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The Neuroethology of Predation and Escape

The Neuroethology of Predation and Escape

Keith T. Sillar, Laurence D. Picton, William J. Heitler

ISBN: 978-1-118-52706-1

Feb 2016

392 pages

Description

The forces of natural selection have been a primary driver in the evolution of adaptive animal behaviours. On the one hand animals must evade predation in order to survive and pass on their genes; on other hand, and for the same underlying reasons, animals must also be capable of successfully capturing prey. This situation has led to an evolutionary arms race in which predator and prey are locked in the battle to survive. A common strategy in each situation is to enhance the speed of response, resulting in the evolution of neural, muscular and biomechanical designs that produce supremely fast and eye-catching behavioral responses.

The aim of this book is to illuminate the design principles of escape and predatory behaviours using a series of case histories from different animal groups and to emphasize the convergent evolution of neural circuitry that optimizes the chances of survival. Using these case histories the authors describe sensory mechanisms that aid prey and predator detection, central neural circuit designs that increase speed of response and neuromuscular and biomechanical properties that aid the performance of escape and predatory movements.

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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