The Neuroethology of Predation and Escape

THE NEUROETHOLOGY OF PREDATION AND ESCAPE To eat and not get eaten is key to animal survival, and the arms race between predators and prey has driven the evolution of many rapid and spectacular behaviours. This book explores the neural mechanisms controlling predation and escape, where specialisations in afferent pathways, central circuits, motor control and biomechanics can be traced through to natural animal behaviour. Each chapter provides an integrated and comparative review of case studies in neuroethology. Ranging from the classic studies on bat biosonar and insect counter-measures, through to fish-eating snails armed with powerful neurotoxins, the book covers a diverse and fascinating range of adaptations. Common principles of biological design and organization are highlighted throughout the text. The book is aimed at several audiences: for lecturers and students. This synthesis will help to underpin the curriculum in neuroscience and behavioural biology, especially for courses focusing on neuroethology for postgraduate students. The sections devoted to your area of specialism will give a flying start to your research reading, while the other chapters offer breadth and insights from comparative studies for academic researchers. The book will provide a valuable resource and an enjoyable read Above all, we hope this book will inspire the next generation of neuroethologists.

Table of Contents:
General Introduction xi What This Book Is About xiii How this book is organised xv Who this book is for xvi Acknowledgements xvi References xvii 1 Vision 2 1.1 The electromagnetic spectrum 3 1.2 Eyes: acuity and sensitivity 5 1.2.1 Foveae 6 1.3 Feature recognition and releasing behaviour 8 1.4 Prey capture in toads 9 1.4.1 Attack or avoid: ‘worms’ and ‘anti‐worms’ 9 1.4.2 Retinal processing 11 1.4.3 Feature detector neurons 12 1.4.4 Modulation and plasticity 14 1.4.5 Toad prey capture: the insects fight back 15 1.5 Beyond the visible spectrum 16 1.5.1 Pit organs 16 1.5.2 Thermotransduction 20 1.5.3 Brain processing and cross‐modal integration 21 1.5.4 Behaviour 22 1.5.5 Infrared defence signals 25 1.6 Aerial predators: dragonfly vision 27 1.6.1 Dragonfly eyes 27 1.6.2 Aerial pursuit 28 1.6.3 Predictive foveation 29 1.6.4 Reactive steering: STMDs and TSDNs 30 1.7 Summary 31 Abbreviations 32 References 32 2 Olfaction 36 2.1 Mechanisms of olfaction 38 2.1.1 Detection and specificity 38 2.1.2 Olfactory sub‐systems 40 2.1.3 Brain processing 41 2.2 Olfactory tracking and localisation 41 2.3 Pheromones and kairomones 45 2.3.1 Alarm pheromones 45 2.3.2 Predator odours 46 2.3.3 Dual purpose signals: the MUP family 47 2.3.4 Parasites: when kairomones go bad! 49 2.4 Summary 50 Abbreviations 51 References 51 3 Owl Hearing 54 3.1 Timing and intensity 56 3.2 Owl sound localisation mechanisms 58 3.3 Anatomy 60 3.4 Neural computation 61 3.4.1 The auditory map 62 3.4.2 Early stage processing 66 3.4.3 ITD processing 69 3.4.4 IID processing 76 3.5 Combining ITD and IID specificity in the inferior colliculus 77 3.6 Audio‐visual integration and experience‐dependent tuning of the auditory map 78 3.6.1 Audio‐visual discrepancy can re‐map the ICC‐ICX connections 80 3.6.2 Motor adaptation 82 3.6.3 Age and experience matter! 82 3.6.4 Cellular mechanisms of re‐mapping 82 3.7 Summary 83 Abbreviations 84 References 85 4 Mammalian Hearing 88 4.1 Spectral cues 90 4.1.1 Neural processing of spectral cues 90 4.2 Binaural processing 92 4.2.1 IID processing 93 4.2.2 ITD processing 94 4.2.3 Calyx of Held 99 4.3 Do mammals have a space map like owls? 100 4.4 Comparative studies in mammals 101 4.5 Summary 102 4.5.1 Caveats 102 Abbreviations 102 References 103 5 The Biosonar System of Bats 106 5.1 Bat echolocation 107 5.1.1 Why ultrasound? 108 5.1.2 Range limits 109 5.2 The sound production system 109 5.2.1 Types of sound: CF and FM pulses 110 5.2.2 Echolocation in predation: a three‐phase attack strategy 112 5.2.3 Duty cycle and pulse‐echo overlap 113 5.3 The sound reception system 114 5.3.1 Bats have big ears 114 5.3.2 Peripheral specialisations: automatic gain control and acoustic fovea 115 5.4 Eco‐physiology: different calls for different situations 116 5.4.1 Target discovery 117 5.4.2 Target range and texture 118 5.4.3 Target location 119 5.4.4 Target velocity: the Doppler shift 119 5.4.5 Target identity: flutter detection 121 5.4.6 Jamming avoidance response 123 5.4.7 Food competition and intentional jamming 123 5.5 Brain mechanisms of echo detection 124 5.5.1 The auditory cortex 125 5.5.2 Range and size analysis: the FM‐FM area 125 5.5.3 Velocity analysis: the CF‐CF area 128 5.5.4 Fine frequency analysis: the DSCF area 130 5.6 Evolutionary considerations 131 5.7 The insects fight back 132 5.7.1 Moth ears and evasive action 132 5.7.2 Bad taste 133 5.7.3 Shouting back 134 5.8 Final thoughts 135 5.9 Summary 136 Abbreviations 137 References 137 6 Electrolocation and Electric Organs 140 6.1 Passive electrolocation 142 6.1.1 Ampullary electroreceptors 142 6.1.2 Prey localisation 145 6.1.3 Mammalian electrolocation 146 6.2 Electric fish 148 6.3 Strongly electric fish 151 6.3.1 Freshwater fish: the electric eel 151 6.3.2 Marine fish: The electric ray 156 6.3.3 Avoiding self‐electrocution 158 6.4 Active electrolocation 158 6.4.1 Weakly electric fish 158 6.4.2 Tuberous electroreceptors 161 6.4.3 Brain maps for active electrolocation 163 6.4.4 Avoiding detection mostly 164 6.4.5 Frequency niches 166 6.4.6 The jamming avoidance response 167 6.5 Summary 174 Abbreviations 175 References 175 7 The Crayfish Escape Tail‐Flip 178 7.1 Invertebrate vs. vertebrate nervous systems 179 7.2 Tail‐flip form and function 180 7.3 Command neurons 182 7.4 Motor output 184 7.4.1 Directional control 184 7.4.2 Rectifying electrical synapses 186 7.4.3 Depolarising inhibition 188 7.4.4 FF drive and the segmental giant neuron 189 7.4.5 Limb activity during GF tail‐flips 189 7.4.6 Tail extension 190 7.4.7 Non‐giant tail‐flips 190 7.5 Activation of GF tail‐flips 191 7.5.1 Coincidence detection 193 7.5.2 Habituation and prevention of self‐stimulation 195 7.6 Modulation and neuroeconomics 196 7.6.1 Mechanisms of modulation 197 7.6.2 Serotonin modulation 198 7.7 Social status, serotonin and the crayfish tail‐flip 198 7.7.1 Social status effects on tail‐flip threshold 199 7.7.2 Serotonin effects on tail‐flip threshold depend on social status 200 7.8 Evolution and adaptations of the tail‐flip circuitry 202 7.8.1 Penaeus: a unique myelination mechanism gives ultra‐rapid conduction 205 7.9 Summary 208 Abbreviations 208 References 209 8 Fish Escape: the Mauthner System 212 8.1 Fish ears and the lateral line 214 8.1.1 Directional sensitivity 215 8.2 Mauthner cells 215 8.2.1 Biophysical properties 217 8.3 Sensory inputs to M‐cells 218 8.3.1 Feedforward inhibition and threshold setting 220 8.3.2 PHP neurons: electrical inhibition 220 8.4 Directional selectivity and the lateral line 222 8.4.1 Obstacle avoidance 223 8.5 M‐cell output 223 8.5.1 Feedback electrical inhibition: collateral PHP neurons 223 8.5.2 Spinal motor output 224 8.5.3 Spinal inhibitory interneurons: CoLos 224 8.6 The Mauthner system: command, control and flexibility 226 8.7 Stage 2 and beyond 230 8.8 Social status and escape threshold 230 8.9 Adaptations and modifications of the M‐circuit 233 8.10 Predators fight back: the amazing tentacled snake 235 8.11 Summary 239 Abbreviations 239 References 240 9 The Mammalian Startle Response 244 9.1 Pathologies 246 9.2 Neural circuitry of the mammalian startle response 248 9.3 Modulation of startle 250 9.4 Summary 250 Abbreviations 251 References 251 10 The Ballistic Attack of Archer Fish 254 10.1 The water pistol 255 10.2 Perceptual problems and solutions 257 10.3 Learning to shoot 260 10.4 Prey retrieval by archer fish 261 10.4.1 Computing the landing point 262 10.4.2 Orientation 263 10.4.3 Dash to the target 264 10.5 Summary 264 References 265 11 Catapults for Attack and Escape 266 11.1 The bow and arrow 268 11.2 Catapults require multi‐stage motor programmes 269 11.3 Grasshopper jumping 270 11.3.1 Biomechanics 270 11.3.2 The behaviour 270 11.3.3 The hind legs 271 11.3.4 The motor programme 273 11.3.5 Directional control 279 11.3.6 Evolution of the grasshopper strategy 279 11.4 Froghoppers: the champion insect jumpers 280 11.4.1 Ratchet locks 282 11.4.2 Synchronisation 282 11.5 Mantis shrimps 284 11.5.1 Mantis shrimp catapults 285 11.5.2 Cavitation bubbles 287 11.6 Snapping (pistol) shrimps 288 11.7 Multi‐function mouthparts: the trap‐jaw ant 291 11.8 Prey capture with prehensile tongues 293 11.8.1 The chameleon tongue: sliding springs and supercontracting muscles 293 11.8.2 Salamander tongue projection 297 11.9 Temperature independence of catapults 300 11.10 Summary 300 Abbreviations 301 References 301 12 Molluscan Defence and Escape Systems 304 12.1 Squid jet propulsion 306 12.1.1 Biomechanics 306 12.1.2 Neural circuitry 307 12.1.3 Jetting behaviour 311 12.2 Inking 312 12.2.1 Neuroecology of inking 314 12.2.2 Neural circuitry of inking 315 12.3 Cephalopod colour and shape control 316 12.3.1 Chromatophores 317 12.3.2 Iridophores 319 12.3.3 Leucophores 321 12.3.4 Photophores 321 12.3.5 Body shape and dermal papillae 322 12.4 Summary 323 Abbreviations 323 References 323 13 Neurotoxins for Attack and Defence 326 13.1 Cone snails 328 13.1.1 The biology of cone snail envenomation 329 13.1.2 Conopeptides 333 13.1.3 The billion dollar mollusc 340 13.1.4 ‘Rapid’ conch escape 341 13.2 The neuroethology of ‘zombie’ cockroaches 343 13.2.1 Sensory mechanisms of stinger precision 344 13.2.2 Transient paralysis 345 13.2.3 Intense grooming 346 13.2.4 Docile hypokinesia 346 13.3 Venom resistance 347 13.3.1 Targeting pain pathways 350 13.3.2 From pain to analgesia 350 13.4 Summary 352 Abbreviations 352 References 352 14 Concluding Thoughts 356 14.1 The need for speed 358 14.2 Safety in numbers 360 14.3 The unbalancing influences of humankind 361 References 363 Index 364

About the Author :
Keith T. Sillar School of Psychology and Neuroscience, University of St Andrews, Scotland, UK Laurence D. Picton School of Psychology and Neuroscience, University of St Andrews, Scotland, UK William J. Heitler School of Biology, University of St Andrews, Scotland, UK