Cursorial mammals, birds and lizards have been shown to use walking and running centre-of-mass (COM) mechanics during locomotion (Cavagna et al. 1977; Farley & Ko 1997). In walking mechanics, the COM arcs upward towards mid-step vaulting over the limbs. Kinetic energy (KE) and gravitational potential energy (PE) of the COM fluctuate out-of-phase, and energy is exchanged like an inverted pendulum. In running mechanics, the COM arcs downward during the step and KE and PE cycle together (in-phase) with their minima at mid-step. It is generally assumed that animals change from walking mechanics to running mechanics when increasing speed (Cavagna et al. 1977; Dickinson et al. 2000).

Similar COM mechanics have also been demonstrated in non-cursorial animals, such as elephants (Hutchinson et al. 2003), penguins (Griffin & Kram 2000), crocodilians (Willey et al. 2004) and frogs (Ahn et al. 2004). Their presence in frogs suggests that both mechanical energy patterns may be a primitive feature of tetrapods. Although frogs appeared about 200 million years ago, they are morphologically derived for hopping and swimming and do not represent the generalized tetrapod condition (Estes & Rieg 1973).

To test the generality of mechanical energy patterns in quadrupedal vertebrates, we studied whole-body locomotor mechanics in the most generalized surviving models for amniotes (tuataras, Sphenodon punctatus) and tetrapods (tiger salamanders, Ambystoma tigrinum). The tuatara (Sphenodontia; Wilkinson & Benton 1996) has changed little morphologically in approximately 225 million years (Apestequia & Novas 2003; Rest et al. 2003). This ‘living fossil’ has long been considered the best living model of the basic amniote morphotype (Romer 1956; Carroll 1988). The tiger salamander, A. tigrinum, represents a good living model for a generalized tetrapod: Ambystoma retain many plesiomorphic features of basal tetrapods (Carroll & Holmes 1980; Jarvik 1980) with a body plan that has remained essentially unchanged for at least 150 million years (Gao & Shubin 2001).

We studied locomotor mechanics as animals travelled over a force platform at their full range of speeds. Simultaneous kinematic (120Hz video) and whole-body three-dimensional ground reaction force data (500Hz sampling) were recorded from three tuataras (0.732–0.747kg) and six tiger salamanders (0.29–0.63kg) moving down a 3m track over an incorporated 0.5m long force platform. A sandpaper (320 grit) surface provided traction. Body temperatures were 16–18°C during data collection: tuataras were housed and run at 16–18°C; salamanders were housed at 16–18°C and moved momentarily to 19–20°C room/track temperature during runs.

Tuataras took one to two steps and salamanders approximately five steps while their whole body was over the entire force platform. Both species only used diagonal couplets footfall patterns; therefore, a ‘step’ was the time from the initial impact of one diagonal couplet until the impact of the opposite couplet. Force data from individual steps were recorded, scaled and converted into mechanical energy data as in previous research (Parchman et al. 2003). Forces were integrated to calculate COM velocities, accelerations and fluctuations in gravitational PE, KE and total mechanical energy (TME) of the COM (details in Parchman et al. 2003). KE was the sum of fore-aft, mediolateral and vertical kinetic energies of the COM. The phase shift between fluctuations in PE and KE was used to determine whether the animal was walking (180±45°) or running (0±45°) during each step (Cavagna et al. 1977; Ahn et al. 2004). Pendular effectiveness was estimated as per cent recovery of external mechanical energy following Willey et al. (2004).

Footfall patterns to quantify gaits and synchronize ground reaction forces were quantified from video recordings (downloaded with Studio DV and digitized with APAS). A camera (JVC GRL-9800) mounted above the centre of the force plate and angled mirrors on either side of the force plate allowed simultaneous filming of dorsal and lateral views (and footfall patterns). Lines at 0.12m intervals along the platform were used as the frame of reference for calculating velocity of the rostral tip of the animal. We calculated mean velocity over the entire force plate and only trials with all 0.12m interval velocities±25% of the mean platform velocity were used. Numerous trials were recorded (i) to sample the fullest range of velocities (and, therefore, mechanical patterns and gaits) that the animals would use and (ii) to maximize the number of steps at more or less constant velocity (±25%). Gaits (footfall patterns) for each step were described by plotting duty factor (percentage of the stride that the reference hindlimb was on the ground) versus limb phase (duration between footfalls of the reference hindlimb and ipsilateral forelimb, relative to stride duration) following Hildebrand (1976). All procedures followed approved animal care and use protocols.

Figure 1 Biomechanics and gaits of primitive tetrapods (a) the tiger salamander and (b) the tuatara. (i) Fluctuations in gravitational potential (PE) and kinetic energy (KE) and total mechanical energy (TME) of the COM showing out-of-phase (walking) and in-phase (more ...)

Figure 2 Evolution of walking (W) and running (R) locomotor mechanics in tetrapods. Grey bars indicate the earliest known appearance of animals considered morphologically similar to extant forms (Estes & Rieg 1973; Rest et al. 2003; Gao & Shubin (more ...)

Terrestrial locomotion has also evolved in each of the major arthropod groups. Locomotor mechanics, although limited, have been studied in Chelicerata (harvestmen, Sensenig & Shultz in press), Myriapoda (centipedes, Anderson et al. 2000), Hexapoda (cockroaches, Full & Tu 1990) and Crustacea (ghost crabs, Blickhan & Full 1987). All of these use running mechanics, but only the Crustacea use both walking and running mechanics. Arthropods have repeatedly shifted to terrestrial locomotion, but only one group appears to have evolved walking and running mechanics. Therefore, the use of both mechanical energy patterns has evolved independently in the Crustacea and Tetrapoda.

Running mechanics are also associated with energy savings via elastic energy storage in biological spring elements of the limbs and axial column when animals ‘bounce’ during running strides (Alexander 1988; Biewener 2003). However, spring savings are strongly size dependent (Biewener et al. 1981; Pollock & Shadwick 1994) and appear to be limited to larger animals (approx. above 5kg). Tendons have to be a certain size and shape relative to the loads they transmit before they can store sufficient amounts of elastic energy useful for cyclic quadrupedal locomotion (Biewener 2003). We have no evidence that spring savings are unrealized; however, tuataras and salamanders are in the size range where appreciable elastic energy recovery is not expected (Biewener 2003). Thus, although they clearly use running mechanics we are left to wonder why.

An emerging tenet of locomotor research is that legged animals change to running mechanics as they increase speed (Dickinson et al. 2000). This is true for cursorial mammals that are widely known to transition from footfall patterns (four beat gaits, singlefoot gaits) with walking mechanics, to diagonal couplets gaits with running mechanics, to the galloping gait with a combination of both mechanical patterns (Cavagna et al. 1977; Hoyt & Taylor 1981; Minetti et al. 1999; Biewener 2003). In addition, the ghost crab (Full & Tu 1990) and some lizards (McElroy & Reilly 2005) change both gaits and mechanics with speed.

In contrast, the salamanders and tuataras used only diagonal couplets gaits with both walking (mean limb phase, 42.9 and 45.8%, respectively) and running (44.0 and 44.8%, respectively) mechanics (figure 1a(iv),b(iv)) over the same narrow range of slow speeds (figure 1a(ii),b(ii)). Thus, the salamander and tuatara do not increase speed much or show the speed-related changes in gait or mechanics observed in faster animals. A narrow speed range and a lack of speed effects have also been shown for quadrupedal locomotion in frogs (Ahn et al. 2004). The natural histories of amphibians and tuataras (and by inference early tetrapods) show that these lumbering species use primarily slow locomotion. Accordingly, our data show they take advantage of pendular savings during walking, but have not adapted running mechanics for increasing speed. Therefore, the general tenet that gait and mechanics change with speed appears to be limited to cursorial animals that shift to faster speeds.

Table 1 Centre-of-mass (COM) displacements in relation to hip height in tetrapod locomotion. (Note that the lumbering species have well over an order of magnitude greater relative displacements of the COM.)

Activity temperature and metabolism may also influence the ability to increase speed. Amphibians and the tuatara have variable field activity temperatures between 10 and 26°C (Hutchison & Dupre 1992; Cartland & Grimmond 1994), whereas lizards and mammals maintain high body temperatures when active (30–41°C; Schmidt-Nielsen 1990). Thus, it appears that temperature effects (on, for example, muscle function and aerobic capacity) may partially explain the lack of speed effects in primitive tetrapods.

In salamanders, the cost of transport (Jkg⁻¹m⁻¹) is the lowest recorded among animals from insects to lizards (Gatten et al. 1992) and tuataras exhibit maximum O₂ consumption rates during activity less than half that of tiger salamanders (Bennett 1982). Low aerobic capacities are believed to be adaptations for activity at low body temperatures (Bennett 1982). However, they appear to constrain the locomotor speed and speed ranges used in these cold adapted species, and thus may limit their ability to take full advantage of energy saving mechanics. The evolution of higher activity temperature may go hand in hand with higher metabolic rate, size (thus springs), posture (thus hip height) and relative COM fluctuations (a switch to KE driven TME) in the evolution of cursoriality to provide ecologically relevant energy savings via walking and running mechanics. Clearly, a broader perspective in terms of locomotor data (reporting hip height and gaits, speed ranges), model species and data on the contributions of springs in small animals is needed to begin to understand how COM mechanics have evolved with the need for speed in tetrapods.

The support of the US National Science Foundation, the Ohio University Research Challenge Program and the Department of Herpetology of the Toledo Zoological Society is greatly appreciated.