Mimicry, Crypsis, Masquerade and other Adaptive Resemblances

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.

• Preface, xiiiA comment on statistics, xvA comment on scientific names, xviAcknowledgements, xvii1 INTRODUCTION AND CLASSIFICATION OF MIMICRY SYSTEMS, 1A brief history, 2On definitions of ‘mimicry’ and adaptive resemblance, 3The concept of ‘adaptive resemblance’, 8The classification of mimicry systems, 9Wickler’s system, 9Vane‐Wright’s system, 10Georges Pasteur (1930–2015), 11Other approaches, 13Endler, 13Zabka & Tembrock, 13Maran, 14Mimicry as demonstration of evolution, 142 CAMOUFLAGE: CRYPSIS AND DISRUPTIVE COLOURATION IN ANIMALS, 19Introduction, 20Distinguishing crypsis from masquerade, 20Crypsis examples, 24Countershading, 24Experimental tests of concealment by countershading, 27Bioluminescent counter‐illumination, 28Background matching, 29Visual sensitivity of predators, 30To make a perfect match or compromise, 31Colour polymorphism, 32Seasonal colour polymorphism, 32Butterfly pupal colour polymorphism, 32Winter pelage: pelts and plumage, 35Melanism, 37Industrial melanism, 37Fire melanism, 40Background selection, 41Orientation and positioning, 43Transparency, 45Reflectance and silvering, 47Adaptive colour change, 49Caterpillars and food plant colouration, 50Daily and medium‐paced changes, 54Rapid colour change, 56Chameleons, 56Cephalopod chromatophores and dermal papillae, 57Bird eggs and their backgrounds, 58Disguising your eyes, 61Disruptive and distractive markings, 61Edge‐intercepting patches, 61Distractive markings, 63Zebra stripes and tsetse flies, 66Stripes and motion dazzle – more zebras, kraits and tigers, 69Computer graphics experiments with human subjects, 69Observations on real animals, 69Comparative analysis, 71Dual signals, 72Protective crypsis in non‐visual modalities, 73Apostatic and antiapostatic selection, 73Search images, 74Experimental tests of search image, 76Gestalt perception, 76Effect of cryptic prey variability, 77Reflexive selection and aspect diversity, 77Searching for cryptic prey – mathematical models, 80Ontogenetic changes and crypsis, 81Hiding the evidence, 82Petiole clipping by caterpillars, 82Exogenous crypsis, 82Military camouflage and masquerade, 853 CAMOUFLAGE: MASQUERADE, 87Introduction, 88Classic examples, 88Twigs as models, 88Leaves (alive or dead) as models, 88Bird dropping resemblances, 89Spider web stabilimenta, 93Tubeworms, etc., 94Experimental tests of survival value of masquerade, 94Ontogenetic changes and masquerade, 97Thanatosis (death feigning), 97Feign or flee? The trade‐offs of thanatosis, 100Other aspects of death mimicry, 100Seedless seeds and seedless fruit, 1004 APOSEMATISM AND ITS EVOLUTION, 103Introduction, 104Initial evolution of aposematism, 108Associations of unpalatable experience with place, 109Mathematical models and ideas of warning colouration evolution, 112Kin selection models, 112Green beard selection, 112Family selection models, 113Individual selection models, 113Spatial models and metapopulations, 116Handicap and signal honesty, 117Early warnings – reflex bleeding, vomiting and other noxious secretions, 120Longevity of aposematic protected taxa, 121Macroevolutionary consequences, 121Experimental studies, 121Tough aposematic prey and individual selection, 121Pyrazine and other early warnings, 123Learning and memorability, 124Strength of obnoxiousness, 126Is the nature of the protective compound important?, 126Neophobia and the role of novelty, 127Innate responses of predators, 130Aposematism and gregariousness, 132Phylogenetic analysis of aposematism and gregariousness, 134Behaviour of protected aposematic animals, 135Of birds and butterflies, 135Evolution of sluggishness, 139Origins of protective compounds, 140Plant‐derived toxins, 140Cardiac glycosides, 141Pyrrolizidine alkaloids, 144De novo synthesis of protective compounds, 145Obtaining toxins from animal sources, 147Costs of chemical defence, 149Aposematism with non‐chemical defence, 150Escape speed and low profitability, 150Parasitoids and aposematic insects, 152Diversity of aposematic forms, 152Egg load assessment, 154Proof of aposematism, 154Bioluminescence as a warning signal, 155Warning sounds, 155Warning colouration in mammals, 157Weapon advertisement, 158Mutualistic aposematism, 160Aposematism induced by a parasite, 161Aposematic commensalism, 161Polymorphism and geographic variation in aposematic species, 161Aposematism in plants, 163Synergistic selection of unpalatability in plants, 165Aposematism in fungi, 166Why are some unpalatable organisms aposematic and others not?, 1675 ANTI‐PREDATOR MIMICRY. I. MATHEMATICAL MODELS, 171Introduction, 172Properties of models, rewards, learning rates and numerical relationships, 172Simple models and their limitations, 173Muller’s original model, 173Simple models of Batesian and Mullerian mimicry, 173Are Batesian and Mullerian mimicry different?, 174An information theory model, 176Monte‐Carlo simulations, 177More refined models – time, learning, forgetting and sampling, 180Importance of alternative prey, 181Signal detection theory, 181Genetic and evolutionary models, 182Coevolutionary chases, 185Models involving population dynamics, 185Neural networks and evolution of Batesian mimicry, 188Automimicry in Batesian/Mullerian mimicry, 188Predator’s dilemma with potentially harmful prey, 1906 ANTI‐PREDATOR MIMICRY. II. EXPERIMENTAL TESTS, 191Introduction, 192Experimental tests of mimetic advantage, 192How similar do mimics need to be?, 194Is a two‐step process necessary?, 198Relative abundances of models and mimics in nature, 198Sex‐limited mimicries and mimetic load, 198Mimetic load, 203Apostatic selection and Batesian mimicry, 204Mullerian mimicry and unequal defence, 204Imperfect (satyric) mimicry, 2067 ANTI‐PREDATOR MIMICRY. III. BATESIAN AND MULLERIAN EXAMPLES, 213Introduction, 214Types of model, 214Mimicry of slow flight in butterflies, 214The Batesian/Mullerian spectrum, 215Famous butterflies: ecology, genetics and supergenes, 216Heliconius, 216Hybrid zones, 217Wing pattern genetics, 219Modelling polymorphism, 220Danaus and Hypolimnas, 220Papilio dardanus, 221Papilio glaucus, 223Papilio memnon, 223Supergenes and their origins, 223Mimicry between caterpillars, 224Some specific types of model among insects, 225Wasp (and bee) mimicry, 225How to look like a wasp, 228Time of appearance of aculeate mimics, 228Pseudostings and pseudostinging behaviour, 230Wasmannian (or ant) mimicry, 231Ant mimicry as defence against predation, 231Ant mimicry by spiders, 234Spiders that feed on ants, 236How to look like an ant or an ant carrying something?, 236Myrmecomorphy by caterpillars, 237Ant chemical mimicry by parasitoid wasps, 237Protective mimicries among vertebrates, 239Fish, 239Batesian mimicry among fish, 239Mullerian mimicry among fish, 239Batesian and Mullerian mimicry among terrestrial vertebrates, 239The coral snake problem – Emsleyan (or Mertensian) mimicry, 240Other snakes, zig‐zag markings and head shape, 244Mimicry of invertebrates by terrestrial vertebrates, 246Inaccurate (satyric) mimics, 248Mimicry of model behaviour, 249Aide mémoire mimicry, 250Batesian–Poultonian (predator) mimicry, 251Mimicry within predator–prey and host–parasite systems, 253Bluff and appearing larger than you are, 253Collective mimicry including an aggressive mimicry, 255Jamming, 255Man as model – the case of the samurai crab, 2588 ANTI‐PREDATOR MIMICRY. ATTACK DEFLECTION, SCHOOLING, ETC., 259Introduction, 260Attack deflection devices, 260Eyespots, 260Experimental tests of importance of eyespot features, 262Eyespots in butterflies, 266Wing marginal eyespots, 267Eyes with sparkles, 267Eyespots on caterpillars, 269Importance of eyespot conspicuousness, 269Eyespots and fish, 269Not just an eyespot but a whole head, winking and other enhancements, 271Reverse mimicry, 271Insects, 271Reverse mimicry in flight, 275Reverse mimicry in terrestrial vertebrates, 275Other deflectors, 277Injury feigning in nesting birds, 277Tail‐shedding (urotomy) in lizards and snakes, 277Flash and startle colouration, 280Intimidating displays and bizarre mimicries, 283Schooling, flocking and predator confusion, 284‘Social’ mimicry in birds and fish, 286Alarm call mimicry for protection, 2879 ANTI‐HERBIVORY DECEPTIONS, 289Introduction, 290Crypsis as protection in plants, 290Leaf mottling and variegation for crypsis, 291Mistletoes and lianas, 293Fruit masquerade by leaves, 294Protective Batesian and Mullerian mimicry in plants, 295False indicators of damage or likely future damage, 296Conspicuousness of leafmines, 297Dark central florets in some Apiaceae, 297Mimicry of silk or fungal hyphae, 299Insect egg mimics, 299Defensive aphid and caterpillar mimicry in plants, 300Aphid deterrence by alarm pheromone mimicry, 300Ant mimicry in plants, 301Of orchids and bees, 301Carrion mimicry as defence, 302Algae and corals, 302Plant galls, 302Experimental evidence for plant aposematism and Batesian mimetic potential in plants, 30210 AGGRESSIVE DECEPTIONS, 305Introduction, 306Cryptic versus alluring features, 307Crypsis and masquerade by predators, 307Stealth, 307Shadowing, 308Seasonal polymorphisms in predators, 308Why seabirds are black and white (and grey), 309Chemical crypsis by a predatory fish, 309Alluring mimicries, 310Flower mimicry, 312Rain mimicry, 315Physical lures, 315Angling fish, 315Caudal (and tongue) lures in reptiles, 317Caudal lure in a dragonfly, 318Death feigning as a lure, 318Other prey and food mimicry, 319The case of the German cockroach, 319Wolves in sheeps’ clothing, 319Vulture‐like hawks, 319Cleaner fish and their mimics, 320Mingling with an innocuous crowd, 322Duping by mimicry of competitors, 323Seeming to be conspecific, 324Getting close, 325Appearing to be a potential mate, 325Pheromone lures, 326Mimicking danger as a flushing device, 328Human use of aggressive mimicry, 328Cuckoldry, inquilines and brood parasitism, 329Cuckoldry in birds, 329Gentes and ‘cuckoo’ eggs, 332Cues for egg rejection, 335Mimicry by chicks – genetic and substantive differences, 338Cuckoo chick appearance, 338Begging calls, 339Cuckoo and host coevolution, 340Mimicry between adult cuckoos and their hosts, 340Hawk mimicry by adult cuckoos, 340Mimicry of harmless birds by adult cuckoos, 342Brood parasitism and inquilinism in social insects, 342Cuckoo bees and cuckoo wasps, 342Kleptoparasites of bees, 346Myrmecophily, 346Acquired chemical mimicry in social parasites and inquilines, 346Brood‐parasitic and slave‐making ants, 348Chemical mimicry and ant and termite inquilines, 349A brood‐parasitic aphid, 349Ants and aphid trophallaxis, 349Aphidiine parasitoids of ant‐attended aphids, 350Does aggressive mimicry occur in plants?, 35011 SEXUAL MIMICRIES IN ANIMALS (INCLUDING HUMANS), 353Introduction, 354Mimicking the opposite sex, 354Female mimicry by males, 354Avoiding aggression from competing males, 357Mate guarding through distracting other males, 357Androchromatism and male mimicry by females, 358Egg dummies on fish, 360Food dummies and sex, 362Mimicry by sperm‐dependent all‐female lineages, 363Female genital mimicry in a female, 363Energy‐saving cheating for sex, 364Behavioural deceptions in higher vertebrates, 364Polygynous birds, 364Deceptive use of alarm calls and paternity protection, 365Female–female mounting behaviour in mammals and birds, 365Mimicry in humans, 367Make‐up, clothes and silicone, 367Cryptic oestrus in humans, 368Flirting in humans, 36812 REPRODUCTIVE MIMICRIES IN PLANTS, 371Introduction, 372Pollinator deception, 372Pollinator sex pheromone mimicry, 376Food deception, 382Specific floral mimicry, 382Generalised floral mimicry, 386Mimicry of a fungus‐infected plant, 388Brood‐site/oviposition‐site deception, 388Shelter mimicry, 392Flower similarity over time, 392Flower automimicry – intraspecific food deception (bakerian mimicry), 393Mathematical modelling of sexual deception by plants, 394Pollinator guild syndromes, 394Bird‐pollinated systems, 39413 INTRA‐ AND INTERSPECIFIC COOPERATION, COMPETITION AND HIERARCHIES, 399Introduction, 400Remaining looking young, 400Delayed plumage maturation, 400Interspecific social dominance mimicry, 401Bird song and alarm call mimicry – deceptive acquisition of resources, 401Wicklerian mimicry – mimicry of opposite sex to reduce aggression, 403Female resemblance in male primates, 403Social appeasement by female mimicry in an insect, 404Hyperfemininity in prereproductive adolescent primates, 404Mimicry of male genitalia by females, 404The case of the spotted hyaena, 404Mimicry of male genitalia in other mammals, 404Phallic mimicry by males, 405Appetitive (foraging) mimicry, 406Appetitive mimicry and deceptive use of alarm calls, 406Beau Geste and seeming to be more than you are, 408Appearing older than you are, 408Weapon automimicry, 40814 ADAPTIVE RESEMBLANCES AND DISPERSAL: SEEDS, SPORES AND EGGS, 409Introduction, 410Fruit and seed dispersal by birds, 410Warningly coloured fruit, 414Fruit mimicry by seeds, 414Seed dispersal by humans, arable weeds and Vavilovian mimicry, 414Seed elaiosomes and their insect mimics, 415Mimicry by parasites to facilitate host finding, 415The trematode and the snail, 415The trematode and the fish, 416Pocketbook clams and fish, 416‘Termite balls’, 417Pseudoflowers, pseudo‐anthers and pseudo‐pollen, 417Truffles, 418Mimicry of dead flesh by fungi and mosses, 419Deception of dung beetles by fruit, 41915 MOLECULAR MIMICRY: PARASITES, PATHOGENS AND PLANTS, 421Introduction, 422Macro‐animal systems, 422Anemone fish, 422Parasitic helminthes, 422Platyhelminthes (Trematoda), 422Tapeworms (Platyhelminthes: Cestoda), 423Parasitic nematodes, 423Parasitoid wasp eggs, 424Pathogenic fungi, 424Protista, 424Chagas’ disease, 424Microbial systems, 424Bacterial chemical mimicry and autoimmune responses, 424Helicobacter pylori, 425Campylobacter jejuni, 425Mimicry by plant‐pathogenic bacteria, 425Viruses, 425Plants, 425Sugar, toxin and satiation mimicry, 425Phytoecdysteroids – plant chemicals that mimicinsect moulting hormone, 427Plant oestrogens – phyto‐contraceptives, 427Extended glossary, 429References, 445Author index, 515General index, 533Taxonomic index, 539