Comparative Biochemistry and Physiology Part A 131Ž. 2001 61᎐75 Review How muscles accommodate movement in different physical environments: aquatic vs. terrestrial locomotion ଝ in vertebrates Gary B. Gillisa,U, Richard W. Blobb aDepartment of Organismic and E¨olutionary Biology, Har¨ard Uni¨ersity, Concord Field Station, Old Causeway Rd., Bedford, MA 01730, USA bDepartment of Zoology, Di¨ision of Fishes, Field Museum of Natural History, 1400 South Lake Shore Dri¨e, Chicago, IL 60605, USA Received 13 January 2001; received in revised form 15 May 2001; accepted 22 August 2001 Abstract Representatives of nearly all vertebrate classes are capable of coordinated movement through aquatic and terrestrial environments. Though there are good data from a variety of species on basic patterns of muscle recruitment during locomotion in a single environment, we know much less about how vertebrates use the same musculoskeletal structures to accommodate locomotion in physically distinct environments. To address this issue, we have gathered data from a broad range of vertebrates that move successfully through water and across land, including eels, toads, turtles and rats. Using high-speed video in combination with electromyography and sonomicrometry, we have quantified and compared the activity and strain of individual muscles and the movements they generate during aquatic vs. terrestrial locomotion. In each focal species, transitions in environment consistently elicit alterations in motor output by major locomotor muscles, including changes in the intensity and duration of muscle activity and shifts in the timing of activity with respect to muscle length change. In many cases, these alterations likely change the functional roles played by muscles between aquatic and terrestrial locomotion. Thus, a variety of forms of motor plasticity appear to underlie the ability of many species to move successfully through different physical environments and produce diverse behaviors in nature. ᮊ 2001 Elsevier Science Inc. All rights reserved. Keywords: Modulation; Biomechanics; Kinematics; EMG; Muscle; Vertebrate; Locomotion; Aquatic; Terrestrial; Electromyography; Sonomicrometry; Environment ଝ This paper was originally presented as part of the ESCPB Congress symposium ‘Learning about the Comparative Biomechanics of Locomotion and Feeding’, Liege July 26᎐27, 2000. U ` Corresponding author. Tel.: q1-781-275-1275; fax: q1-781-275-9613. E-mail address: [email protected]Ž. G.B. Gillis . 1095-6433r01r$ - see front matter ᮊ 2001 Elsevier Science Inc. All rights reserved. PII: S 1 0 9 5 - 6 4 3 3Ž. 0 1 00466-4 62 G.B. Gillis, R.W. Blob rComparati¨e Biochemistry and Physiology Part A 131() 2001 61᎐75 1. Introduction accomplish a variety of motor tasks that often have very different functional requirementsŽ Mac- The vertebrate musculoskeletal system is a pherson, 1991; Johnston and Bekoff, 1996. The complex, integrated assemblage that incorporates ability to perform a variety of motor behaviors, bone, connective tissue and muscle. Whereas bone often in a range of environments, is crucial for forms the structural framework of the body, ten- survival in many species. Studies of several sys- dons, ligaments and muscles provide the functio- tems have begun to explore how muscle recruit- nal linkages among structural elements. Muscle, ment is modulated to perform a greater breadth through its dynamic contractile capacity, serves as of tasksŽ Gruner and Altman, 1980; Jasmin and the actuator of these elements, and thus is re- Gardiner, 1987; Buford and Smith, 1990; Roy et sponsible for generating the coordinated move- al., 1991; Smith and Carlson-Kuhta, 1995; John- ments involved in the behaviors that pique our ston and Bekoff, 1996; Kamel et al., 1996; intellectual curiosity as biologists. To understand Ashley-Ross and Lauder, 1997; Delvolve et al., how skeletal muscles provided the force, work 1997; Biewener and Gillis, 1999; Earhart and and power necessary to generate such coordi- Stein, 2000; Moon, 2000. Comparisons of muscle nated movements, scientists first examined their activity patterns during aquatic and terrestrial basic structural organization and later tested their locomotion have proven to be a particularly physiological properties in vitroŽ e.g. Woledge et promising focus for studies of the mechanisms of al., 1985. More recently, to gain insight into how motor flexibility. muscles are functionally integrated and operate Perhaps no single factor pervades as many in vivo, biologists have begun to correlate pat- facets of an organism’s biology as the environ- terns of muscle activity with the movements they ment in which it lives. Water and air represent create during various dynamic behaviors. Loco- the fluid media in which organisms must survive motion in particular has received considerable and reproduce, and the many physical disparities study and, as a result, there are now quantitative Ž.e.g. density, viscosity, gravitational load between data on movements and patterns of muscle acti- these environments can have important conse- vation involved in locomotor behaviors as diverse quences for organismal design and functionŽ De- as the axial undulations and fin motions of jours et al., 1987; Denny, 1993; Vogel, 1994. swimming fishŽ Westneat and Walker, 1997; Al- Nevertheless, transitions between aquatic and ter- tringham and Ellerby, 1999. , the ballistic jumps of restrial environments are not unusual among ani- frogsŽ. Marsh, 1994 , the serpentine motions of mals, and can occur over a variety of temporal snakesŽ. Jayne, 1988; Moon and Gans, 1998 , the scalesŽ. Little, 1983; Gordon and Olson, 1995 . At limb oscillations of quadrupedsŽ Engberg and least some members of nearly all vertebrate Lundberg, 1969; Goslow et al., 1981. and bipeds classesŽ as well as members of multiple inverte- Ž.Battye and Joseph, 1966; Gatesy, 1999 and even brate phyla. are capable of making such transi- the flapping flight of birdsŽ Dial, 1992; Tobalske, tions. Environmental transitions that occur over 1995. More recently, direct experimental analy- large time scalesŽ e.g. the movement of ancestral ses of muscle force, strain, and activation in tetrapods from water out onto land. or take place concert with kinematic data have facilitated in- over the course of ontogenyŽ e.g. anuran meta- sight into the specific functional roles individual morphosis. can be facilitated by numerous struc- muscles play during certain locomotor move- tural and physiological adaptations or develop- mentsŽ Roberts et al., 1997; Biewener et al., mental transformations. However, animals that 1998a,b. make more ephemeral transitions between aquatic Research on in vivo muscle function has af- and terrestrial habitats are faced with the forded a detailed understanding of muscle use formidable problem of functioning adequately in during many distinct, steady-state activities in different environments while using the same suite which the mechanical demands placed on the of structural and physiological traits. musculoskeletal system vary relatively little. How- What, then, are the musculoskeletal bases un- ever, animals must perform a wide range of be- derlying locomotion in water and on land for such haviors with only a finite number of muscles animals? One possibility is that few or no alter- available to contribute to these tasks. As a result, ations in motor output or musculoskeletal func- many of the same muscles must be recruited to tion are required to accommodate movement in G.B. Gillis, R.W. Blob rComparati¨e Biochemistry and Physiology Part A 131() 2001 61᎐75 63 these physically distinct habitats. Perhaps an ani- changes in muscle fascicle lengthŽ. strains also mal can activate the same suite of locomotor were evaluated based on kinematic measure- muscles in the same way to drive its anatomical mentsŽ. eels or direct measurements obtained structures to generate sufficient propulsion in through sonomicrometryŽ.Ž toads and rats tech- both water and on land. This seems rather un- niques reviewed by Jayne and Lauder, 1995; likely given the dramatically different physical Biewener et al., 1998a,b; Olson and Marsh, 1998. properties that characterize aquatic and terres- Aquatic trials were recorded either in a flow tank trial environmentsŽ. Denny, 1993; Vogel, 1994 . Ž.eels, turtles or in still water within a large Therefore, if the dynamics of the locomotor sys- aquariumŽ. toads, rats . Terrestrial trials were tem must be actively altered, and shifts in the measured on a treadmillŽ. rats , on a solid surface timing or degree of muscle activation andror Ž.toads, turtles , or on wet packed sand Ž. eels . strain patterns do underlie the capacity to move Locomotor speeds of the animals could be easily adequately in different environments, can general controlled in the flow tank or on the treadmill, patterns be identified? For example, does the but in all other circumstances speeds were se- influence of gravity on land lead to consistent lected by the animal. Nevertheless, in all cases increases in the intensity and duration of activity the largest possible range of steady speeds was in muscles important for counteracting body obtained, with all experiments performed at room weight and propelling the body forwards during temperatureŽ. 20᎐22ЊC . Because our studies ex- each locomotor cycle? Does the increased fluid amined species belonging to diverse lineages that viscosity in water necessitate greater levels of use different modes of locomotion, we intend our muscle activity in limb flexors during swimming review