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Springs, steroids, and slingshots: the roles of enhancers and constraints in animal movement

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Abstract

Whole-body movement is an essential part of life for many animal species, and is used to evade predators, capture prey, and perform many other behaviors. In many cases, the ability to perform rapid movements may be crucial to fitness as doing so may allow animals to do things like effectively capture an elusive prey or to elude a chasing predator. A significant body of research has been devoted toward the musculoskeletal and neurobiological basis of animal movement, with large reviews and volumes written on locomotion and feeding. Biologists have also defined how movement can be quantified and compared among different species. Arnold (Am Zool 23:347–361, 1983) first clearly explained that the ability to perform an ecologically important task could be labeled and quantified as maximum performance abilities, a point that is elaborated upon later (Garland and Losos, Ecological morphology: integrative organismal biology. University of Chicago Press, Chicago, 1994; Irschick et al., Evol Ecol Res 10:177–196, 2008). Some commonly examined performance traits include maximum sprint speed, maximum acceleration or deceleration, maneuverability, maximum aerobic capacity (VO2max), bite force, and rapidity of tongue projection, among other examples. Although the ability to perform such movements can be limited by muscle physiology, there are several situations in which the limits of muscle physiology are circumvented with a range of specializations. Here, we synthesize the literature dealing with movement (primarily ballistic) enhancers. Our goal is both to encapsulate the current state of knowledge of enhancers, and also to provide a broader evolutionary framework that might explain in which ecological contexts they have evolved, and how they can be studied in the future. Some common mechanisms for enhancing movement include elastic energy storage (e.g., tendons and other materials) in vertebrates and invertebrates, or hormonal changes (e.g., increased testosterone levels).

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References

  • Aerts P (1998) Vertical jumping in Galago senegalensis: the quest for an obligate mechanical power amplifier. Philos Trans R Soc Lond B 353:1607–1620

    Article  Google Scholar 

  • Alexander RM (2002) Tendon elasticity and muscle function. Comp Biochem Physiol A Mol Integr Physiol 133:1001–1011

    Article  PubMed  Google Scholar 

  • Alexander RM (2003) Principles of animal locomotion. Princeton University Press, Princeton

    Google Scholar 

  • Alexander RM (2004) Hitching a lift hydrodynamically—in swimming, flying and cycling. J Biol 3:7

    Article  PubMed  Google Scholar 

  • Alexander RM, Vernon A (1975) The mechanics of hopping by kangaroos (Macropodidae). J Zool Lond 177:265–303

    Article  Google Scholar 

  • Alfaro ME, Brock CD, Banbury BL, Wainwright PC (2009) Does evolutionary innovation in pharyngeal jaws lead to rapid lineage diversification in labrid fishes? BMC Evol Biol 9:255–269

    Article  PubMed  Google Scholar 

  • Anderson FC, Pandy MG (1993) Storage and utilization of elastic strain energy during jumping. J Biomech 26:1413–1427

    Article  PubMed  CAS  Google Scholar 

  • Anderson CV, Deban SM (2010) Ballistic tongue projection in chameleons maintains high performance at low temperatures. Proc Natl Acad Sci 107:5495–5499

    Google Scholar 

  • Angilletta MJ, Cooper BS, Schuler MS, Boyles JG (2010) The evolution of thermal physiology in endotherms. Front Biosci 2:861–881

    Article  Google Scholar 

  • Arnold SJ (1983) Morphology, performance and fitness. Am Zool 23:347–361

    Google Scholar 

  • Astley HC, Roberts TJ (2012) Evidence for a vertebrate catapult: elastic energy storage in the plantaris tendon during frog jumping. Biol Lett 8:386–389

    Article  PubMed  Google Scholar 

  • Azizi E, Roberts TJ (2009) Biaxial strain and variable stiffness in aponeuroses. J Physiol 587:4309–4318

    Article  PubMed  CAS  Google Scholar 

  • Bauwens D, Garland T Jr, Castilla AM, Van Damme R (1995) Evolution of sprint speed in lacertid lizards: morphological, physiological and behavioral covariation. Evolution 49:848–863

    Article  Google Scholar 

  • Bennet AF (1984) Thermal dependence of muscle function. Am J Physiol 247:R217–R229

    Google Scholar 

  • Bennet-Clark HC, Lucey ECA (1967) The jump of the flea: a study of the energetics and a model of the mechanism. J Exp Biol 47:59–76

    PubMed  CAS  Google Scholar 

  • Bernal D, Donley JM, Shadwick RE, Syme DA (2005) Mammal-like muscles power swimming in a cold-water shark. Nature 437:1349–1352

    Article  PubMed  CAS  Google Scholar 

  • Biewener AA (1998) Muscle function in vivo: a comparison of muscles used for elastic energy savings versus muscles used to generate mechanical power. Am Zool 38:703–717

    CAS  Google Scholar 

  • Biewener AA (2003) Animal locomotion. Oxford University Press, Oxford

  • Biewener AA, Alexander RMcN, Heglund NC (1981) Elastic energy storage in the hopping of kangaroo rats (Dipodomys spectabilis). J Zool Lond 195:369–383

    Article  Google Scholar 

  • Biewener AA, Konieczynski DD, Baudinette RV (1998) In vivo muscle force–length behavior during steady-speed hopping in tammar wallabies. J Exp Biol 201:1681–1694

    PubMed  CAS  Google Scholar 

  • Blake RW (2004) Fish functional design and swimming performance. J Fish Biol 65:1193–1222

    Article  Google Scholar 

  • Bond JE, Opell BD (1998) Testing adaptive radiation and key innovation hypotheses in spiders. Evolution 52:403–414

    Article  Google Scholar 

  • Burrows M (2003) Froghopper insects leap to new heights. Nature 424:509

    Article  PubMed  CAS  Google Scholar 

  • Burrows M (2006a) Jumping performance of froghopper insects. J Exp Biol 209:4607–4621

    Article  PubMed  Google Scholar 

  • Burrows M (2006b) Morphology and action of the hind leg joints controlling jumping in froghopper insects. J Exp Biol 209:4622–4637

    Article  PubMed  Google Scholar 

  • Burrows M (2008) Jumping strategies and performance in shore bugs (Hemiptera, Heteroptera, Saldidae). J Exp Biol 212:106–115

    Article  Google Scholar 

  • Butler PJ, Jones DR (1997) Physiology of diving of birds and mammals. Physiol Rev 77:837–899

    PubMed  CAS  Google Scholar 

  • Carrier DR (1987) The evolution of locomotor stamina in tetrapods: circumventing a mechanical constraint. Paleobiology 13:326–341

    Google Scholar 

  • Carrier DR (1991) Conflict in the hypaxial musculo-skeletal system: documenting an evolutionary constraint. Am Zool 31:644–654

    Google Scholar 

  • Casey TM, Hegel JR, Buser CS (1981) Physiology and energetics of pre-flight warm-up in the eastern tent caterpillar moth Malacosoma americanum. J Exp Biol 94:119–135

    Google Scholar 

  • Claverie T, Chan E, Patek SN (2011) Modularity and scaling in fast movements: power amplification in mantis shrimp. Evolution 65:443–461

    Article  PubMed  Google Scholar 

  • Curtin NA, Woledge RC, Aerts P (2005) Muscle directly meets the vast power demands in agile lizards. Proc R Soc B 272:581–584

    Article  PubMed  Google Scholar 

  • de Groot JH, van Leeuwen JL (2004) Evidence for an elastic projection mechanism in the chameleon tongue. Proc R Soc Lond B 271:761–770

    Article  Google Scholar 

  • Deban SM, Wake DB, Roth G (1997) Salamander with a ballistic tongue. Nature 389:27–28

    Article  CAS  Google Scholar 

  • Dickinson MH, Lighton JR (1995) Muscle efficieny and elastic storage in the flight motor of Drosophila. Science 268:87–90

    Article  PubMed  CAS  Google Scholar 

  • Dluglosz EM, Chappell MA, McGilivray DG, Syme DA, Garland T Jr (2009) Locomotor trade-offs in mice selectively bred for high voluntary wheel running. J Exp Biol 212:2612–2618

    Article  Google Scholar 

  • Donoughe S, Crall JD, Merz RA, Combes SA (2011) Resilin in dragonfly and damselfly wings and its implications for wing flexibility. J Morphol 272:1409–1421

    Article  PubMed  Google Scholar 

  • Dorn TW, Schache AG, Pandy MG (2012) Muscular strategy shift in human running: dependence of running speed on hip and ankle muscle performance. J Exp Biol 215:1944–1956

    Article  PubMed  Google Scholar 

  • Ellerby DJ, Cleary M, Marsh RL, Buchanan CI (2003) Measurement of maximum oxygen consumption in guinea fowl Numida meleagris indicates that birds and mammals display a similar diversity of aerobic scopes during running. Physiol Biochem Zool 76:695–703

    Article  PubMed  Google Scholar 

  • Enriquez J, Gullans S (2012) Genetically enhanced Olympics are coming. Nature 487:297

    Article  PubMed  CAS  Google Scholar 

  • Garland T Jr (1984) Physiological correlates of locomotory performance in a lizard: an allometric approach. Am J Physiol 247:R806–R815

    PubMed  CAS  Google Scholar 

  • Garland T Jr, Losos JB (1994) Ecological morphology of locomotor performance in squamate reptiles. In: Wainwright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology. University of Chicago Press, Chicago, pp 240–302

    Google Scholar 

  • Garland T Jr, Else PL, Hulbert AJ, Tap P (1987) Effects of endurance training and captivity on activity metabolism of lizards. Am J Physiol Regul Physiol 252:R450–R456

    CAS  Google Scholar 

  • Garland T Jr, Bennett AF, Daniels CB (1990) Heritability of locomotor performance and its correlates in a natural population of vertebrates. Experientia 46:530–533

    Article  Google Scholar 

  • Girgenrath M, Marsh RL (2003) Season and testosterone affect contractile properties of fast calling muscles in the gray tree frog Hyla chrysoscelis. Am J Physiol Regul Integr Comp Physiol 284:R1513–R1520

    PubMed  CAS  Google Scholar 

  • Griggs RC, Kingston W, Jozefowicz RF, Herr BE, Forbes G, Halliday D (1989) Effect of testosterone on muscle mass and muscle protein synthesis. J Appl Physiol 66:498–503

    Google Scholar 

  • Gould SJ, Lewontin RC (1979) The spandrels of San Marco and the panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B 205:581–598

    Article  PubMed  CAS  Google Scholar 

  • Gronenberg W (1996) Fast actions in small animals: springs and click mechanisms. J Comp Physiol A 178:727–734

    Article  Google Scholar 

  • Haas F, Gorb S, Blickhan R (2000) The function of resilin in beetle wings. Proc R Soc Lond B 267:1375–1381

    Article  CAS  Google Scholar 

  • Hammond KA, Chappell MA, Cardullo RA, Lin R-S, Johnsen TS (2000) The mechanistic basis of aerobic performance variation in red junglefowl. J Exp Biol 203:2053–2064

    PubMed  CAS  Google Scholar 

  • Hau M (2007) Regulation of male traits by testosterone: implications for the evolution of vertebrate life histories. BioEssays 29:133–144

    Article  PubMed  CAS  Google Scholar 

  • Henry HT, Ellerby DJ, Marsh RL (2005) Performance of guinea fowl Numida meleagris during jumping requires storage and release of elastic energy. J Exp Biol 208:3293–3302

    Article  PubMed  Google Scholar 

  • Herrel A, Bonneaud C (2012) Trade-offs between burst performance and maximal exertion capacity in a wild amphibian, Xenopus tropicalis. J Exp Biol 215:3106–3111

    Article  PubMed  Google Scholar 

  • Herrel A, Podos J, Huber SK, Hendry AP (2005) Evolution of bite force in Darwin’s finches: a key role for head width. J Evol Biol 18:669–675

    Article  PubMed  CAS  Google Scholar 

  • Herrel A, Podos J, Vanhooydonck B, Hendry AP (2009) Force–velocity trade-off in Darwin’s finch jaw function: a biomechanical basis for ecological speciation? Funct Ecol 23:119–125

    Article  Google Scholar 

  • Higham TE, Biewener AA (2008) Integration within and between muscles during terrestrial locomotion: effects of incline and speed. J Exp Biol 211:2303–2316

    Article  PubMed  Google Scholar 

  • Higham TE, Korchari PG, McBrayer LM (2011) How muscles define maximum locomotor performance in lizards: an analysis using stance and swing phase muscles. J Exp Biol 214:1685–1691

    Article  PubMed  Google Scholar 

  • Hill AV (1938) The heat of shortening and the dynamic constants of muscle. Proc R Soc Lond B Biol 126:136–195

    Article  Google Scholar 

  • Hodges SA, Arnold ML (1995) Spurring plant diversification: are floral nectar spurs a key innovation? Proc R Soc Lond B 262:343–348

    Article  Google Scholar 

  • Hoyt DF, Kenagy GJ (1988) Energy costs of walking and running gaits and their aerobic limits in golden-mantled ground squirrels. Physiol Zool 61:34–40

    Google Scholar 

  • Huey RB, Hertz PE (1984) Effects of body size and slope on acceleration of a lizard (Stellio stellio). J Exp Biol 110:113–123

    Google Scholar 

  • Husak JF (2006) Does survival depend on how fast you can run or how fast you do run? Funct Ecol 20:1080–1086

    Article  Google Scholar 

  • Husak JF, Irschick DJ (2009) Steroid use and human performance: lessons for integrative biologists. Integr Comp Biol 49:354–364

    Article  PubMed  Google Scholar 

  • Husak JF, Irschick DJ, Meyers JJ, Lailvaux SP, Moore IT (2007) Hormones, sexual signals, and performance of green anole lizards (Anolis carolinensis). Horm Behav 52:360–367

    Article  PubMed  CAS  Google Scholar 

  • Hustert R, Baldus M (2010) Ballistic movements of jumping legs implemented as variable components of cricket behaviour. J Exp Biol 213:4055–4064

    Article  PubMed  CAS  Google Scholar 

  • Huyghe K, Husak JF, Moore IT, Vanhooydonck B, Van Damme R, Molina-Borja M, Herrel A (2010) Effects of testosterone on morphology, performance, and muscle mass in a lizard. J Exp Zool 313A:9–16

    Article  CAS  Google Scholar 

  • Irschick DJ, Garland T Jr (2001) Integrating function and ecology in studies of adaptation: investigations of locomotor capacity as a model system. Annu Rev Ecol Syst 32:367–396

    Article  Google Scholar 

  • Irschick DJ, Meyers JJ, Husak JF, Le Galliard J-F (2008) How does selection operate on whole-organism function performance capabilities? A review and synthesis. Evol Ecol Res 10:177–196

    Google Scholar 

  • James RS, Navas CA, Herrel A (2007) How important are skeletal muscle mechanics in setting limits on jumping performance? J Exp Biol 210:923–933

    Article  PubMed  Google Scholar 

  • Josephson RK (1999) Dissecting muscle power output. J Exp Biol 202:3369–3375

    PubMed  CAS  Google Scholar 

  • Kaufmann JS, Bennett AF (1989) The effect of temperature and thermal acclimation on locomotor performance in Xantusia vigilis, the desert night lizard. Physiol Zool 62:1047–1058

    Google Scholar 

  • Klukowski M, Jenkinson NM, Nelson CE (1998) Effects of testosterone on locomotor performance and growth in field-active northern fence lizards, Sceloporus undulatus hyacinthinus. Physiol Zool 71:506–514

    PubMed  CAS  Google Scholar 

  • Kohlsdorf T, Navas C (2012) Evolution of form and function: morphophysiological relationships and locomotor performance in tropidurine lizards. J Zool Lond 288:41–49

    Article  Google Scholar 

  • Komi PV, Bosco C (1978) Utilization of stored elastic energy in leg extensor muscles by men and women. Med Sci Sport 10:261–265

    CAS  Google Scholar 

  • Kubo K, Kawakami Y, Fukunaga T (1999) Influence of elastic properties of tendon structures on jump performance in humans. J Appl Physiol 87:2090–2096

    PubMed  CAS  Google Scholar 

  • Lauder GV (1996) The argument from design. In: Rose MR, Lauder GV (eds) Adaptation. Academic Press, San Diego, pp 55–91

    Google Scholar 

  • Lauder GV, Drucker EG (2004) Morphology and experimental hydrodynamics of fish fin control surfaces. IEEE J Ocean Eng 29:556–571

    Article  Google Scholar 

  • Legreneur P, Laurin M, Monteil KM, Bels V (2012) Convergent exaptation of leap up for escape in distantly related arboreal amniotes. Adapt Behav 20:67–77

    Article  Google Scholar 

  • Liao JC (2007) A review of fish swimming mechanics and behaviour in altered flows. Philos Trans R Soc B 362:1973–1993

    Article  Google Scholar 

  • Lomo R, Westgaard RH, Dahl HA (1974) Contractile properties of muscle: control by pattern of muscle activity in the rat. Proc R Soc Lond B 187:99–103

    Article  PubMed  CAS  Google Scholar 

  • Lutz GJ, Rome LC (1996) Muscle function during jumping in frogs. I. Sarcomere length change, EMG pattern, and jumping performance. Am J Physiol 271:C563–C570

    PubMed  CAS  Google Scholar 

  • Marsh RL (1999) How muscles deal with real-world loads: the influence of length trajectory on muscle performance. J Exp Biol 202:3377–3385

    PubMed  CAS  Google Scholar 

  • McElroy EJ, McBrayer LD (2010) Getting up to speed: acceleration strategies in the Florida scrub lizard, Sceloporus woodi. Physiol Biochem Zool 83:643–653

    Article  PubMed  Google Scholar 

  • Nishikawa KC (2000) Feeding in frogs. In: Schwen KK (ed) Feeding: form, function and evolution in tetrapod vertebrates. Academic Press, San Diego, pp 117–147

  • O’Connor JL, McBrayer LM, Higham TE, Husak JF, Moore IT, Rostal DC (2011) Effects of training and testosterone on muscle fiber types and locomotor performance in male six-lined racerunners (Aspidoscelis sexlineata). Physiol Biochem Zool 84:394–405

    Article  PubMed  CAS  Google Scholar 

  • Owerkowicz T, Farmer CG, Hicks JW, Brainerd EL (1999) Contribution of gular pumping to lung ventilation in monitor lizards. Science 284:1661–1663

    Article  PubMed  CAS  Google Scholar 

  • Patek SN, Korff WL, Caldwell RL (2004) Biomechanics: deadly strike mechanism of a mantis shrimp—the shrimp packs a punch powerful enough to smash its prey’s shell underwater. Nature 428:819–820

    Article  PubMed  CAS  Google Scholar 

  • Patek SN, Baio JE, Fisher BL, Suarez AV (2006) Multifunctionality and mechanical origins: ballistic jaw propulsion in trap-jaw ants. Proc Natl Acad Sci 103:12787–12792

    Article  PubMed  CAS  Google Scholar 

  • Patek SN, Dudek DM, Rosario MV (2011) From bouncy legs to poisoned arrows: elastic movements in invertebrates. J Exp Biol 214:1973–1980

    Article  PubMed  CAS  Google Scholar 

  • Pollock CM, Shadwick RE (1994) Allometry of muscle, tendon, and elastic energy storage capacity in mammals. Am J Physiol Regul Integr Comp Physiol 266:R1022–R1031

    CAS  Google Scholar 

  • Powell PL, Roy RR, Kanim P, Bello MA, Edgerton VR (1984) Predictability of skeletal muscle tension from architectural determinations in guinea pig hindlimbs. J Appl Physiol 57:1715–1721

    PubMed  CAS  Google Scholar 

  • Prilutsky BI, Herzog W, Allinger TL (1996) Mechanical power and work of cat soleus, gastrocnemius and plantaris muscles during locomotion: possible functional significance of muscle design and force patterns. J Exp Biol 199:801–814

    PubMed  CAS  Google Scholar 

  • Roberts TJ (2002) The integrated function of muscles and tendons during locomotion. Comp Biol Physiol A 133:1087–1099

    Google Scholar 

  • Roberts TJ, Azizi E (2011) Flexible mechanisms: the diverse roles of biological springs in vertebrate movement. J Exp Biol 214:353–361

    Article  PubMed  Google Scholar 

  • Roberts TJ, Marsh RL (2003) Probing the limits to muscle-powered accelerations: lessons from jumping bullfrogs. J Exp Biol 206:2567–2580

    Article  PubMed  Google Scholar 

  • Roberts TJ, Marsh RL, Weyland PG, Taylor CR (1997) Muscular force in running turkeys: the economy of minimizing work. Science 275:1113–1115

    Article  PubMed  CAS  Google Scholar 

  • Roberts TJ, Abbott EM, Azizi E (2011) The weak link: do muscle properties determine locomotor performance in frogs? Philos Trans R Soc B 366:1488–1495

    Article  Google Scholar 

  • Rome LC, Choi IH, Lutz G, Sosnicki A (1992) The influence of temperature on muscle function in the fast swimming scup. I: shortening velocity and muscle recruitment during swimming. J Exp Biol 163:259–279

    PubMed  CAS  Google Scholar 

  • Salmons S, Henriksson J (1981) The adaptive response of skeletal muscle to increased use. Muscle Nerve 4:94–105

    Article  PubMed  CAS  Google Scholar 

  • Sellers WI, Pataky TC, Cravaggi P, Crompton RH (2010) Evolutionary robotic approaches in primate gait analysis. Int J Primatol 31:321–338

    Article  Google Scholar 

  • Sensenig AT, Schultz JW (2003) Mechanics of cuticular elastic energy storage in leg joints lacking extensor muscles in arachnids. J Exp Biol 206:771–784

    Article  PubMed  Google Scholar 

  • Sensenig AT, Schultz JW (2004) Elastic energy storage in the pedipalpal joints of scorpions and sun-spiders (Arachnida, Scorpiones, Solifugae). J Arachnol 32:1–10

    Article  Google Scholar 

  • Sorci G, Swallow JG, Garland T Jr, Clobert J (1995) Quantitative genetics of locomotor speed and endurance in the lizard Lacerta vivipara. Physiol Zool 68:698–720

    Google Scholar 

  • Spagna JC, Vakis AI, Schmidt CA, Patek SN, Zhang X, Tsutsui ND, Suarez AV (2008) Phylogeny, scaling, and the generation of extreme forces in trap-jaw ants. J Exp Biol 211:2358–2368

    Article  PubMed  Google Scholar 

  • Sutton GP, Burrows M (2011) Biomechanics of jumping in the flea. J Exp Biol 214:836–847

    Article  PubMed  Google Scholar 

  • Syme DA (2006) Functional properties of skeletal muscle. In: Shadwick RE, Lauder GV (eds) Fish biomechanics. Academic Press, New York, pp 179–240

    Google Scholar 

  • Syme DA, Shadwick RE (2011) Red muscle function in stiff-bodied swimmers: there and almost back again. Philos Trans R Soc B 366:1507–1515

    Article  Google Scholar 

  • Tan H, Wilson AM (2011) Grip and limb force limits to turning performance in competition horses. Proc R Soc B 278:2105–2111

    Article  PubMed  Google Scholar 

  • Taylor CR, Maloiy GMO, Weibel ER, Langman VA, Kamau JMZ, Seeherman HJ, Heglund NC (1981) Design of the mammalian respiratory system. III: scaling maximum aerobic capacity to body mass: wild and domestic mammals. Respir Physiol 44:25–37

    Article  PubMed  CAS  Google Scholar 

  • Toro E, Herrel A, Irschick DJ (2004) The evolution of jumping performance in Caribbean Anolis lizards: solutions to biomechanical trade-offs. Am Nat 163:844–856

    Article  PubMed  Google Scholar 

  • Usherwood JR, Wilson AM (2005) No force limit on greyhound sprint speed. Nature 438:753–754

    Article  PubMed  CAS  Google Scholar 

  • Vanhooydonck B, Van Damme R, Aerts P (2001) Speed and stamina trade-off in lacertid lizards. Evolution 55:1040–1048

    Article  PubMed  CAS  Google Scholar 

  • Vanhooydonck B, Aerts P, Irschick DJ, Herrel A (2006) Power generation during locomotion in Anolis lizards: an ecomorphological approach. In: Herrel A, Speck T, Rowe NP (eds) Ecology and biomechanics. CRC Press, Boca Raton, pp 253–269

  • Van Wassenbergh S, Strother JA, Flammang BE, Ferry-Graham L, Aerts P (2008) Extremely fast prey capture in pipefish is powered by elastic recoil. J R Soc Interface 5:285–296

    Article  PubMed  Google Scholar 

  • Van Wassenbergh S, Roos G, Genbrugge A, Leysen H, Aerts P, Adriaens D, Herrel A (2009) Suction is kid's play: extremely fast suction in newborn seahorses. Biol Lett 5:200–203

    Article  PubMed  Google Scholar 

  • Wainwright SA, Vosburgh F, Hebrank JH (1978) Shark skin: function in locomotion. Science 202:747

    Article  PubMed  CAS  Google Scholar 

  • Walker JA (2004) Kinematics and performance of maneuvering control surfaces in Teleost fishes. IEEE J Ocean Eng 29:572–584

    Article  Google Scholar 

  • Walker JA, Westneat MW (2000) Mechanical performance of aquatic rowing and flying. Proc R Soc Lond B 267:1875–1881

    Article  CAS  Google Scholar 

  • Webb PW (1975) Acceleration performance of rainbow trout, Salmo gairdneri, and green sunfish, Lepomis cyanellus. J Exp Biol 63:451–465

    Google Scholar 

  • Webb PW (2006) Stability and maneuverability. In: Shadwick RE, Lauder GV (eds) Fish biomechanics. Academic Press, San Diego, pp 281–332

    Google Scholar 

  • Williams SB, Tan H, Usherwood JR, Wilson RS (2009) Pitch then power: limitations to acceleration in quadrupeds. Biol Lett 5:610–613

    Article  PubMed  Google Scholar 

  • Wilson RS, James RS, Van Damme R (2002) Trade-offs between speed and endurance in the frog Xenopus laevis: a multi-level approach. J Exp Biol 205:1145–1152

    PubMed  Google Scholar 

  • Wu GC, Wright JC, Whitaker DL, Ahn AN (2010) Kinematic evidence for superfast locomotory muscle in two species of teneriffiid mites. J Exp Biol 213:2551–2556

    Article  PubMed  Google Scholar 

  • Zehr EP, Sale DG (1994) Ballistic movement: muscle activation and neuromuscular adaptation. Can J Appl Physiol 19:363–378

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Anthony Herrel and two anonymous reviewers for their thoughtful and constructive comments on an earlier version of this manuscript. We thank members of Richard Blob and Timothy Higham’s labs for discussing certain topics in this manuscript.

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Higham, T.E., Irschick, D.J. Springs, steroids, and slingshots: the roles of enhancers and constraints in animal movement. J Comp Physiol B 183, 583–595 (2013). https://doi.org/10.1007/s00360-012-0734-z

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