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The Energetic Cost of Limbless Locomotion Reprint Series 3 August 1990, Volume 249, pp. 524-527 The Energetic Cost of Limbless Locomotion MICHAELWALTON, BRUCE C. JAYNE, AND ALBERTF. BENNETT Copyright 63 1990 by the American Association for the Advancement of Science The Energetic Cost of Limbless Locomotion The net energetic cost of terrestrial locomotion by the snake Coluber constrictor, moving by lateral undulation, is equivalent to the net energetic cost of running by limbed animals (arthropods, lizards, birds, and mammals) of similar size. In contrast to lateral undulation and limbed locomotion, concertina locomotion by Coluber is more energet- ically expensive. The findings donot support the widely held notion that the energetic cost of terrestrial locomotion by limbless animals is less than that of limbed animals. PECIES WITH REDUCED LIMBS OR NO contact with the ground (4, 12). In narrow limbs and elongate bodies have passageways such as tunnels, snakes often Sevolved independently from limbed perform concertina locomotion exclusively antecedents in several groups of vertebrates: (4). Snakes performing concertina locomo- salamanders, caecilians, amphisbaenians, liz- tion stop periodically, and certain parts of ards, and snakes (1). An important factor the body are moved forward while others proposed to explain the evolution of limb- maintain static contact with the ground. In lessness is its presumptively low energetic passageways, snakes alternately press them- cost, such that energetic expenditure during selves against the sides by forming a series of locomotion by limbless animals is expected bends and then extend themselves forward to be less than that of limbed animals of from the region of static contact (4, 13). In similar size (1,2). Biomechanical arguments comparison to lateral undulation, concertina advanced in support of the low energetic locomotion involves higher momentum cost of limbless locomotion include no costs changes (4), resistance due to static (as well associated with vertical displacement of the as sliding) friction (4), and usually slower center of gravity (1, 3, 4), no costs to forward speed (11) and, therefore, probably accelerate or decelerate limbs (3), and low entails higher energetic costs. cost for support of the body (I). A prelimi- Although these considerations logically nary study, published only as an abstract, suggest differential costs of the two locorno- reported that the energetic cost of locomo- tor modes, only if we directly determine the tion of the garter snake (Thamnophis sirtalis) metabolic rates of moving animals can these was only 30% of that predicted for a qua- be verified and compared to anticipated drupedal lizard of similar size (5). Although values for limbed animals. In the current that study was preliminary, it has been wide- study, we measured energy expenditure as ly cited in review articles (1-3, 6, 7) and the rate of oxygen consumption of snakes at textbooks (4, 8) in support of mechanical rest (~02rest), in the moments just before arguments for the low cost of limbless loco- locomotory exercise ( i/Oz ,e.,,), and dur- motion. We sought to test the generality of ing locomotion at several speeds (0.2 to 1.0 these conclusions by examining the energet- km hour-' for lateral undulation, 0.06 to ic cost of locomotion in a snake, the black 0.14 km hour-' for concertina locomotion) racer (Coluber constrictor) . on motorized treadmills (14, 15). Endur- A snake may utilize a variety of locomo- ance, measured as time sustained on tread, tor modes, depending on both speed and as a function of speed and locomotor mode surface encountered (4, 9-1 1). Lateral undu- was also determined (16). Videotapes were lation and concertina locomotion are two used to verify locomotor mode and to corre- common modes that use lateral vertebral late frequency of movement with energy movements to generate propulsive forces. expenditure. By dividing oxygen consump- During lateral undulation on the ground, tion by frequency of movement, we estimat- snakes move along an approximately sinu- ed energetic costs of single cycles of lateral soidal trajectory. Bends in the body contact undulatory and concertina movement. with the substrate and push posteriorly on The metabolic response of VO~to speed projections from the ground, propelling the in Coluber constrictor [mass = 102.8 ) 6.1 body forward. All parts of the body move (SE) g, n = 71 locomoting by lateral undu- simultaneously with the same overall speed, lation is similar to that observed in many while forward and lateral components of terrestrial vertebrates with limbs (17): ~02 velocity change as a result of the sinusoidal increases as a linear function of speed (18) trajectory (10, 11). Snakes moving with throughout the range of sustainable speeds lateral undulation experience only sliding (0.2 to 0.5 km hour-'), above which Vo2is constant and endurance decreases (speeds Deparnnent of Ecology and Evolutionary Biology, Uni- greater than 0.5 km hour-') (Fig. 1, A and versity of California, Irvine, CA 92717. B). Oxygen consumption also increased as a SCIENCE, VOL. 249 linear function of speed during concertina Fig. 2. (A) Frequency of movement as a locomotion by C. constrictor (19) but with a function of speed. For lateral undulation (0) the rcgression equation relating frequcncy of greater slope than that of lateral undulation movement (J)(in cycles per minute) to mean (t = 3.67, df = 28, P < 0.001, Fig. 1A). forward speed (spced) (in kdometcrs pcr The point of intersection between the in- hour) is: J= 54.9 x speed + 1.6, n = 41, creasing and constant phases of the metabol- P < 0.001. Sample sizes for lateral undulation ic resDonse lot defines the maximal rate of are as follows: 0.2 km hour-', n = 6; 0.3 km hour-', n = 6; 0.4 km hour-', n = 6; 0.5 Ian oxyg;n corknption ( VO~ ,,,) and the hour-', n = 5; 0.6 km hour-', n = 7; 0.8 km lowest speed at which i/02 ,, is achieved, hour-', n = 7; 1.0 km hour-', 11 = 3. Thc 0- often termed the maximum aerobic speed regression equation for concertina locomotion 0.0 0.2 0.4 0.6 0.8 1.0 (MAS) (20). Coluber constrictor performing (A) is J= 132 x speed + 1.2, n= 10, Mean speed (km hour-') P < 0.05. Sample slzes for concertina locomo- lateral undulation achieves h2,, = 0.83 B tion arc 0.15 km hour-', n = 5 and 0.2 km ml of O2per gram per hour + 0.06 (n = 5) hour-', n = 5. (B) Gross energetic cost of a at MAS = 0.5 km hour-' (Fig.- 1A). This single cycle of movement as a function of ~0~ is nine times the resting rate and is speed. We calculated these values by dividing similar to the maximum rate previously re- V02 at a particular specd by the frequency of movcmcnt over the same time interval. Sam- ported for this species (21). The MAS is ple sizes are as in Fig. 1A for corresponding one-tenth of the maximum burst specd (22) speeds. of these animals (mean maximum burst speed = 5.5 2 0.4 km hour-'). Endurance decreased too precipitously during concerti- na locomotion (Fig. 1B) to permit us to Mean speed (km hour -') determine i/02,ax and MAS for this loco- motor mode. na locomotion is indistinguishable from by both aerobic metabolism and increasing Rates of oxygen consumption extrapolat- zero (t = 0.89, df = 7, P > 0.40), i/02 contributions of anaerobic metabolism. The ed to zero speed (the y intercept) are often (I= 1.5O,df=7,P>O.lO),and bQ ,,,, energetic cost of a single cycle of lateral elevated above resting rates, and earlier in- (t = 2.36, df = 7, P > 0.50). The y inter- undulation does not change within the vestigators have interpreted this increment cepts for the metabolic responses during range of aerobically sustainable speeds [F(3, as the energetic cost of postural support concertina and lateral undulation are also 9) = 2.57, P = 0.121 (Fig. 2B) but does (20). For C. constrictor performing lateral indistinguishable from each other (t = 1.84, vary significantly among individual snakes undulation, the y intercept is elevated above df = 28, P > 0.05). [F(3, 26) = 33.9, P < O.OOl] (23). zero (t = 2.61, df = 21, P < 0.02) but is Snakes increase speed by increasing the Concertina locomotion has an increased indistinguishable from the resting (t = 1.39, number of cycles of movement per unit time energetic cost compared to that of lateral df=21, P>0.10) or pre-exercise (Fig. 2A). The frequency of lateral undula- undulation. The oxygen consumption of (t = 0.33, df = 21, P > 0.50) rates of oxy- tion continues to increase beyond the range animals performing concertina locomotion gen consumption (Fig. 1A). The y intercept of sustainable speed. Thus, undulation at exceeds ~02predicted for snakes perform- for the metabolic response during concerti- nonsustainable speeds is probably supported ing lateral undulation at similar speeds (Fig. 1A). Furthermore, endurance during con- certina locomotion is much less than for Fig. l..(A) Stcady-statc rate of oxygen consump- tion (PO2) as a hction of speed for seven lateral undulation at similar speeds (Fig. individuals performing lateral undulation (0)and 1B). The elevated energetic cost of concerti- three individuals performing concertina locomo- na locomotion is attributable to two factors: tion (A). Mean speed is reported, because animals (i) snakes performing concertina locomo- moving by concertina locomotion periodically stop. The mean resting rate of oxygen consump- tion require more cycles of movement to tion is indicated by the x at zero speed; prc- sustain the same speed than they do during exercise ratcs of oxygen consumption are indicat- lateral undulation [two-tailed paired t test ed by circles at zero speed.
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