Markerless tracking suggests a tactile sensing role for forelegs of Dolomedes spiders during locomotion

Summary statement We developed a machine vision technique for markerless tracking of locomotion in the spider Dolomedes aquaticus. Gait analysis suggests that each pair of legs plays a specific role in locomotion. Abstract Because of their rigid exoskeleton with relatively simple joint mechanics, arthropods can provide useful models for studying the sensory-neural and mechanical design principles of agile animal locomotion. Gait analysis usually requires attaching markers or manually identifying reference points in video frames, which can be time consuming and inaccurate, especially with small animals. Here we describe a markerless motion capture technique and its application to gait analysis in the New Zealand semi-aquatic hunting spider, Dolomedes aquaticus. Our machine vision approach uses a model of the spider’s skeleton to infer the location of the centre of mass and the configuration of the skeleton in successive video frames. We found that stride length and frequency are correlated with running speed. Inter-limb coordination during the gait cycle suggests that different legs have specialized roles in locomotion. Phase relationships among the six hindmost legs exhibit an alternating tripod gait, as in hexapod insects. The middle two leg pairs appear to be primarily responsible for generating thrust, while the hind legs contribute more to stability. The front legs are not phase-coupled to the other legs and appear to be used as tactile probes during locomotion. Our machine vision approach has the potential to automate arthropod gait analysis, making it faster and easier. Our results indicate how specialization of limb function may contribute to locomotor efficiency and agility of a specialized hunting spider, and how arthropod design principles may contribute to developing efficient, agile legged robots.

[1]  J. Shultz,et al.  Walking and Surface Film Locomotion in Terrestrial and Semi-Aquatic Spiders , 1987 .

[2]  R. S. Wilson,et al.  The hydraulic interaction between prosoma and opisthosoma in Amaurobius ferox (Chelicerata, Araneae) , 1973, Zeitschrift für Morphologie der Tiere.

[3]  Hans-Peter Seidel,et al.  Motion capture using joint skeleton tracking and surface estimation , 2009, 2009 IEEE Conference on Computer Vision and Pattern Recognition.

[4]  Benjamin L. de Bivort,et al.  Ethology as a physical science , 2018, Nature Physics.

[5]  C. CHRISTOPHER AMAYA,et al.  The Effects of Leg Autotomy on Running Speed and Foraging Ability in Two Species of Wolf Spider, (Lycosidae) , 2001 .

[6]  Pushmeet Kohli,et al.  PoseCut: Simultaneous Segmentation and 3D Pose Estimation of Humans Using Dynamic Graph-Cuts , 2006, ECCV.

[7]  William Bialek,et al.  Mapping the stereotyped behaviour of freely moving fruit flies , 2013, Journal of The Royal Society Interface.

[8]  Emiliano Gambaretto,et al.  Markerless motion capture: the challenge of accuracy in capturing animal motions through model based approaches , 2009, Optical Engineering + Applications.

[9]  R. F. Bowerman,et al.  The control of arthropod walking. , 1977, Comparative biochemistry and physiology. A, Comparative physiology.

[10]  Volker Dürr,et al.  Motion analysis using stochastic optimisation and posture disambiguation , 2005 .

[11]  D. A. Parry,et al.  Spider Leg-muscles and the Autotomy Mechanism , 1957 .

[12]  D. Greig,et al.  Exact Maximum A Posteriori Estimation for Binary Images , 1989 .

[13]  R. S. Wilson Some comments on the hydrostatic system of spiders (Chelicerata, Araneae) , 2004, Zeitschrift für Morphologie der Tiere.

[14]  Charles R. Fourtner,et al.  Chelicerate Skeletal Neuromuscular Systems , 1973 .

[15]  R. Blickhan,et al.  Cupiennius salei: biomechanical properties of the tibia–metatarsus joint and its flexing muscles , 2010, Journal of Comparative Physiology B.

[16]  Todd D. Levine,et al.  Interactive effects of leg autotomy and incline on locomotor performance and kinematics of the cellar spider, Pholcus manueli , 2017, Ecology and evolution.

[17]  Adrian Hilton,et al.  A survey of advances in vision-based human motion capture and analysis , 2006, Comput. Vis. Image Underst..

[18]  R. H. Brown,et al.  The Hydraulic Mechanism of the Spider Leg , 1959 .

[19]  W. Gerrard Effect of Temperature , 1976 .

[20]  Ugne Klibaite,et al.  An unsupervised method for quantifying the behavior of paired animals , 2016, Physical biology.

[21]  Heinrich Reichert,et al.  GABAergic inhibition of leg motoneurons is required for normal walking behavior in freely moving Drosophila , 2017, Proceedings of the National Academy of Sciences.

[22]  T. M. Ward,et al.  Locomotion in Burrowing and Vagrant Wolf Spiders (Lycosidae) , 1981 .

[23]  A. Minetti,et al.  Biomechanics of octopedal locomotion: kinematic and kinetic analysis of the spider Grammostola mollicoma , 2011, Journal of Experimental Biology.

[24]  J. Spagna,et al.  Gait characteristics of two fast-running spider species (Hololena adnexa and Hololena curta), including an aerial phase (Araneae: Agelenidae) , 2011 .

[25]  Jamon,et al.  Locomotor patterns in freely moving crayfish (Procambarus clarkii) , 1995, The Journal of experimental biology.

[26]  Itai Cohen,et al.  Walking like an ant: a quantitative and experimental approach to understanding locomotor mimicry in the jumping spider Myrmarachne formicaria , 2017, Proceedings of the Royal Society B: Biological Sciences.

[27]  Suter,et al.  Locomotion on the water surface: hydrodynamic constraints on rowing velocity require a gait change , 1999, The Journal of experimental biology.

[28]  Robert F. Bowerman,et al.  The control of walking in the scorpion , 2004, Journal of comparative physiology.

[29]  Jack K. Harris,et al.  The Forces Exerted on the Substrate by Walking and Stationary Crickets , 1980 .

[30]  A. Ruina,et al.  Efficiency, speed, and scaling of two-dimensional passive-dynamic walking , 2000 .

[31]  Lyn M. Forster,et al.  Spiders of New Zealand and Their Worldwide Kin , 2000 .

[32]  Christopher A. Brown,et al.  Between-sex Variation in Running Speed and a Potential Cost of Leg Autotomy in the Wolf Spider Pirata sedentarius , 2005 .

[33]  Robert F. Bowerman,et al.  The morphology and physiology of some walking leg motor neurones in a scorpion , 1980, Journal of comparative physiology.

[34]  Michael Unser,et al.  FlyLimbTracker: An active contour based approach for leg segment tracking in unmarked, freely behaving Drosophila , 2016, bioRxiv.

[35]  Yu Zeng,et al.  Biomechanics of omnidirectional strikes in flat spiders , 2018, Journal of Experimental Biology.

[36]  D. Wilson Insect walking. , 1966, Annual review of entomology.

[37]  Michael H Dickinson,et al.  Wing and body motion during flight initiation in Drosophila revealed by automated visual tracking , 2009, Journal of Experimental Biology.

[38]  Roger D. Santer,et al.  Tactile learning by a whip spider, Phrynus marginemaculatus C.L. Koch (Arachnida, Amblypygi) , 2009, Journal of Comparative Physiology A.

[39]  Vladimir Kolmogorov,et al.  An experimental comparison of min-cut/max- flow algorithms for energy minimization in vision , 2001, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[40]  R. Foelix,et al.  The biology of spiders. , 1987 .

[41]  Vladimir Kolmogorov,et al.  An Experimental Comparison of Min-Cut/Max-Flow Algorithms for Energy Minimization in Vision , 2004, IEEE Trans. Pattern Anal. Mach. Intell..

[42]  Rasmus Larsen,et al.  Analyzing Gait Using a Time-of-Flight Camera , 2009, SCIA.

[43]  R. H. Brown,et al.  The Jumping Mechanism of Salticid Spiders , 1959 .

[44]  Lawrence S. Dillon,et al.  The myology of the araneid leg , 1952 .

[45]  M. Land Stepping movements made by jumping spiders during turns mediated by the lateral eyes. , 1972, The Journal of experimental biology.

[46]  R J Full,et al.  Distributed mechanical feedback in arthropods and robots simplifies control of rapid running on challenging terrain , 2007, Bioinspiration & biomimetics.

[47]  Hans-Peter Seidel,et al.  Motion capture using joint skeleton tracking and surface estimation , 2009, CVPR.

[48]  A. Ahn,et al.  Effect of temperature on leg kinematics in sprinting tarantulas (Aphonopelma hentzi): high speed may limit hydraulic joint actuation , 2015, The Journal of Experimental Biology.

[49]  Jitendra Malik,et al.  Twist Based Acquisition and Tracking of Animal and Human Kinematics , 2004, International Journal of Computer Vision.

[50]  R. Blickhan Stiffness of an arthropod leg joint. , 1986, Journal of biomechanics.

[51]  Ernst-August Seyfarth,et al.  Heterogeneity of spider leg muscle: Histochemistry and electrophysiology of identified fibers in the claw levator , 1987, Journal of Comparative Physiology B.

[52]  G. M. Hughes The Co-Ordination of Insect Movements I The Walking Movements of Insects , 1952 .

[53]  Stacia B. Moffett,et al.  Alteration of locomotor behavior in wolf spiders carrying normal and weighted egg cocoons , 1980 .

[54]  R. Blickhan,et al.  Strains in the exoskeleton of spiders , 2004, Journal of Comparative Physiology A.

[55]  J. Shultz,et al.  Evolution of locomotion in arachnida: The hydraulic pressure pump of the giant whipscorpion, Mastigoproctus Giganteus (Uropygi) , 1991, Journal of morphology.

[56]  M G Paulin,et al.  An upper-body can improve the stability and efficiency of passive dynamic walking. , 2011, Journal of theoretical biology.

[57]  R. Full,et al.  Mechanics of a rapid running insect: two-, four- and six-legged locomotion. , 1991, The Journal of experimental biology.

[58]  T. Weihmann Crawling at High Speeds: Steady Level Locomotion in the Spider Cupiennius salei—Global Kinematics and Implications for Centre of Mass Dynamics , 2013, PloS one.

[59]  R J Full,et al.  How animals move: an integrative view. , 2000, Science.

[60]  A. Sensenig,et al.  MECHANICAL ENERGY OSCILLATIONS DURING LOCOMOTION IN THE HARVESTMAN LEIOBUNUM VITTATUM (OPILIONES) , 2006 .

[61]  Neill W. Campbell,et al.  Quadruped gait analysis using sparse motion information , 2003, Proceedings 2003 International Conference on Image Processing (Cat. No.03CH37429).

[62]  H. Cruse The function of the legs in the free walking stick insect,Carausius morosus , 1976, Journal of comparative physiology.

[63]  Marie-Paule Cani,et al.  Animal gaits from video: Comparative studies , 2006, Graph. Model..

[64]  Roy E. Ritzmann,et al.  Computer-Assisted 3D Kinematic Analysis of All Leg Joints in Walking Insects , 2010, PloS one.

[65]  C. H. Ellis THE MECHANISM OF EXTENSION IN THE LEGS OF SPIDERS , 1944 .

[66]  M. Rieu,et al.  Morphology and physiology , 2005, Experientia.

[67]  Donald M. Wilson Stepping Patterns in Tarantula Spiders , 1967 .

[68]  Marie-Paule Cani,et al.  Animal gaits from video , 2004, SCA '04.

[69]  J. Anderson,et al.  The fluid pressure pumps of spiders (Chelicerata, Araneae) , 1975, Zeitschrift für Morphologie der Tiere.

[70]  Jonathan Reiskind,et al.  Ant-Mimicry in Panamanian Clubionid and Salticid Spiders (Araneae: Clubionidae, Salticidae) , 1977 .

[71]  Stefan Reußenzehn,et al.  Mechanical design of the legs of Dolomedes aquaticus - Novel approaches to quantify the hydraulic contribution to joint movement and to create a segmented 3D spider model , 2010 .

[72]  Nicholas I. Fisher,et al.  Statistical Analysis of Circular Data , 1993 .

[73]  Heinrich Reichert,et al.  GABAergic inhibition of leg motoneurons is required for normal walking behavior in freely moving Drosophila , 2017 .

[74]  HiltonAdrian,et al.  A survey of advances in vision-based human motion capture and analysis , 2006 .

[75]  Robert F. Bowerman,et al.  An electrophysiological survey of joint receptors in the walking legs of the scorpion,Paruroctonus mesaensis , 1976, Journal of comparative physiology.

[76]  Torsten Bumgarner,et al.  Biomechanics and Motor Control of Human Movement , 2013 .