Mimicry, Crypsis, Masquerade and other Adaptive Resemblances

Deals with all aspects of adaptive resemblance

• Full colour
• Covers everything from classic examples of Batesian, Mullerian, aggressive and sexual mimicries through to human behavioural and microbial molecular deceptions
• Highlights areas where additonal work or specific exeprimentation could be fruitful
• Includes, animals, plants, micro-organisms and humans

Preface, xiii

A comment on statistics, xv

A comment on scientific names, xvi

Acknowledgements, xvii

1 INTRODUCTION AND CLASSIFICATION OF MIMICRY SYSTEMS, 1

A brief history, 2

On definitions of ‘mimicry’ and adaptive resemblance, 3

The concept of ‘adaptive resemblance’, 8

The classification of mimicry systems, 9

Wickler’s system, 9

Vane‐Wright’s system, 10

Georges Pasteur (1930–2015), 11

Other approaches, 13

Endler, 13

Zabka & Tembrock, 13

Maran, 14

Mimicry as demonstration of evolution, 14

2 CAMOUFLAGE: CRYPSIS AND DISRUPTIVE COLOURATION IN ANIMALS, 19

Introduction, 20

Distinguishing crypsis from masquerade, 20

Crypsis examples, 24

Countershading, 24

Experimental tests of concealment by countershading, 27

Bioluminescent counter‐illumination, 28

Background matching, 29

Visual sensitivity of predators, 30

To make a perfect match or compromise, 31

Colour polymorphism, 32

Seasonal colour polymorphism, 32

Butterfly pupal colour polymorphism, 32

Winter pelage: pelts and plumage, 35

Melanism, 37

Industrial melanism, 37

Fire melanism, 40

Background selection, 41

Orientation and positioning, 43

Transparency, 45

Reflectance and silvering, 47

Adaptive colour change, 49

Caterpillars and food plant colouration, 50

Daily and medium‐paced changes, 54

Rapid colour change, 56

Chameleons, 56

Cephalopod chromatophores and dermal papillae, 57

Bird eggs and their backgrounds, 58

Disguising your eyes, 61

Disruptive and distractive markings, 61

Edge‐intercepting patches, 61

Distractive markings, 63

Zebra stripes and tsetse flies, 66

Stripes and motion dazzle – more zebras, kraits and tigers, 69

Computer graphics experiments with human subjects, 69

Observations on real animals, 69

Comparative analysis, 71

Dual signals, 72

Protective crypsis in non‐visual modalities, 73

Apostatic and antiapostatic selection, 73

Search images, 74

Experimental tests of search image, 76

Gestalt perception, 76

Effect of cryptic prey variability, 77

Reflexive selection and aspect diversity, 77

Searching for cryptic prey – mathematical models, 80

Ontogenetic changes and crypsis, 81

Hiding the evidence, 82

Petiole clipping by caterpillars, 82

Exogenous crypsis, 82

Military camouflage and masquerade, 85

3 CAMOUFLAGE: MASQUERADE, 87

Introduction, 88

Classic examples, 88

Twigs as models, 88

Leaves (alive or dead) as models, 88

Bird dropping resemblances, 89

Spider web stabilimenta, 93

Tubeworms, etc., 94

Experimental tests of survival value of masquerade, 94

Ontogenetic changes and masquerade, 97

Thanatosis (death feigning), 97

Feign or flee? The trade‐offs of thanatosis, 100

Other aspects of death mimicry, 100

Seedless seeds and seedless fruit, 100

4 APOSEMATISM AND ITS EVOLUTION, 103

Introduction, 104

Initial evolution of aposematism, 108

Associations of unpalatable experience with place, 109

Mathematical models and ideas of warning colouration evolution, 112

Kin selection models, 112

Green beard selection, 112

Family selection models, 113

Individual selection models, 113

Spatial models and metapopulations, 116

Handicap and signal honesty, 117

Early warnings – reflex bleeding, vomiting and other noxious secretions, 120

Longevity of aposematic protected taxa, 121

Macroevolutionary consequences, 121

Experimental studies, 121

Tough aposematic prey and individual selection, 121

Pyrazine and other early warnings, 123

Learning and memorability, 124

Strength of obnoxiousness, 126

Is the nature of the protective compound important?, 126

Neophobia and the role of novelty, 127

Innate responses of predators, 130

Aposematism and gregariousness, 132

Phylogenetic analysis of aposematism and gregariousness, 134

Behaviour of protected aposematic animals, 135

Of birds and butterflies, 135

Evolution of sluggishness, 139

Origins of protective compounds, 140

Plant‐derived toxins, 140

Cardiac glycosides, 141

Pyrrolizidine alkaloids, 144

De novo synthesis of protective compounds, 145

Obtaining toxins from animal sources, 147

Costs of chemical defence, 149

Aposematism with non‐chemical defence, 150

Escape speed and low profitability, 150

Parasitoids and aposematic insects, 152

Diversity of aposematic forms, 152

Egg load assessment, 154

Proof of aposematism, 154

Bioluminescence as a warning signal, 155

Warning sounds, 155

Warning colouration in mammals, 157

Weapon advertisement, 158

Mutualistic aposematism, 160

Aposematism induced by a parasite, 161

Aposematic commensalism, 161

Polymorphism and geographic variation in aposematic species, 161

Aposematism in plants, 163

Synergistic selection of unpalatability in plants, 165

Aposematism in fungi, 166

Why are some unpalatable organisms aposematic and others not?, 167

5 ANTI‐PREDATOR MIMICRY. I. MATHEMATICAL MODELS, 171

Introduction, 172

Properties of models, rewards, learning rates and numerical relationships, 172

Simple models and their limitations, 173

Muller’s original model, 173

Simple models of Batesian and Mullerian mimicry, 173

Are Batesian and Mullerian mimicry different?, 174

An information theory model, 176

Monte‐Carlo simulations, 177

More refined models – time, learning, forgetting and sampling, 180

Importance of alternative prey, 181

Signal detection theory, 181

Genetic and evolutionary models, 182

Coevolutionary chases, 185

Models involving population dynamics, 185

Neural networks and evolution of Batesian mimicry, 188

Automimicry in Batesian/Mullerian mimicry, 188

Predator’s dilemma with potentially harmful prey, 190

6 ANTI‐PREDATOR MIMICRY. II. EXPERIMENTAL TESTS, 191

Introduction, 192

Experimental tests of mimetic advantage, 192

How similar do mimics need to be?, 194

Is a two‐step process necessary?, 198

Relative abundances of models and mimics in nature, 198

Sex‐limited mimicries and mimetic load, 198

Mimetic load, 203

Apostatic selection and Batesian mimicry, 204

Mullerian mimicry and unequal defence, 204

Imperfect (satyric) mimicry, 206

7 ANTI‐PREDATOR MIMICRY. III. BATESIAN AND MULLERIAN EXAMPLES, 213

Introduction, 214

Types of model, 214

Mimicry of slow flight in butterflies, 214

The Batesian/Mullerian spectrum, 215

Famous butterflies: ecology, genetics and supergenes, 216

Heliconius, 216

Hybrid zones, 217

Wing pattern genetics, 219

Modelling polymorphism, 220

Danaus and Hypolimnas, 220

Papilio dardanus, 221

Papilio glaucus, 223

Papilio memnon, 223

Supergenes and their origins, 223

Mimicry between caterpillars, 224

Some specific types of model among insects, 225

Wasp (and bee) mimicry, 225

How to look like a wasp, 228

Time of appearance of aculeate mimics, 228

Pseudostings and pseudostinging behaviour, 230

Wasmannian (or ant) mimicry, 231

Ant mimicry as defence against predation, 231

Ant mimicry by spiders, 234

Spiders that feed on ants, 236

How to look like an ant or an ant carrying something?, 236

Myrmecomorphy by caterpillars, 237

Ant chemical mimicry by parasitoid wasps, 237

Protective mimicries among vertebrates, 239

Fish, 239

Batesian mimicry among fish, 239

Mullerian mimicry among fish, 239

Batesian and Mullerian mimicry among terrestrial vertebrates, 239

The coral snake problem – Emsleyan (or Mertensian) mimicry, 240

Other snakes, zig‐zag markings and head shape, 244

Mimicry of invertebrates by terrestrial vertebrates, 246

Inaccurate (satyric) mimics, 248

Mimicry of model behaviour, 249

Aide mémoire mimicry, 250

Batesian–Poultonian (predator) mimicry, 251

Mimicry within predator–prey and host–parasite systems, 253

Bluff and appearing larger than you are, 253

Collective mimicry including an aggressive mimicry, 255

Jamming, 255

Man as model – the case of the samurai crab, 258

8 ANTI‐PREDATOR MIMICRY. ATTACK DEFLECTION, SCHOOLING, ETC., 259

Introduction, 260

Attack deflection devices, 260

Eyespots, 260

Experimental tests of importance of eyespot features, 262

Eyespots in butterflies, 266

Wing marginal eyespots, 267

Eyes with sparkles, 267

Eyespots on caterpillars, 269

Importance of eyespot conspicuousness, 269

Eyespots and fish, 269

Not just an eyespot but a whole head, winking and other enhancements, 271

Reverse mimicry, 271

Insects, 271

Reverse mimicry in flight, 275

Reverse mimicry in terrestrial vertebrates, 275

Other deflectors, 277

Injury feigning in nesting birds, 277

Tail‐shedding (urotomy) in lizards and snakes, 277

Flash and startle colouration, 280

Intimidating displays and bizarre mimicries, 283

Schooling, flocking and predator confusion, 284

‘Social’ mimicry in birds and fish, 286

Alarm call mimicry for protection, 287

9 ANTI‐HERBIVORY DECEPTIONS, 289

Introduction, 290

Crypsis as protection in plants, 290

Leaf mottling and variegation for crypsis, 291

Mistletoes and lianas, 293

Fruit masquerade by leaves, 294

Protective Batesian and Mullerian mimicry in plants, 295

False indicators of damage or likely future damage, 296

Conspicuousness of leafmines, 297

Dark central florets in some Apiaceae, 297

Mimicry of silk or fungal hyphae, 299

Insect egg mimics, 299

Defensive aphid and caterpillar mimicry in plants, 300

Aphid deterrence by alarm pheromone mimicry, 300

Ant mimicry in plants, 301

Of orchids and bees, 301

Carrion mimicry as defence, 302

Algae and corals, 302

Plant galls, 302

Experimental evidence for plant aposematism and Batesian mimetic potential in plants, 302

10 AGGRESSIVE DECEPTIONS, 305

Introduction, 306

Cryptic versus alluring features, 307

Crypsis and masquerade by predators, 307

Stealth, 307

Shadowing, 308

Seasonal polymorphisms in predators, 308

Why seabirds are black and white (and grey), 309

Chemical crypsis by a predatory fish, 309

Alluring mimicries, 310

Flower mimicry, 312

Rain mimicry, 315

Physical lures, 315

Angling fish, 315

Caudal (and tongue) lures in reptiles, 317

Caudal lure in a dragonfly, 318

Death feigning as a lure, 318

Other prey and food mimicry, 319

The case of the German cockroach, 319

Wolves in sheeps’ clothing, 319

Vulture‐like hawks, 319

Cleaner fish and their mimics, 320

Mingling with an innocuous crowd, 322

Duping by mimicry of competitors, 323

Seeming to be conspecific, 324

Getting close, 325

Appearing to be a potential mate, 325

Pheromone lures, 326

Mimicking danger as a flushing device, 328

Human use of aggressive mimicry, 328

Cuckoldry, inquilines and brood parasitism, 329

Cuckoldry in birds, 329

Gentes and ‘cuckoo’ eggs, 332

Cues for egg rejection, 335

Mimicry by chicks – genetic and substantive differences, 338

Cuckoo chick appearance, 338

Begging calls, 339

Cuckoo and host coevolution, 340

Mimicry between adult cuckoos and their hosts, 340

Hawk mimicry by adult cuckoos, 340

Mimicry of harmless birds by adult cuckoos, 342

Brood parasitism and inquilinism in social insects, 342

Cuckoo bees and cuckoo wasps, 342

Kleptoparasites of bees, 346

Myrmecophily, 346

Acquired chemical mimicry in social parasites and inquilines, 346

Brood‐parasitic and slave‐making ants, 348

Chemical mimicry and ant and termite inquilines, 349

A brood‐parasitic aphid, 349

Ants and aphid trophallaxis, 349

Aphidiine parasitoids of ant‐attended aphids, 350

Does aggressive mimicry occur in plants?, 350

11 SEXUAL MIMICRIES IN ANIMALS (INCLUDING HUMANS), 353

Introduction, 354

Mimicking the opposite sex, 354

Female mimicry by males, 354

Avoiding aggression from competing males, 357

Mate guarding through distracting other males, 357

Androchromatism and male mimicry by females, 358

Egg dummies on fish, 360

Food dummies and sex, 362

Mimicry by sperm‐dependent all‐female lineages, 363

Female genital mimicry in a female, 363

Energy‐saving cheating for sex, 364

Behavioural deceptions in higher vertebrates, 364

Polygynous birds, 364

Deceptive use of alarm calls and paternity protection, 365

Female–female mounting behaviour in mammals and birds, 365

Mimicry in humans, 367

Make‐up, clothes and silicone, 367

Cryptic oestrus in humans, 368

Flirting in humans, 368

12 REPRODUCTIVE MIMICRIES IN PLANTS, 371

Introduction, 372

Pollinator deception, 372

Pollinator sex pheromone mimicry, 376

Food deception, 382

Specific floral mimicry, 382

Generalised floral mimicry, 386

Mimicry of a fungus‐infected plant, 388

Brood‐site/oviposition‐site deception, 388

Shelter mimicry, 392

Flower similarity over time, 392

Flower automimicry – intraspecific food deception (bakerian mimicry), 393

Mathematical modelling of sexual deception by plants, 394

Pollinator guild syndromes, 394

Bird‐pollinated systems, 394

13 INTRA‐ AND INTERSPECIFIC COOPERATION, COMPETITION AND HIERARCHIES, 399

Introduction, 400

Remaining looking young, 400

Delayed plumage maturation, 400

Interspecific social dominance mimicry, 401

Bird song and alarm call mimicry – deceptive acquisition of resources, 401

Wicklerian mimicry – mimicry of opposite sex to reduce aggression, 403

Female resemblance in male primates, 403

Social appeasement by female mimicry in an insect, 404

Hyperfemininity in prereproductive adolescent primates, 404

Mimicry of male genitalia by females, 404

The case of the spotted hyaena, 404

Mimicry of male genitalia in other mammals, 404

Phallic mimicry by males, 405

Appetitive (foraging) mimicry, 406

Appetitive mimicry and deceptive use of alarm calls, 406

Beau Geste and seeming to be more than you are, 408

Appearing older than you are, 408

Weapon automimicry, 408

14 ADAPTIVE RESEMBLANCES AND DISPERSAL: SEEDS, SPORES AND EGGS, 409

Introduction, 410

Fruit and seed dispersal by birds, 410

Warningly coloured fruit, 414

Fruit mimicry by seeds, 414

Seed dispersal by humans, arable weeds and Vavilovian mimicry, 414

Seed elaiosomes and their insect mimics, 415

Mimicry by parasites to facilitate host finding, 415

The trematode and the snail, 415

The trematode and the fish, 416

Pocketbook clams and fish, 416

‘Termite balls’, 417

Pseudoflowers, pseudo‐anthers and pseudo‐pollen, 417

Truffles, 418

Mimicry of dead flesh by fungi and mosses, 419

Deception of dung beetles by fruit, 419

15 MOLECULAR MIMICRY: PARASITES, PATHOGENS AND PLANTS, 421

Introduction, 422

Macro‐animal systems, 422

Anemone fish, 422

Parasitic helminthes, 422

Platyhelminthes (Trematoda), 422

Tapeworms (Platyhelminthes: Cestoda), 423

Parasitic nematodes, 423

Parasitoid wasp eggs, 424

Pathogenic fungi, 424

Protista, 424

Chagas’ disease, 424

Microbial systems, 424

Bacterial chemical mimicry and autoimmune responses, 424

Helicobacter pylori, 425

Campylobacter jejuni, 425

Mimicry by plant‐pathogenic bacteria, 425

Viruses, 425

Plants, 425

Sugar, toxin and satiation mimicry, 425

Phytoecdysteroids – plant chemicals that mimicinsect moulting hormone, 427

Plant oestrogens – phyto‐contraceptives, 427

Extended glossary, 429

References, 445

Author index, 515

General index, 533

Taxonomic index, 539

Donald L.J. Quicke retired in 2013 to live in Thailand where he is a Visiting Professor at Chulalongkorn University. Hestudied zoology at Oxford University where he became especially interested in mimicry. In 1976 he travelled to Kenya to experience tropical biodiversity and more of the diversity of life and his work there on insect coloration fertilised his interests as well as on parasitoid wasps, another of his many passions. From then on he kept abreast of the increasingly experimental and theoretical developments in the field even though his academic research took him in diverse other directions. Having now retired he has been able devote his time, in addition to bird watching and butterfly photography, to synthesising and extending his interest in this topic. Mimicry, Crypsis, Masquerade and other Adaptive Resemblances is the result of this work.

Mimicry, Crypsis, Masquerade and other Adaptive Resemblances synthesises the wide range of adaptations of living organisms that are the result of natural selection favouring an appearance that resembles some other organism or inanimate object. The book covers a wide range of examples, most from animals and plants, but fungi, protists, bacteria and even viruses, are discussed, and even some human aspects are included to illustrate the enormous range of the topic. Many different modalities of resemblance are involved, such as behavour, coloration, shading, texture, bioluminescence, structure, chemistry and sound. The author explores the results of the growing number of experimental tests that have been conducted in the field, explaining key models and experimental set-ups in an accessible manner.

The book is beautifully illustrated in full colour throughout with hundreds of photos of animals and plants, but also includes many graphs that illustrate research findings, and some mathematical equations and models that explore and explain the depths of evolution's complexities. Mimicry, Crypsis, Masquerade and other Adaptive Resemblances:

• Covers everthing including classic examples of animal and plant camouflage, the evolution of warning signals, Batesian, Müllerian, aggressive, and sexual mimicries
• Extends to some human behavioural and microbial molecular deceptions, plus many other topics
• Highlights areas where additional work or specific experimentation could be fruitful
• Includes over 500 images to aid understanding

This book is far more than a course text, for which it is ideal for levels ranging through undergraduate to graduate levels, it is the most comprehensive resource on this diverse subject area for many years. It is written in a way that can be understood easily by all readers including amateur natural history enthusiasts.