Comparative Biochemistry and Physiology Part B 120 (1998) 41–49 Review Energetics and biomechanics of locomotion by red kangaroos (Macropus rufus) Rodger Kram a,*, Terence J. Dawson b a Department of Integrati6e Biology, Uni6ersity of California, Berkeley CA 94720-3140, USA b School of Biological Sciences, Uni6ersity of New South Wales, Sydney NSW 2052, Australia Received 15 May 1997; received in revised form 22 September 1997; accepted 7 October 1997 Abstract As red kangaroos hop faster over level ground, their rate of oxygen consumption (indicating metabolic energy consumption) remains nearly the same. This phenomenon has been attributed to exceptional elastic energy storage and recovery via long compliant tendons in the legs. Alternatively, red kangaroos may have exceptionally efficient muscles. To estimate efficiency, we measured the metabolic cost of uphill hopping, where muscle fibers must perform mechanical work against gravity. We found that −1 uphill hopping was much more expensive than level hopping. The maximal rate of oxygen consumption measured (3 ml O2 kg s−1) exceeds all but a few vertebrate species. However, efficiency values were normal, 30%. At faster level hopping speeds the effective mechanical advantage of the extensor muscles of the ankle joint remained the same. Thus, kangaroos generate the same muscular force at all speeds but do so more rapidly at faster hopping speeds. This contradicts a recent hypothesis for what sets the cost of locomotion. The cost of transport (J kg−1 m−1) decreases at faster hopping speeds, yet red kangaroos prefer to use relatively slow speeds that avoid high levels of tendon stress. © 1998 Elsevier Science Inc. All rights reserved. Keywords: Locomotion; Biomechanics; Kangaroos; Metabolic energy; Oxygen consumption; Energetics; Musculoskeletal; Tendon; Macropus rufus 1. Introduction fully satisfactory answers. What mechanisms can ac- count for the remarkable energetics? Why don’t red Some 25 years ago, Dawson and CR Taylor reported kangaroos hop at very fast speeds on a regular basis, that red kangaroos (Macropus rufus)1 consume since it appears to be a cheaper way to travel a given metabolic energy at nearly the same rate whether they distance? Although this paper does not fully resolve hop slowly (2 m s−1) or as fast as6ms−1 [17]. In the these questions, we present some unique data that adds ensuing years, several species of wallabies have also new insight is presented. been shown to have a nearly constant rate of energy In the original report, Dawson and Taylor [17] sug- consumption across hopping speed [5,48]. The biome- gested that the remarkable energetics of hopping are chanics of the phenomenon have been investigated ‘‘probably due to a greater storage and recovery of [4,5,7,9,24,30,35,37] but two questions still do not have energy in the elastic elements... in the rear limbs’’. Several research groups have explored this possibility. Alexander and Vernon [4] estimated that at6ms−1, elastic energy storage saves a red kangaroo up to 70% * Corresponding author. Tel.: +1 510 6439370; fax: +1 510 6436264; e-mail: [email protected] of the metabolic energy which would otherwise be 1 In 1973, this species was known as Megaleia rufa. required. However, subsequent measurements suggest 0305-0491/98/$19.00 © 1998 Elsevier Science Inc. All rights reserved. PII S0305-0491(98)00022-4 42 R. Kram, T.J. Dawson / Comparati6e Biochemistry and Physiology, Part B 120 (1998) 41–49 that some of their assumptions were in error and that approach or by the newer cost of generating force this 70% value is probably too high [9]. Ker et al. approach. [30] estimated that in the wallaby, Macropus rufo- Regardless of the mechanism behind the energetics, griseus, at least one third of the mechanical energy the behavior of red kangaroos seems to violate an- per hop is stored and recovered elastically. Griffiths other general ‘rule’ of animal locomotion. That ‘rule’ [24] studied the wallaby, Thylogale billardierii, using a is that within each gait, animals prefer to use the combination of kinematic and force sensing tendon speed that minimizes the amount of energy required buckles. He reported about 41% savings due to elastic to travel a unit distance (i.e. minimize the cost of energy reutilization but no increase in elastic savings transport). This idea was established for human walk- at faster speeds. Most recently, Biewener and ing more than 60 years ago [34]. Hoyt and Taylor Baudinette [9] studied the Tammar wallaby, Macropus [27] demonstrated that the idea applies to the three eugenii, over a range of hopping speeds and suggested basic gaits of quadrupeds and there are many other that without the elastic energy storage in the ankle examples in nature [3]. Because metabolic rate re- extensor tendons, the metabolic rate would be nearly mains nearly constant at faster hopping speed in red twice as great as that observed. kangaroos, the cost per unit distance monotonically Traditionally, there has been an assumed link be- decreases. If red kangaroos were to follow the rule of tween the metabolic cost and the mechanical work preferring to travel at the speed with the lowest cost done in running [13]. However, muscle consumes of transport, they would prefer to hop at their maxi- metabolic energy when it generates force isometrically mum speed on a regular basis. Red kangaroos are even though it does no work. The idea has emerged reported to be capable of hopping as fast as 14 m that tendons act largely as springs and that muscles s−1 yet they normally travel at much slower speeds act primarily as tension generators. If true, the [15]. All measurements of oxygen consumption for metabolic cost of level running would be dominated red kangaroo locomotion have been made during by the cost of generating muscular force rather than treadmill hopping where air resistance is zero. reflecting the mechanical work done by muscle Baudinette et al. [5] suggested that at higher speeds, [31,44,45]. Recent direct measurements of muscle fiber air resistance may play an increasingly important role length changes in running turkeys support this view such that a minimum cost of transport would be of muscles as primarily acting as tension generators reached at about 12 m s−1. However, there are no [39]. However, even if elastic storage and recovery of empirical metabolic data beyond6ms−1. Moreover, mechanical energy is such that no additional mechani- red kangaroos rarely hop as fast as 12 m s−1. cal work output of muscle is needed at faster hopping Biomechanical limitations may explain the behav- speeds, an energetic puzzle still remains. ioral preference of red kangaroos for moving at According to the cost of generating force approach speeds below the energetically optimal speed. In some [31], metabolic rate increases at faster speeds because situations, quadrupeds appear to select their gait muscle forces must be developed more quickly, re- based on acceptable levels of musculoskeletal stress quiring muscle fibers with faster intrinsic speeds. rather than minimizing metabolic cost [21]. Animals Muscle fibers with faster intrinsic speeds are less eco- appear to choose speeds that allow for some safety nomical force generators. Thus, in most animals, factor in terms of avoiding dangerous levels of bone, metabolic cost increases with running or hopping muscle or tendon stress (stress=force/cross sectional speed. Kram and Taylor [31] proposed that the time area) [11,36]. While Biewener and Baudinette’s [9] of foot–ground contact reflects the time of muscle data for Tammar wallabies (B6 kg) indicate that force development. In a variety of animals, across a muscle and tendon stresses do not approach critical wide speed range, they found that metabolic rate is levels even at speeds of 10 m s−1, Bennett and GC inversely proportional to foot–ground contact time Taylor’s [7] insightful analysis suggests that large hop- [31]. ping macropodids might easily reach critical tendon Macropodids maintain a nearly constant hop fre- stress levels. However, Bennett and Taylor’s [7] allo- quency over their normal speed range but the fraction metric comparison did not examine a large speed of the stride period when the feet are on the ground range for any one species. Thus, better estimates of (duty factor) decreases at faster speeds [7] Therefore, mechanical stresses in red kangaroos over a range of contact time decreases at faster hopping speeds. Thus, speeds are needed to consider if stress levels can ex- red kangaroos appear to be an exception to the cost plain their locomotor behavior. of generating force approach; at faster hopping Given these unresolved issues, three experiments speeds, contact time decreases but metabolic rate re- were conducted that pertain to the energetics and mains nearly constant. At present, the unusual en- biomechanics of red kangaroo locomotion. ergetics of red kangaroo locomotion are not 1. During level hopping, muscle fibers may do little explained by the traditional mechanical work based work because the tendons can store and recover en- R. Kram, T.J. Dawson / Comparati6e Biochemistry and Physiology, Part B 120 (1998) 41–49 43 ergy from hop to hop. On the other hand, the muscles 2.2. Oxygen consumption measurements of red kangaroos may be exceptionally efficient. We wanted to understand the various functions of muscle One female (body mass 20.4 kg) was cooperative and during locomotion (perform work versus generate ten- readily trained to hop on a motorized treadmill. We sion) and the associated metabolic cost. We hypothe- attempted to train a much larger male kangaroo to hop sized that red kangaroos have exceptionally efficient on the treadmill but we were unsuccessful. The tread- muscles compared to other similarly sized animals. To mill was located in a temperature controlled room that test this hypothesis, we measured the rate of oxygen was cooled to approximately 5°C to prevent the animal consumption during uphill hopping and calculated the from overheating.