Scaling effects on vertebrate ectotherm muscle and whole body performance

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As discussed in Section 11.2, body size has a large effect on the physiology and locomotor performance of animals; therefore, it is important to elucidate the extent to which body size accounts for interindividual differences in behavioral and underlying muscle performance. However, in many such scaling relationships, there is a large amount of scatter, suggesting that mass-independent differences in behavioral performance are also important in evolutionary physiology.

Generally, as animal size increases, skeletal muscle shortening velocity and contraction kinetics become slower, a pattern confirmed in both interspecific and interindividual studies. Interindividual studies within anuran [41,44,46], lizard [58,59], and fish [2,60] species have highlighted that as body size increases, there are usually decreases in temporal traits of muscle functions, including relative muscle shortening velocity and twitch activation and relaxation rates, i.e., muscle in smaller individuals of a species will tend to produce force quicker, shorten relatively faster, and relax quicker. In contrast, maximum isometric muscle stress and normalized power output are generally unaffected by body size [41,44,46,58,60]. Body size-dependent changes in the mechanical properties of skeletal muscle have in some cases been linked to underlying muscle structure and/or fiber type (see Section 11.4) and are paralleled by compatible alterations in locomotor performance, with smaller individuals often being relatively as fast or even faster (i.e., when speed is expressed relative to body size). Body size is likely to be a confounding factor when comparing the performance of ectothermic individuals because when analogous muscles are compared in endotherms, those from larger animals have an increased proportion of slow myosin and lower maximal shortening velocity (Vmax) within the same fiber type [61]. Indeed 78% of the interspecific variability in Vmax of muscles taken from a range of endotherms and ectotherms can be explained by variation in body size [62]. Among species of terrestrial animals (including endotherms and ectotherms), there is a significant correlation between maximal shortening velocity and maximal stress (P0) in skeletal muscle [62] with muscles that have relatively high Vmax also having, although to a lesser extent, relatively higher P0.

In general, larger individuals within fish, salamander, and lizard species are constrained to comparatively lower stride and tail-beat frequencies, thus, achieving higher absolute locomotory speeds (because of their greater body size) but lower relative (length-specific) locomotory speeds [46,58,63,64]. Also, smaller individuals have higher rates of acceleration during jumping [42,65] and swimming [66]. However, it is apparent in aquatic vertebrates that as body size increases, maneuverability decreases [63,66], with larger individuals turning more slowly and through greater angles. Therefore, larger animal species and individuals can sometimes be at a disadvantage when trying to catch smaller but more maneuverable species and individuals. Some species of large aquatic vertebrates (e.g., killer whales) have countered this problem by developing means of prey capture that maximize acceleration of part of the predator's body (e.g., tail slaps) rather than relying on whole body acceleration [66]. Body size also affects maneuverability during running in terrestrial vertebrates, which apparently affects predator prey choice and tactics used during prey capture [67].

A number of integrative studies have attempted to determine body size effects on both muscle contractile properties and locomotory performance. Muscle twitch duration has been used to predict minimum tail-beat frequency in fish, which in turn was used to calculate maximum swimming speed [2]. Larger fish had slower muscle mechanical properties that led to slower (i.e., constrained) tail-beat frequency, which in turn limited swimming speed. During sprinting in the lizard Dipsosaurus dorsalis, the decrease in stride frequency with body size was matched by an increase in twitch times in fast glycolytic muscle fibers, whereas increases in stride length were related to increased hindlimb length [59] (Figure 11.1). The slope of scaling relationships was identical in D. dorsalis for both limb cycle frequency during sprinting and optimal cycle frequency for maximal muscle power output, further supporting the notion that muscle fiber type is matched to locomotor performance in this species [68]. At lower temperatures in this lizard species, the cycle frequency for maximal muscle power matches the stride frequency used [69], i.e., the muscle in smaller individuals tends to cycle at a faster rate (frequency) with faster activation, shortening, and relaxation rates tending to enable higher stride frequencies by minimizing the ground contact time [70,71]. The higher stride frequencies in smaller individuals are vital to enable them to achieve the same, or similar, sprint velocity as larger individuals of the same species [59]. In contrast, larger individuals within a species have slower, more economical muscle fibers optimized to work at lower limb cycle frequency during sprinting, yet still achieve the same sprint speed because of their longer limb length (but see Ref. [70] for a full discussion on lower stride frequency in larger lizards).

Optimal cycle frequency for maximal muscle work loop-power output decreases with increasing body size [44,58,72]. Altringham and co-workers [44] have shown that interindividual variation in the optimal cycle frequency for work loop-power output in Xenopus muscle fiber bundles is more dependent on body size in slower muscle fibers (from adductor magnus) than in faster muscle fibers (from sartorius), with scaling exponents of Mb0-23 and Mb007, respectively. It has been argued that in faster muscles and muscle fiber bundles, contractile speed decreases less dramatically with body size as animals attempt to maximize speed and power available for escape responses [44]. In contrast, in slower muscle and muscle fibers, rapid muscle shortening velocity or deactivation rate is not as crucial to organismal performance; therefore, large energetic savings can be made by decreasing these variables, hence, the relatively high scaling exponent [71].

Despite the general patterns of body size-related changes in locomotory performance, the effect of body size can vary between species. Within some species of

FIGURE 11.1 (A) Stride length, (B) stride frequency, and (C) running velocity as functions of body mass during sprint runs with a body temperature of 35°C in the lizard Dipsosaurus dorsalis. Data are plotted on log-log coordinates. Solid lines represent regression lines. (From Marsh, R.L., J. Exp. Biol., 137, 119, 1988, with permission.)

FIGURE 11.1 (A) Stride length, (B) stride frequency, and (C) running velocity as functions of body mass during sprint runs with a body temperature of 35°C in the lizard Dipsosaurus dorsalis. Data are plotted on log-log coordinates. Solid lines represent regression lines. (From Marsh, R.L., J. Exp. Biol., 137, 119, 1988, with permission.)

Anolis lizard, maximum acceleration and distance achieved during jumping increased with hindlimb length, yet within other species the relationship between performance and hindlimb length was negative [73].

11.4 relationships between muscle specialization and the individual behavioral performance of vertebrate ectotherms

As mentioned in the introduction to the present chapter, within the context of vertebrate ectotherms, sprint speed has been more frequently studied and seems of particular ecological relevance in lizards and fish. Speed during burst running and swimming is dependent on stride length and stride frequency. Stride length in lizards is dependent on limb length and gait whereas stride frequency is dependent on skeletal muscle having rapid activation, high shortening velocity, and fast relaxation. It has been demonstrated that Lacertid species living in more open environments tend to have longer limbs and actually modulate their sprint speed by altering their stride length, and consequently the range of motion of their muscles [74]. In contrast, those species that live in more closed environments (where more vegetation is present to restrict locomotion) have shorter limbs and alter their speed by changing their stride frequency (therefore, altering muscle cycle frequency) [74].

The relationship between sprint speed and muscle activation rate, relaxation rate, and shortening velocity suggests a connection between individual differences in performance and muscle molecular traits. This is because any muscle with rapid activation and relaxation must rely on rapid release and reuptake of calcium, respectively. Rapid relaxation is correlated with greater parvalbumin content in skeletal muscle [75] but comes at a high energetic cost because it requires rapid calcium pumping and fast cycling cross-bridges, two processes that require ATP consumption [76]. Rapid activation and relaxation can also require an increased proportion of the muscle to be devoted to the sarcoplasmic reticulum (SR) t-tubule system to decrease diffusion distances between this system and the thin filaments [77]. Therefore, any muscle that cycles at very high frequencies has a disproportionately large volume of SR. Increased SR volume leads to a proportional decrease in the space available for the contractile filaments, causing muscles that cycle at very high frequency, such as rattlesnake tailshaker and toadfish swimbladder muscles, to produce relatively low force per unit cross-sectional area [76,77]. Higher levels of SR calcium ATPase activity and SR calcium uptake (i.e., two other SR indicators of contractile speed) in sprint-trained horses have been linked with improved sprint performance [78]. Therefore, as has previously been suggested for lizards running at suboptimal temperatures [69], the rate of muscle activation and relaxation can limit sprint performance, because muscles used during sprinting need high power output. Given that both muscle power production and activation and relaxation rates can in some cases affect sprint speed, and that morphological tradeoffs might constrain the maximization of both (see Section 11.5), it is possible that various muscle configurations might, for different reasons, lead to similar sprint speeds among individuals.

Maximal shortening velocity (Vmax) of muscle within a species is primarily dependent on the myosin heavy chain isoforms expressed within the muscle, with significant differences in Vmax existing between fiber types [79]. Other sources of variation in the maximum shortening velocity of muscle may include variation in myosin light chains, troponin, tropomyosin, and various calcium regulatory proteins

[80,81]. In Xenopus laevis, maximal stress, maximal shortening velocity, and maximal power output vary in the same manner between muscle fiber types decreasing from type 1 to type 2 to type 3 to type 4 to tonic [79]. Higher muscle force in both ectotherms and endotherms is thought to be primarily due to relatively higher myofibrillar volume [77].

Muscle architecture can be varied to match the task performed. Evidence from human limb muscles suggests that muscles with a higher pennation angle should produce relatively higher forces (because of a larger physiological cross-sectional area) and may produce greater force at any muscle-shortening velocity (because of lower fiber-shortening velocity) when compared with more parallel fibered muscles [82]. However, muscles that are less pennate are better suited to larger length changes, with the result that antigravity extensor muscles are more pennate and flexor muscles are more parallel fibered. It is possible that interindividual variability in muscle architecture may occur leading to changes in muscle size, muscle pennation, and the position of the origin and insertion of muscles such as have been found between species. For example, projectile theory suggests that jumping performance could be altered by changing: (1) hindlimb length to affect the distance or time period over which the propulsive force acts; (2) hindlimb jumping muscle size to alter the power available for propulsion; and (3) moving the position of the origins or insertions of the jumping muscles to alter the angular velocity of the limbs [83]. Within a given clade, jumping specialists usually have longer hindlimbs [40,43,65,84] and more enlarged hindlimb musculature, across or within species [65], or across species [40]. One notable example of muscle specialization is evidenced in the longissimus dorsi muscle of amphisbaenians, which provides the high forces required for digging. In the amphisbaenid species Leposternon microcephalum, this muscle is highly pennate (to increase the physiological cross-sectional area and hence force) and overall has fast moderately oxidative muscle fibers. Subtle biochemical changes along the longitudinal axes suggest higher glycolytic capacity in the distal fibers that seems specialized to match the function of this section of the muscle and perhaps enhance force toward the end of the digging strokes, when greater forces are required [85].

Skeletal muscle can perform many different tasks during animal behavior, acting to rapidly produce high power output, produce power efficiently over long periods, produce high force for long periods, produce force isometrically to stabilize a limb, transmit force, or absorb power to act as a brake [86]. Essentially the mechanical properties of muscle are determined by their composition, which in turn reflects tradeoffs between the differing tasks performed by the muscle [77]. In mammalian muscles, the fiber type of a muscle has been correlated to its daily activity patterns [87].

In many animals, including fish, frogs, and lizards, different muscles may contain different proportions of fiber type, and within muscles, fiber types are separated into distinct regions. The mechanical properties of the different muscles and fiber types and the proportions of different fiber types within muscles match the force and power output required by their different functions [79,88,89]. For example, in Rana pipiens, the hindlimb muscles primarily used to power jumping (89%) consist of the fastest, most powerful, type-1 muscle fibers, which should maximize burst jumping performance to enable rapid escape from predators [90].

In contrast, hindlimb muscles not used to power jumping are composed of far fewer (29%) type-1 muscle fibers.

Skeletal muscle is also involved in sound production, which is a highly specialized activity. The trunk muscles that support calling in males of many species of frog and some other vertebrate ectotherms are highly aerobic and cycle continuously over many hours a day during the mating season [13]. This behavior relates to the mating success of males, which in many species is highly dependent on energetically demanding vocal displays involved in female attraction and male-to-male interactions [51]. Males able to produce the most energetic calls are often more attractive to females [91]. The structure of trunk muscles reflects both the aerobic nature and high cycle frequency requirements of the behavior they support, including 100% fast oxidative glycolytic fibers [92], high citrate synthase activity [93], and high densities of mitochondria and capillaries [94]. Differences in calling rate between species have been linked to differences in mechanical properties of calling muscles [92].

The amplexus behavior of male anurans requires the forearms of the male to be maintained in a relatively fixed position for long periods to hold the female during breeding. The forearm muscles involved in this behavior can produce high, sustained isometric force (Navas and James, unpublished results) [9]. These sustained forces can even be maintained via only short periods of electrical activation because of very slow muscle relaxation rates. These mechanical requirements are only needed by the males, and indeed, there is marked sexual dimorphism as evidenced by muscular hypertrophy [9] and increased proportion of tonic fibers in males [95]. Reproductively successful toads in the species Bufo marinus (those found in amplexus) had significantly larger forelimb muscle mass (when corrected for body size) than those calling males not found in amplexus [96]. Therefore, these muscles seem well adapted and vital for their role in producing high forces to successfully grip the female during amplexus but would, for instance, be of limited use during cyclic locomotion due to the prolonged relaxation times.

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