12. Invertebrate locomotor systems R 0 B E R T J. F U L L 1 Department of Integrative Biology, University of California at Berkeley, Berkeley, Californio CHAPTER CONTENTS Speed Size Mechanisms of Locomotion Mode of locomotion Swimming Species Low Reynolds numbers (Re << 1) Temperature High Reynolds numbers (Re > 1,000) Conclusions Intermediate Reynolds numbers (1 < Re <: 1,000) Trends Crawling Speed, cycle frequency, and cycle distance Peristalsis Mechanical power output Two anchors Metabolic power input Pedal waves Explanatory hypotheses of trends Walking, running, and rolling Future Research Gaits Comparative muscle physiology Design trends and hypotheses Comparative bioenergetics and exercise physiology Dynamic models of rolling, walking, and running Comparative biomechanics Design of legs Collaboration Jumping Direct experiments using innovative technology Body size Cybercreatures and experiments: computer modeling Drag Appendix: List of Symbols Species Flying Aerodynamics of wings and bodies G 1id i n g Forward flapping flight ORGANISMAL BIOLOGY is entering an exciting new era Hovering of integration following the maturation of specialized Comparison of locomotor dynamics Speed fields. Comparative physiology, broadly defined to in- Frequency clude functional morphology and comparative biome- Mechanical power output chanics, sits in an opportune position with respect Production of Locomotion: Musculoskeletal Systems to its level of biological organization. Being between Filament, sarcomere, and muscle level molecular biology and behavioral ecology offers the Force production Force-velocity relationship possibility of linking molecular function to relevant Muscle-organism level whole-animal performance and behavior in the field. Muscle mechanical power output The technologies of rapid data acquisition, analysis, Mechanical advantage and moments imaging, and computer modeling will allow unprece- Energy transfer dented advancements in the future because the over- Energetics of Locomotion Aerobic metabolism whelming complexity involved in system integration Speed can be addressed for the first time. Size Why study locomotion? First, locomotion is one of Mode of locomotion the best behaviors to study from a systems viewpoint Species because the integration of systems is so evident. Muscu- Temperature and dehydration Anaerobic metabolism loskeletal systems-hydrostatic and jointed frame- Aerobic response pattern work-which produce movement, nervous and endo- Mixed aerobic and nonaerobic response pattern crine systems that control movement, and circulatory Nonaerobic response pattern and respiratory systems that sustain locomotion, are Endurance and metabolism often interdependent. I discuss the conversion of chemi- Continuous locomotion Intermittent locomotion cal energy in muscle cells to the mechanical energy that Metabolic cost of transport the whole animal generates for locomotion (Fig. 12.1). Chemical Energy Conversion of Chemical Energy Into Locomotor Mechanical Energy A Segmental Enerm (Comparative bioenergetics & (Comparatiie muscle physiology & (Comparative biomechanics) Exercise physiology) Functional morphology) L ~~ 0 Kinetic C (translational, rotational) High-energy phosphates Isolated muscle dynamics 0 M 0 T I 0 V YR Musculo-skeletal Joint Energy Transfer Across Joint Segment and Body Motion Mechanical Energy Dynamics Dynamics or Segment Boundary Output Stimulation /Activation & Musculo- ,,- skelelal - skelelal Energy enters segment Force Force - length function MJ and 2positive FM Force - velocity function Energy leaves segment Segmental Segmental acceleration W velocity 1Kinetic Energy- Joint Angular -+ MJ or2negative Passive Spring-damping (translation, (translation, Acceleration rotation) rotation) Energy is transferred I I I I from one segment to another aJ=0 Musculo-skeletal isometric contraction Velocity le ency Gravitational - Musculo-skeletal JoinlAn le Strain 4 herev absorbed and/or I scOred for release 1 CHAPTER 12: INVERTEBRATE LOCOMOTOR SYSTEMS 855 This requires a synthesis of information from the fields have already been accomplished and offer a tool for of comparative bioenergetics, comparative muscle testing function (493). Fifth, invertebrate locomotion physiology, functional morphology, comparative exer- and energetics are becoming increasingly important in cise physiology, and comparative biomechanics. Sec- ecology, where we seek an understanding of the spatial ond, locomotion is central to the behavior and function and temporal patterns of the distribution of animals. of nearly all animals during at least some phase of life, Invertebrates are important in disease and can act so general comparisons are possible among diverse as biological control agents, so an understanding of species. invertebrate locomotion is of obvious economic impor- Why study invertebrate locomotion in particular? tance. Finally, data on invertebrate locomotion can First, the typical, or representative, animal on Earth, if serve as biological inspiration to those studying artifi- there is one, must be an invertebrate. Three-fourths of cial intelligence and control, mechanics, and robotics the world’s animals are insects. Second, nowhere is from the nano- to mesoscopic scale in particular (193). there greater diversity within a group. The number and No review of invertebrate locomotion can be truly variety of arthropods alone exceeds that of vertebrates all-encompassing. Yet, showing only single examples, by 100-fold (217). Basic design principles become clear case studies, or model animals fails to represent the when we examine diverse systems with extreme func- diversity of systems available for study. The case study tional demands. “Natural” experiments can be con- approach may inhibit integration in the future. Instead ducted by the selection of appropriate species using a of listing each group and describing its mode of loco- comparative approach in a phylogenetic context. The motion, I put the information in a framework based variation in locomotor parameters as a result of evolu- on energy to facilitate comparison and integration of tion is far greater than can be attained by any direct muscle function, bioenergetics, exercise physiology, experimental manipulation. Variations due to size, and biomechanics (Fig. 12.1). As a result, I have re- mode of locomotion, species, and temperature allow a stricted my discussion to those groups for which more wide variety of hypotheses to be tested that might complete biomechanical and physiological analyses otherwise be untestable. Third, invertebrates exemplify have been made. the Krogh principle: “For many problems there is an To provide a more quantitative comparison, I have animal on which it can be most conveniently studied” extracted numerous values from the literature. The (332). The relative simplicity and ease of manipulation data selection process was extremely difficult, and of invertebrate systems are assets. For example, some nearly each point can be disputed by some criteria. I insect muscles are innervated by a single nerve that err on the inclusive side. I accepted data unless there produces an electromyographic (EMG) signal with a was an undisputed, independent reason for not includ- single spike. An isolated muscle preparation can func- ing them. In this way, future investigators can more tion aerobically for long periods of time if the trachea easily find particular studies and provide their own are intact since the circulatory system is not required evidence to reject or corroborate the general relation- for oxygen delivery. In a more practical vein, inverte- ships presented here derived from the data sets. brates are often easily attainable and inexpensive to Discussion at nearly any level will be introductory purchase and house. Because of their size, they occupy to the experts and too advanced for those from other little space. One can have a muscle physiology, whole- fields. I apologize to the experts and suggest some animal exercise physiology, and biomechanics labora- extraordinary books and reviews as a general introduc- tory in a single room. Fourth, invertebrates are excel- tion to invertebrate locomotion for fresh minds (10, lent systems for the direct study of the evolution of 11, 14, 16, 17, 19, 66, 166, 221, 232, 258, 286, 315, locomotor traits. Many have short generation times. 357, 406, 472, 485, 489). Genetic manipulations of muscle structure and function After a survey of the different mechanisms used FIG. 12.1. Schematic diagram showing integration of comparative bioenergetics, exercise physiology, functional morphology, muscle physiology, and comparative biomechanics. A: Energy available from several sources is transduced to segments (appendages or body sections) through muscles, depending on geometry. The chapter is organized in sections from right to left. B: Magnification of musculoskele- tal role in transducing energy. Musculoskeletal parameters determine musculoskeletal forces. Musculo- skeletal forces and joint geometry determine moment. Moment gives rise to acceleration, velocity, and angle change. Velocity and angle change (change in muscle length) feedback to affect musculoskeletal force production. Moment and joint angular velocity determine amount of energy transferred. Direction of movement and moment determine whether energy enters, leaves, or is transferred from a segment. Segmental energy and morphology of all segments determine power output of whole body and represent locomotor mechanical energy in A. 856 HANDBOOK OF