently, passive ankle torque and ankle angle were collected during cyclic dorsiflexion and plantarflexion at a range of knee angles. Viscous parameters were determined by fitting the stress relaxation experiment data with a two-term exponential function, and elastic parameters were estimated by fitting the QLV model and viscous parameters to the cyclic experiment data. The model fitted the experimental data well at slow speeds (RMSE: 1.7 ± 0.5N) and at fast speeds (RMSE: 1.9 ± 0.2N). Muscle-tendon units demonstrated a large amount of stress relaxation. Nonetheless, viscoelastic passive length-tension curves estimated with the QLV model were similar to elastic passive length-tension curves obtained using a model that ignored viscosity. There was little difference in the elastic passive length-tension curves at different loading rates. We conclude that (a) the QLV model can be used to quantify viscoelastic behaviors of relaxed human gastrocnemius muscle-tendon units in vivo, and (b) over the range of velocities we examined, the velocity of loading has little effect on the passive length-tension properties of human gastrocnemius muscle-tendon units.     

PRIZES FOR ESSAYS

Mendelsohn, J. M., Kemp, A. C, Biggs, H. C, Biggs, R. &; Brown, C.J. 1989. Wing areas, wing loadings and wing spans of 66 species of African raptors. Ostrich 60:35-42.

The paper provides data on the wing areas of 855 birds of 66 species and wing spans of 918 individuals of 58 species of African raptors. Two measures of wing loading were calculated for those individuals that were weighed. Wing, secondary and ulnar lengths are used to derive an index of wing area which explains 98,8% of the variation in the mean wing areas of 46 species. A regression, derived from this relationship, can be used to estimate wing areas from the three linear measurements, all of which can be taken on museum specimens. Similarly, an index, using the sum of wing and ulnar lengths accounts for 99,5% of the variation in the mean wing spans of 36 species. The wing dimensions of males and females, and adults and juveniles are compared in several species. For those species with adequate samples of measurements of wing area, body mass and wing span, the cost of flapping flight can be estimated with confidence.     

On the use by birds of intertidal areas of the Tagus estuary: implications for management

The use of intertidal areas of the Tagus estuary by birds was re-analysed, based on data from 1990 to 1993, to describe (i) the temporal and spatial patterns of use of intertidal areas, (ii) the diet of birds during winter and (iii) the habitat selection patterns of feeding birds, during winter. The most common birds in the estuary were gulls, waders and ducks. Highest densities were recorded for most species in autumn and winter. The spatial distribution of birds in the intertidal areas of the estuary did not vary significantly across seasons, although broader distributions occurred when bird populations were present in high numbers. In autumn, use of intertidal areas was highly variable. Specific areas in the estuary were identified as holding important densities of birds, or having a high species richness. The most abundant species selected feeding areas according to sediment type, although the presence of channels, saltmarsh or humans also influenced the distribution of birds. The invertebrates Carcinus maenas, Hediste diversicolor and Scrobicularia plana were identified as key prey species. Plant material was important as food for ducks. Implications of these findings for the management of the estuary are discussed.     

Nestedness in fragmented landscapes: birds of the box‐ironbark forests of south‐eastern Australia

Nestedness in biota as a function of species richness – biota of depauperate assemblages being non‐random subsets of richer biotas – has been widely documented in recent years (see Wright et al. 1998 , Oecologia 113: 1–20). Ordering sites by richness maximizes nestedness indices; however, ordering by other criteria such as area or isolation may be more ecologically interpretable. We surveyed birds in true fragments (35 in all), and in “reference areas” in large extant forest blocks (30 locations), of the same range of areas (10, 20, 40, 80 ha). The avifauna was divided into “bush birds”– species dependent on forest and woodland, and “open country” species. We looked at nestedness in four data sets: “bush birds” in fragments and reference areas, and “all birds” in fragments and in reference areas. All data sets were significantly nested. Ordering by area in all cases was not significantly less nested than ordering by richness. Ordering by area in fragments was significantly greater than in reference areas, but the differences in standardized nestedness indices were small (<15%). We identified those birds that had distributions among fragments that conformed strongly with area, those that were more randomly distributed and some species that were more likely to occupy the smallest fragments. Among the latter was a hyperaggressive, invasive, colonial native species (noisy miner Manorina melanocephala). A suite of small, insectivorous birds were more likely to strongly conform with expected distributions in relation to area, which was consistent with observations of their vulnerability to the effects of the noisy miner in smaller fragments.     

Body size, locomotion, and long bone cross-sectional geometry in indriid primates.

The geometry of the midshaft cross-sections of the femur and humerus of five indriid species was analysed. Internal (marrow cavity) and external diameters were measured on X-rays in the anteroposterior (a-p) and mediolateral (m-l) planes; cross-sectional areas, second moments of area, and section moduli were calculated using formulae for a hollow ellipse. Cortical thickness, robusticity indices (relating external diameters to the length of the bones), and a-p/m-l shape variables were also calculated. Model II regression was supplemented by analyses of correlation between size and shape. Indriids are saltatory, i.e., their locomotion is dominated by the hind limbs. Accordingly, the femur is more rigid than the humerus, and it shows a consistent difference between the a-p and m-l planes in measures related to bending strength. Cortical thickness varies considerably both within and across species. The type specimen of the new species Propithecus tattersalli is virtually indistinguishable from P. verreauxi on the basis of its long bone cross-sectional geometry. Femoral robusticity is uncorrelated with size, but humeral robusticity decreases significantly with increasing size. Femoral shape variables (a-p/m-l) are all negatively correlated with body size, indicating that m-l dimensions of the femur increase at a faster rate than do a-p dimensions. The highly loaded plane of movement seems to be more reinforced in the smaller species. Contrary to static biomechanical scaling predictions of positive allometry, all cross-sectional parameters scale relatively close to isometry. It is concluded that either changes in locomotor performance must compensate for the weight-related increase in forces and moments or that the larger-bodied animals operate appreciably closer to the limits of their safety margins.     

Sagittal long bone curvature in birds

The maximum sagittal curvature of the long bones (humeras, radius, ulna, femur, tibiotarsus and tarsometatarsus) of 45 specimens of birds, belonging to 36 species, was measured and regressed to the corresponding body mass. Mathematical results show a tendency of curvature to scale with strong positive allometry. Within the species studied, those with more characteristic flapping flight tend to show relatively low values of curvature in the wing bones. To check the agreement of the present results with current hypotheses on the origin of long bone curvature, previous results on scaling of myological and cross-sectional parameters in birds are considered. Indirect evidence suggests that curvature tends to increase bone stresses. Hypotheses that consider curvature as a consequence of the mechanical action of muscle allocation and optimization of functional strains are discussed at length. The possible double genetic-epigenetic determinism of the curvature character is evoked.