Sand crab digging; the neuroethology and evolution of a "new" behaviour by Zen Faulkes Bachelor of Arts and Science (B.Sc.) University of Lethbridge, 1989 A dissertation submitted in partial fulfilment of the requirements for the degree of DOCTOR OF PHILOSOPHY in the Department of Biology We accept this dissertation as conforming to the required standard: Dorothy H. Paul, Supervisor (Department of Biology) George O. Mackie, Departmental Member (Department of Biology) Craig Hawryshyn, Departmental Member (Department of Biology) Geraldine Outside Men^éei'^epartment of Physical Education) enJal Examiner (MariAJoseph L. Ayers, ExternalenJal Examiner Examiner (Marine (MariAJoseph Science Center, Northeastern University) Copyright © 1996 Zen Faulkes University of Victoria All rights reserved. This dissertation may not be reproduced in whole or in part, by photocopying or other means, without the permission of the author. Supervisor: Dorothy H. Paul ABSTRACT Sand crabs (Anomura: Hippoidea) have evolved a “new” means of locomotion: they use their thoracic legs to dig into the sand instead of walking on the benthos as many other decapod crustaceans do. I examined digging by three sand crab species of two families, Blepharipoda occidentalis (Albuneidae), Lepidopa califomica (Albuneidae) and Emerita analoga (Hippidae). There are several features common to both sand crab families, suggesting that digging has evolved only once in the sand crabs. The leg tip trajectories are similar, with leg 4 circling in the opposite direction to legs 2 and 3 when viewed from the side; contralateral legs tend to alternate; the “tail” (abdomen in albuneids; uropods in hippids) cycles at higher frequencies than the legs; and the inteijoint coordination of a single given leg (e.g., leg 2) is similar in B. occidentalis and E. analoga. There are also features that distinguish the two families. During digging by the albuneids, serially homologous contralateral legs initially alternate, but switch midway through a digging episode to moving synchronously. In E. analoga, the legs 2 and 3 move in bilateral alternation throughout the dig, but the legs 4 can move in bilateral synchrony and a higher frequency than legs 2 and 3 (» the uropods’ frequency). There are also some similarities between sand crab digging and walking by other decapods, suggesting the two behaviours may be homologous. The coordination of ipsilateral legs on one side of an animal is generally similar in digging and closely related walking species, and there are no obvious differences in the distal leg motor neurons in sand crabs and some walking species. Digging and walking differ in that there are rapid “tail” movements during digging but not Ill walking, and that serially homologous digging legs are more specialised in their motor output than walking legs. The inteijoint coordination of legs 2 and 3 resemble backward walking motor patterns by other decapods, whereas that of leg 4 is more similar to forward walking. This suggests that digging is an evolutionary mosaic, comprised of several modified ancestral locomotor behaviours (backward walking in legs 2 and 3, forward walking in leg 4, and tailfiipping). Examiners: Dorothy H. Paul, Supervisor (Department of Biology) George O. Mackie, Departmental Member (Department of Biology) Craig Hawryshyn, Departmental Member (Department of Biology) Geraldine van GyrvoOutside Member (D^paftment--------------------------------------- of Physical Education) Joseph L. Ayers, External/Examiner (Marine Science Center, Northeastern University) IV TABLE OF CONTENTS ABSTRACT............................................................................................................................ii TABLE OF CONTENTS......................................................................................................iv LIST OF TABLES.............................................................................................................. vüi LIST OPnOURES............................................................................................................... ix LIST OF ABBREVIATIONS.............................................................................................. xii ACKNOWLEDGEMENTS.................................................................................................xiv DEDICATION......................................................................................................................xv Chapter 1 ; Exposition ............................................................................................................. 1 The Animais. ...................................................................................................................... / Sand crab natural history ........................................................................................................................................7 Survival value of digging ........................................................................................................................................7 Ontogeny of digging ...............................................................................................................................................8 Sand crab fossil record ...........................................................................................................................................8 The Problem......................................................................................................................9 Homology: definitions and difficulties ...................................................................................................................9 Homologies and behaviour ...................................................................................................................................11 The Techniques. ...............................................................................................................12 Eshkol-Wachman movement notation (EW) ......................................................................................................... 12 Electromyograms (EMGs) .................................................................................................................................... 14 Overview......................................................................................................................... 15 Chapter 2: Interleg coordination ...........................................................................................17 Introduction.....................................................................................................................17 M ethods........................................................................................................................... 18 Data treatment..................................................................................................................................................... 20 Results............................................................................................................................. 21 Tip trajectories ..................................................................................................................................................... 21 Speed .................................................................................................................................................................... 33 Ipsilateral coordination .........................................................................................................................................36 Munida quadrispina ........................................................................................................................................36 Blepharipoda occidentalis.............................................................................................................................. 36 Lepidopa califomica.......................................................................................................................................37 Emerita analoga ............................................................................................................................................. 37 V Bilateral coordination ........................................................................................................................................... 47 Blepharipoda occidentalis and Lepidopa califomica.................................................................................... 47 Perturbations in bilateral coordination caused by leg loss .........................................................................54 Emerita analoga ..............................................................................................................................................58 Discussion........................................................................................................................67 Homology and divergence in sand crab digging ................................................................................................... 67 Evolutionary origins for digging .......................................................................................................................... 68 Central control ......................................................................................................................................................69 Sensory input .......................................................................................................................................................