Skip to main content

The Proposed Anti-herbivory Roles of White Leaf Variegation

  • Chapter
  • First Online:

Part of the book series: Progress in Botany ((BOTANY,volume 76))

Abstract

It has been suggested that white variegation, the outcome of various developmental, genetic, and physiological processes, may defend leaves and other plant organs from herbivory by several proposed mechanisms: camouflage, aposematism (including Müllerian and Batesian mimicry), mimicry of insect damage and fungal attacks, dazzle effects that make it hard for large herbivores to decide where to bite the leaves and for insects to land on them, and by visual repellence of insects from landing as well as by unknown mechanisms. Very few cases of these suggested leaf defenses by variegation have been examined in depth. Some such studied cases were indeed found to actually operate as defense from herbivory either in nature or in experiments, suggesting the potential defensive function of others. However, the specific operating defensive mechanism by white variegation was not always identified or even proposed, even when variegation was found to be associated with reduced herbivory. Studying white variegation has a significant advantage over studying other types of plant defensive coloration because even bi-chromatic vision is sufficient to see these patterns. Moreover, white variegation is probably visible under most types of natural light conditions, including strong moonlight. While in this essay I wish to stimulate an effort for a broader and deeper understanding of the defensive roles of white variegation, the possible simultaneous physiological roles of white leaf variegation that will not be reviewed here should not be ignored.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Addicott FT (1982) Abscission. University of California Press, Berkeley, CA

    Google Scholar 

  • Allen JA, Cooper JM (1985) Crypsis and masquerade. J Biol Educ 19:268–270

    Google Scholar 

  • Allen JA, Knill R (1991) Do grazers leave mottled leaves in the shade? Trends Ecol Evol 6:109–110

    Google Scholar 

  • Aluru MR, Yu F, Fu A, Roderme S (2006) Arabidopsis variegation mutants: new insights into chloroplast biogenesis. J Exp Bot 57:1871–1881

    PubMed  CAS  Google Scholar 

  • Archetti M (2000) The origin of autumn colours by coevolution. J Theor Biol 205:625–630

    PubMed  CAS  Google Scholar 

  • Archetti M, Döring TF, Hagen SB, Hughes NM, Leather SR, Lee DW, Lev-Yadun S, Manetas Y, Ougham HJ, Schaberg PG, Thomas H (2009) Unravelling the evolution of autumn colours: an interdisciplinary approach. Trends Ecol Evol 24:166–173

    PubMed  Google Scholar 

  • Arditti J, Rodriguez E (1982) Dieffenbachia: uses, abuses and toxic constituents: a review. J Ethnopharmacol 5:293–302

    PubMed  CAS  Google Scholar 

  • Bar-Oz G (2004) Epipalaeolithic subsistence strategies in the Levant: a zooarchaeological perspective, The American School of Prehistoric Research (ASPR) monograph series. Brill Academic Publishers, Boston, MA

    Google Scholar 

  • Blanco MA, Martén-Rodríguez S (2007) The stained-glass palm, Geonoma epetiolata. Palms 51:139–146

    Google Scholar 

  • Borowicz VA (1988) Do vertebrates reject decaying fruit? An experimental test with Cornus amomum fruits. Oikos 53:74–78

    Google Scholar 

  • Bradbury JH, Nixon RW (1998) The acridity of raphides from the edible aroids. J Sci Food Agric 76:608–616

    CAS  Google Scholar 

  • Brady J, Shereni W (1988) Landing responses of the tsetse fly Glossina morsitans morsitans Westwood and the stable fly Stomoxys calcitrans (L.) (Diptera: Glossinidae & Muscidae) to black-and-white patterns: a laboratory study. Bull Entomol Res 78:301–311

    Google Scholar 

  • Brown JS (1999) Vigilance, patch use and habitat selection: foraging under predation risk. Evol Ecol Res 1:49–71

    Google Scholar 

  • Brown JS, Kotler BP (2004) Hazardous duty pay and the foraging cost of predation. Ecol Lett 7:999–1014

    Google Scholar 

  • Brown VK, Lawton JH, Grubb PJ (1991) Herbivory and the evolution of leaf size and shape. Phil Trans R Soc Lond B 333:265–272

    Google Scholar 

  • Buchholz R, Levey DJ (1990) The evolutionary triad of microbes, fruits, and seed dispersers: an experiment in fruit choice by cedar waxwings, Bombycilla cedrorum. Oikos 59:200–204

    Google Scholar 

  • Burns KC (2010) Is crypsis a common defensive strategy in plants? Speculation on signal deception in the New Zealand flora. Plant Signal Behav 5:9–13

    PubMed  PubMed Central  Google Scholar 

  • Cahn MG, Harper JL (1976a) The biology of the leaf mark polymorphism in Trifolium repens L. 1. Distribution of phenotypes at a local scale. Heredity 37:309–325

    Google Scholar 

  • Cahn MG, Harper JL (1976b) The biology of the leaf mark polymorphism in Trifolium repens L. 2. Evidence for the selection of leaf marks by rumen fistulated sheep. Heredity 37:327–333

    Google Scholar 

  • Campitelli BE, Steglik I, Stinchcombe JR (2008) Leaf variegation is associated with reduced herbivore damage in Hydrophyllum virginianum. Botany 86:306–313

    Google Scholar 

  • Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press, Chicago, IL

    Google Scholar 

  • Caro T (2009) Contrasting coloration in terrestrial mammals. Phil Trans R Soc B 364:537–548

    PubMed  PubMed Central  Google Scholar 

  • Cole DT (1970) Lithops in habitat. In: Sprechman DL (ed) Lithops. Fairleigh Dickinson University Press, Cranbury, NJ, pp 21–32

    Google Scholar 

  • Cole DT, Cole NA (2005) Lithops – flowering stones. Cactus & Co., Venegono, Italy

    Google Scholar 

  • Coley PD, Bryant JP, Chapin FS III (1985) Resource availability and plant antiherbivore defense. Science 230:895–899

    PubMed  CAS  Google Scholar 

  • Cott HB (1940) Adaptive coloration in animals. Methuen & Co., London

    Google Scholar 

  • Crawford-Sidebotham TJ (1972) The role of slugs and snails in the maintenance of the cyanogenesis polymorphisms of Lotus corniculatus and Trifolium repens. Heredity 28:405–411

    Google Scholar 

  • Cuthill IC, Stevens M, Sheppard J, Maddocks T, Párraga CA, Troscianko TS (2005) Disruptive coloration and background pattern matching. Nature 434:72–74

    PubMed  CAS  Google Scholar 

  • Davis SJM (1987) The archaeology of animals. Yale University Press, New Haven, CT

    Google Scholar 

  • De Moraes CM, Mescher MC, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580

    PubMed  Google Scholar 

  • Dirzo R, Harper JL (1982) Experimental studies on slug-plant interactions IV. The performance of cyanogenic and acyanogenic morphs of Trifolium repens in the field. J Ecol 70:119–138

    Google Scholar 

  • Doku C, Brady J (1989) Landing site preferences of Glossina morsitans morsitans Westwood (Diptera: Glossinidae) in the laboratory: avoidance of horizontal features? Bull Entomol Res 79:521–528

    Google Scholar 

  • Edmunds M (1974) Defence in animals. A survey of anti-predator defences. Longman, Harlow

    Google Scholar 

  • Egri Á, Blahó M, Kriska G, Farkas R, Gyurkovszky M, Åkesson S, Horváth G (2012) Polarotactic tabanids find striped patterns with brightness and/or polarization modulation least attractive: an advantage of zebra stripes. J Exp Biol 215:736–745

    PubMed  Google Scholar 

  • Embar K, Kotler BP, Mukherjee S (2011) Risk management in optimal foragers: the effect of sightlines and predator type on patch use, time allocation, and vigilance in gerbils. Oikos 120:1657–1666

    Google Scholar 

  • Endara MJ, Coley PD (2011) The resource availability hypothesis revisited: a meta-analysis. Funct Ecol 25:389–398

    Google Scholar 

  • Endler JA (1981) An overview of the relationships between mimicry and crypsis. Biol J Linn Soc 16:25–31

    Google Scholar 

  • Evans CRH (1987) Oral ulceration after contact with the houseplant Dieffenbachia. Br Dental J 162:467–468

    CAS  Google Scholar 

  • Evenari M (1989) The history of research on white-green variegated plants. Bot Rev 55:106–139

    Google Scholar 

  • Fadzly N, Burns KC (2010) Hiding from the ghost of herbivory past: evidence for crypsis in an insular tree species. Int J Plant Sci 171:828–833

    Google Scholar 

  • Fadzly N, Jack C, Schaefer HM, Burns KC (2009) Ontogenetic colour changes in an insular tree species: signalling to extinct browsing birds? New Phytol 184:495–501

    PubMed  Google Scholar 

  • Fahn A (1990) Plant anatomy, 4th edn. Pergamon, Oxford

    Google Scholar 

  • Finch S, Jones TH (1989) An analysis of the deterrent effect of Aphids on cabbage root fly (Delia radicum) egg-laying. Ecol Entomol 14:387–391

    Google Scholar 

  • Forbes P (2009) Dazzled and deceived: mimicry and camouflage. Yale University Press, New Haven, CT

    Google Scholar 

  • Forsman A, Herrström J (2004) Asymmetry in size, shape, and color impairs the protective value of conspicuous color patterns. Behav Ecol 15:141–147

    Google Scholar 

  • Forsmann A, Merilaita S (1999) Fearful symmetry: pattern size and asymmetry affects aposematic signal efficacy. Evol Ecol 13:131–140

    Google Scholar 

  • Franceschi VR, Horner HT Jr (1980) Calcium oxalate crystals in plants. Bot Rev 46:361–427

    CAS  Google Scholar 

  • Gardner DG (1994) Injury to the oral mucous membranes caused by the common houseplant, diffenbachia. A review. Oral Surg Oral Med Oral Pathol 78:631–633

    PubMed  CAS  Google Scholar 

  • Gibson G (1992) Do tsetse flies ‘see’ zebras? A field study of the visual response of tsetse to striped targets. Physiol Entomol 17:141–147

    Google Scholar 

  • Givnish TJ (1990) Leaf mottling: relation to growth form and leaf phenology and possible role as camouflage. Funct Ecol 4:463–474

    Google Scholar 

  • Gotelli NJ, Ulrich W (2012) Statistical challenges in null model analysis. Oikos 121:171–180

    Google Scholar 

  • Grubb PJ (1992) A positive distrust in simplicity – lessons from plant defences and from competition among plants and among animals. J Ecol 80:585–610

    Google Scholar 

  • Halpern M, Raats D, Lev-Yadun S (2007a) Plant biological warfare: thorns inject pathogenic bacteria into herbivores. Environ Microbiol 9:584–592

    PubMed  CAS  Google Scholar 

  • Halpern M, Raats D, Lev-Yadun S (2007b) The potential anti-herbivory role of microorganisms on plant thorns. Plant Signal Behav 2:503–504

    PubMed  PubMed Central  Google Scholar 

  • Halpern M, Waissler A, Dror A, Lev-Yadun S (2011) Biological warfare of the spiny plant: introducing pathogenic microorganisms into herbivore’s tissues. Adv Appl Microbiol 74:97–116

    PubMed  CAS  Google Scholar 

  • Hamilton WD, Brown SP (2001) Autumn tree colours as a handicap signal. Proc R Soc Lond B 268:1489–1493

    CAS  Google Scholar 

  • Hara N (1957) Study of the variegated leaves, with special reference to those caused by air spaces. Jap J Bot 16:86–101

    Google Scholar 

  • Harper JL (1977) Population biology of plants. Academic, London

    Google Scholar 

  • Hawlena D, Schmitz OJ (2010) Herbivore physiological response to predation risk and implications for ecosystem nutrient dynamics. Proc Natl Acad Sci U S A 107:15503–15507

    PubMed  CAS  PubMed Central  Google Scholar 

  • Herrera CM (1982) Defense of ripe fruit from pests: its significance in relation to plant-disperser interactions. Am Nat 120:218–241

    Google Scholar 

  • Hinton HE (1973) Natural deception. In: Gregory RL, Gombrich EH (eds) Illusion in nature and art. Duckworth, London, pp 97–159

    Google Scholar 

  • Hornell J (1941) Fishing-poisons. Man 41:126–128

    Google Scholar 

  • Inbar M, Lev-Yadun S (2005) Conspicuous and aposematic spines in the animal kingdom. Naturwiss 92:170–172

    PubMed  CAS  Google Scholar 

  • Inbar M, Doostdar H, Mayer RT (1999) Effects of sessile Whitefly nymphs (Homoptera: Aleyrodidae) on leaf-chewing larvae (Lepidoptera: Noctuidae). Environ Entomol 28:353–357

    Google Scholar 

  • Janzen DH (1977) Why fruits rot, seeds mold, and meat spoils. Am Nat 111:691–713

    CAS  Google Scholar 

  • Jones KA, Krebs JR, Whittingham MJ (2006) Interaction between seed crypsis and habitat structure influence patch choice in a granivorous bird, the chaffinch Fringilla coelebs. J Avian Biol 37:413–418

    Google Scholar 

  • Justus M, Witte L, Hartmann T (1997) Levels and tissue distribution of loline alkaloids in endophyte-infected Festuca pratensis. Phytochem 44:51–57

    CAS  Google Scholar 

  • Kappers IF, Aharoni A, van Herpen TWJM, Luckerhoff LLP, Dicke M, Bouwmeester HJ (2005) Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309:2070–2072

    PubMed  CAS  Google Scholar 

  • Karban R (2007) Deciduous leaf drop reduces insect herbivory. Oecologia 153:81–88

    PubMed  Google Scholar 

  • Kendrick JW, Tucker J, Peoples SA (1955) Nitrate poisoning in cattle due to ingestion of variegated thistle, Silybum marianum. J Am Vet Med Assoc 126:53–56

    PubMed  CAS  Google Scholar 

  • Kessler A, Baldwin IT (2001) Defensive function of herbivore induced plant volatile emissions in nature. Science 291:2141–2144

    PubMed  CAS  Google Scholar 

  • Kettlewell B (1973) The evolution of melanism. Clarendon, Oxford

    Google Scholar 

  • Klooster MR, Clark D, Culley TA (2009) Cryptic bracts facilitate herbivore avoidance in the mycoheterotrophic plant Monotropsis odorata (Ericaceae). Am J Bot 96:2197–2205

    PubMed  Google Scholar 

  • Konoplyova A, Petropoulou Y, Yiotis C, Psaras GK, Manetas Y (2008) The fine structure and photosynthetic cost of structural leaf variegation. Flora 203:653–662

    Google Scholar 

  • Kotepong P, Ketsa S, van Doorn WG (2011) A white mutant of Malay apple fruit (Syzygium malaccense) lacks transcript expression and activity for the last enzyme of anthocyanin synthesis, and the normal expression of a MYB transcription factor. Funct Plant Biol 38:75–86

    CAS  Google Scholar 

  • La Rocca N, Rascio N, Pupillo P (2011) Variegation in Arum italicum leaves. A structural-functional study. Plant Physiol Biochem 49:1392–1398

    PubMed  Google Scholar 

  • La Rocca N, Pupillo P, Puppi G, Rascio N (2014) Erythronium dens-canis L. (Liliaceae): an unusual case of change of leaf mottling. Plant Physiol Biochem 74:108–117

    PubMed  Google Scholar 

  • Landau SY, Ben-Moshe E, Shlosberg A, Bellaiche M, Perevolotsky A (1999) Conditioned aversion to minimize Ferula communis intake by orphaned lambs. J Range Manag 52:436–439

    Google Scholar 

  • Lee D (2007) Nature’s palette. The science of plant color. University Chicago Press, Chicago, IL

    Google Scholar 

  • Lev-Yadun S (2001) Aposematic (warning) coloration associated with thorns in higher plants. J Theor Biol 210:385–388

    PubMed  CAS  Google Scholar 

  • Lev-Yadun S (2003a) Why do some thorny plants resemble green zebras? J Theor Biol 244:483–489

    Google Scholar 

  • Lev-Yadun S (2003b) Weapon (thorn) automimicry and mimicry of aposematic colorful thorns in plants. J Theor Biol 244:183–188

    Google Scholar 

  • Lev-Yadun S (2006a) Defensive coloration in plants: a review of current ideas about anti-herbivore coloration strategies. In: Teixeira da Silva JA (ed) Floriculture, ornamental and plant biotechnology: advances and topical issues, vol IV. Global Science Books, London, pp 292–299

    Google Scholar 

  • Lev-Yadun S (2006b) Defensive functions of white coloration in coastal and dune plants. Isr J Plant Sci 54:317–325

    Google Scholar 

  • Lev-Yadun S (2009a) Aposematic (warning) coloration in plants. In: Baluska F (ed) Plant-environment interactions, vol II, From sensory plant biology to active behavior. Springer, Berlin, pp 167–202

    Google Scholar 

  • Lev-Yadun S (2009b) Müllerian and Batesian mimicry rings of white-variegated aposematic spiny and thorny plants: a hypothesis. Isr J Plant Sci 57:107–116

    Google Scholar 

  • Lev-Yadun S (2009c) Müllerian mimicry in aposematic spiny plants. Plant Signal Behav 4:482–483

    PubMed  PubMed Central  Google Scholar 

  • Lev-Yadun S (2011) Fearful symmetry in aposematic plants. Plant Signal Behav 6:1739–1740

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lev-Yadun S (2013) Theoretical and functional complexity of white variegation of unripe fleshy fruits. Plant Signal Behav 8:e25851

    PubMed Central  Google Scholar 

  • Lev-Yadun S (2014) Potential defence from herbivory by dazzle effects and trickery coloration of leaf variegation. Biol J Linn Soc 111:692–697

    Google Scholar 

  • Lev-Yadun S, Gould KS (2007) What do red and yellow autumn leaves signal? Bot Rev 73:279–289

    Google Scholar 

  • Lev-Yadun S, Gould KS (2009) Role of anthocyanins in plant defense. In: Gould KS, Davies KM, Winefield C (eds) Life’s colorful solutions: the biosynthesis, functions, and applications of anthocyanins. Springer, Berlin, pp 21–48

    Google Scholar 

  • Lev-Yadun S, Halpern M (2007) Ergot (Claviceps purpurea) - an aposematic fungus. Symbiosis J 43:105–108

    Google Scholar 

  • Lev-Yadun S, Halpern M (2008) External and internal spines in plants insert pathogenic microorganisms into herbivore’s tissues for defense. In: Van Dijk T (ed) Microbial ecology research trends. Nova Scientific, New York, NY, pp 155–168

    Google Scholar 

  • Lev-Yadun S, Ne’eman G (2004) When may green plants be aposematic? Biol J Linn Soc 81:413–416

    Google Scholar 

  • Lev-Yadun S, Ne’eman G (2006) Color changes in old aposematic thorns, spines, and prickles. Isr J Plant Sci 54:327–333

    Google Scholar 

  • Lev-Yadun S, Ne’eman G (2013) Bimodal colour pattern of individual Pinus halepensis Mill. seeds – an adaptation for crypsis. Biol J Linn Soc 109:271–278

    Google Scholar 

  • Lev-Yadun S, Gopher A, Abbo S (2000) The cradle of agriculture. Science 288:1602–1603

    PubMed  CAS  Google Scholar 

  • Lev-Yadun S, Dafni A, Flaishman MA, Inbar M, Izhaki I, Katzir G, Ne’eman G (2004a) Plant coloration undermines herbivorous insect camouflage. Bioessays 26:1126–1130

    PubMed  Google Scholar 

  • Lev-Yadun S, Flaishman MA, Atzmon N (2004b) Nonchimeric variegated mutation in Cupressus sempervirens L. Int J Plant Sci 165:257–261

    Google Scholar 

  • Lev-Yadun S, Ne’eman G, Izhaki I (2009) Unripe red fruits may be aposematic. Plant Signal Behav 4:836–841

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lüttge U (1997) Physiological ecology of tropical plants. Springer, Berlin

    Google Scholar 

  • Mackay DA, Jones RE (1989) Leaf shape and the host-finding behaviour of two ovipositing monophagous butterfly species. Ecol Entomol 14:423–431

    Google Scholar 

  • Majerus MEN (1998) Melanism. Evolution in action. Oxford University Press, Oxford

    Google Scholar 

  • Manzur MI, Courtney SP (1984) Influence of insect damage in fruits of hawthorn on bird foraging and seed dispersal. Oikos 43:265–270

    Google Scholar 

  • Martínez-Abraín A (2008) Statistical significance and biological relevance: a call for a more cautious interpretation of results in ecology. Acta Oecol 34:9–11

    Google Scholar 

  • McKey D, Waterman PG, Mbi CN, Gartlan JS, Struhsaker TT (1978) Phenolic content of vegetation in two African rain forests: ecological implications. Science 202:61–64

    Google Scholar 

  • Merilaita S (1998) Crypsis through disruptive coloration in an isopod. Proc R Soc Lond B 265:1059–1064

    Google Scholar 

  • Midgley JJ (2004) Why are spines of African Acacia species white? Afr J Range Forage Sci 21:211–212

    Google Scholar 

  • Midgley JJ, Botha MA, Balfour D (2001) Patterns of thorn length, density, type and colour in African Acacias. Afr J Range Forage Sci 18:59–61

    Google Scholar 

  • Mudge JF (2013) Explicit consideration of critical effect sizes and costs of errors can improve decision-making in plant science. New Phytol 199:876–878

    PubMed  Google Scholar 

  • Nassar O, Lev-Yadun S (2009) How prickly is a prickly pear? Isr J Plant Sci 57:117–124

    Google Scholar 

  • Niemelä P, Tuomi J, Siren S (1984) Selective herbivory on mosaic leaves of variegated Acer pseudoplatanus. Experientia 40:1433–1434

    Google Scholar 

  • Noy-Meir I, Gutman M, Kaplan Y (1989) Responses of Mediterranean grassland plants to grazing and protection. J Ecol 77:290–310

    Google Scholar 

  • Ohmiya A, Kishimoto S, Aida R, Yoshioka S, Sumitomo K (2006) Carotenoid cleavage dioxygenase (CmCCD4a) contributes to white color formation in chrysanthemum petals. Plant Physiol 142:1193–1201

    PubMed  CAS  PubMed Central  Google Scholar 

  • Ortolani A (1999) Spots, stripes, tail tips and dark eyes: predicting the function of carnivore colour patterns using the comparative method. Biol J Linn Soc 67:433–476

    Google Scholar 

  • Osorio D, Srinivasan MV (1991) Camouflage by edge enhancement in animal coloration patterns and its implications for visual mechanisms. Proc R Soc Lond B 244:81–85

    CAS  Google Scholar 

  • Perevolotsky A, Seligman N (1998) Role of grazing in Mediterranean rangeland ecosystems. Inversion of a paradigm. BioScience 48:1007–1017

    Google Scholar 

  • Pfister JA, Müller-Schwarze D, Balph DF (1990) Effects of predator fecal odors on feed selection by sheep and cattle. J Chem Ecol 16:573–583

    PubMed  CAS  Google Scholar 

  • Poethig RS (1987) Clonal analysis of cell lineage patterns in plant development. Am J Bot 74:581–594

    Google Scholar 

  • Porter JK (1994) Chemical constituents of grass endophytes. In: Bacon CW, White JF (eds) Biotechnology of endophytic fungi of grasses. CRC, Boca Raton, FL, pp 103–123

    Google Scholar 

  • Preisser EL (2009) The physiology of predator stress in free-ranging prey. J Anim Ecol 78:1103–1105

    PubMed  Google Scholar 

  • Prokopy RJ, Owens ED (1983) Visual detection of plants by herbivorous insects. Annu Rev Entomol 28:337–364

    Google Scholar 

  • Rasmann S, Agrawal AA (2011) Latitudinal patterns in plant defense: evolution of cardenolides, their toxicity and induction following herbivory. Ecol Lett 14:476–483

    PubMed  Google Scholar 

  • Rausher MD (1978) Search image for leaf shape in a butterfly. Science 200:1071–1073

    PubMed  CAS  Google Scholar 

  • Reeves JL (2011) Vision should not be overlooked as an important sensory modality for finding host plants. Environ Entomol 40:855–863

    PubMed  Google Scholar 

  • Reznicek G, Jurenitsch J, Robien W, Kubelka W (1989) Saponins in Cyclamen species: configuration of cyclamiretin C and structure of isocyclamin. Phytochem 28:825–828

    CAS  Google Scholar 

  • Ripple WJ, Beschta RL (2004) Wolves and the ecology of fear: can predation risk structure ecosystems? BioScience 54:755–766

    Google Scholar 

  • Ronel M, Lev-Yadun S (2009) Spiny plants in the archaeological record of Israel. J Arid Environ 73:754–761

    Google Scholar 

  • Ronel M, Lev-Yadun S (2012) The spiny, thorny and prickly plants in the flora of Israel. Bot J Linn Soc 168:344–352

    Google Scholar 

  • Ronel M, Khateeb S, Lev-Yadun S (2009) Protective spiny modules in thistles of the Asteraceae in Israel. J Torrey Bot Soc 136:46–56

    Google Scholar 

  • Ronel M, Ne’eman G, Lev-Yadun S (2010) Spiny east-Mediterranean plant species flower later and in a drier season than non-spiny species. Flora 205:276–281

    Google Scholar 

  • Rosso D, Bode R, Li W, Krol M, Saccon D, Wang S, Schillaci LA, Rodermel SR, Maxwell DP, Hüner PA (2009) Photosynthetic redox imbalance governs leaf sectoring in the Arabidopsis thaliana variegation mutants immutans, spotty, var1, and var2. Plant Cell 21:3473–3492

    PubMed  CAS  PubMed Central  Google Scholar 

  • Rothschild M (1986) The red smell of danger. New Sci 111:34–36

    Google Scholar 

  • Rothschild M, Moore B (1987) Pyrazines as alerting signals in toxic plants and insects. In: Labeyrie V, Fabres G, Lachaise D (eds) Insects – plants. Dr W. Junk, Dordrecht, pp 97–101

    Google Scholar 

  • Rowland HM, Mappes J, Ruxton GD, Speed MP (2010) Mimicry between unequally defended prey can be parasitic: evidence for quasi-Batesian mimicry. Ecol Lett 13:1494–1502

    PubMed  Google Scholar 

  • Rubino DL, McCarthy BC (2004) Presence of aposematic (warning) coloration in vascular plants of southeastern Ohio. J Torrey Bot Soc 131:252–256

    Google Scholar 

  • Ruxton GD (2002) The possible fitness benefits of striped coat coloration for zebra. Mammal Rev 32:237–244

    Google Scholar 

  • Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack. The evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, Oxford

    Google Scholar 

  • Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343

    Google Scholar 

  • Sakai WS, Hanson M, Jones RC (1972) Raphids with barbs and grooves in Xanthosoma sagittifolium (Araceae). Science 178:314–315

    PubMed  CAS  Google Scholar 

  • Salts D, Ward D (2000) Responding to a three-pronged attack: desert lilies subject to herbivory by dorcas gazelles. Plant Ecol 148:127–138

    Google Scholar 

  • Scarchuk J, Lent JM (1965) The structure of mottled-leaf summer squash. J Hered 56:167–168

    CAS  Google Scholar 

  • Schaefer HM, Ruxton GD (2009) Deception in plants: mimicry or perceptual exploitation? Trends Ecol Evol 24:676–685

    PubMed  Google Scholar 

  • Schaefer HM, Ruxton GD (2011) Plant-animal communication. Oxford University Press, New York, NY

    Google Scholar 

  • Schaefer M, Stobbe N (2006) Disruptive coloration provides camouflage independent of background matching. Proc R Soc Lond B 273:2427–2432

    Google Scholar 

  • Schemske DW, Mittelbach GG, Cornell HV, Sobel JM, Roy K (2009) Is there a latitudinal gradient in the importance of biotic interactions. Annu Rev Ecol Evol Syst 40:245–269

    Google Scholar 

  • Sheriff MJ, Krebs CJ, Boonstra R (2009) The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. J Anim Ecol 78:1249–1258

    PubMed  Google Scholar 

  • Shifriss O (1981) Do Cucurbita plants with silvery leaves escape virus infection? Cucurbit Genetics Cooperative Report 4:42–43

    Google Scholar 

  • Skelhorn J, Rowland HM, Ruxton GD (2010a) The evolution and ecology of masquerade. Biol J Linn Soc 99:1–8

    Google Scholar 

  • Skelhorn J, Rowland HM, Speed MP, Ruxton GD (2010b) Masquerade: camouflage without crypsis. Science 327:51

    PubMed  CAS  Google Scholar 

  • Skelhorn J, Rowland HM, Speed MP, De Wert L, Quinn L, Delf J, Ruxton GD (2010c) Size-dependent misclassification of masqueradinf prey. Behav Ecol 21:1344–1348

    Google Scholar 

  • Smith AP (1986) Ecology of leaf color polymorphism in a tropical forest species: habitat segregation and herbivory. Oecologia 69:283–287

    Google Scholar 

  • Soltau U, Dötterl S, Liede-Schumann S (2009) Leaf variegation in Caladium steudneriifolium (Araceae): a case of mimicry? Evol Ecol 23:503–512

    Google Scholar 

  • Speed MP, Ruxton GD (2005) Warning displays in spiny animals: one (more) evolutionary route to aposematism. Evolution 59:2499–2508

    PubMed  Google Scholar 

  • Stanley RM II (1998) To fool a glass eye. Camouflage versus photoreconnaissance in World War II. Smithsonian Institute Press, Washington, DC

    Google Scholar 

  • Steiner MC (2005) The faunas of Hayonim Cave (Israel): a 200,000-year record of Paleolithic diet, demography and society. Peabody Museum of Archaeology and Ethnology, Cambridge

    Google Scholar 

  • Stevens M, Cuthill IC, Windsor AMM, Walker HJ (2006) Disruptive contrast in animal camouflage. Proc R Soc B 273:2433–2438

    PubMed  PubMed Central  Google Scholar 

  • Tchernov E (1979) Quaternary fauna. In: Horowitz A (ed) The quaternary of Israel. Academic, New York, NY, pp 257–290

    Google Scholar 

  • Terlouw EMC, Boissy A, Blinet P (1998) Behavioural responses of cattle to the odours of blood and urine from conspecifics and to the odour of faeces from carnivores. Appl Anim Behav Sci 57:9–21

    Google Scholar 

  • Tilney-Bassett RAE (1986) Plant chimeras. Edward Arnold, London

    Google Scholar 

  • Tsukaya H, Okada H, Mohamed M (2004) A novel feature of structural variegation in leaves of the tropical plant Schismatoglottis calyptrata. J Plant Res 117:477–480

    PubMed  Google Scholar 

  • von Helversen B, Schooler LJ, Czienskowski U (2013) Are stripes beneficial? Dazzle camouflage influences perceived speed and hit rates. PLoS One 8:e61173

    Google Scholar 

  • Waage JK (1981) How the zebra got its stripes – biting flies as selective agents in the evolution of zebra coloration. J Ent Soc S Afr 44:351–358

    Google Scholar 

  • Wäli PP, Wäli PR, Saikkonen K, Tuomi J (2013) Is the pathogenic ergot fungus a conditional defensive mutualist for its host grass? PLoS One 8:e69249

    PubMed  PubMed Central  Google Scholar 

  • Ward D, Spiegel M, Saltz D (1997) Gazelle herbivory and interpopulation differences in calcium oxalate content of leaves of a desert lily. J Chem Ecol 23:333–346

    CAS  Google Scholar 

  • Wickler W (1968) Mimicry in plants and animals. Weidenfeld and Nicolson, London

    Google Scholar 

  • Wiens D (1978) Mimicry in plants. Evol Biol 11:365–403

    Google Scholar 

  • Wilkinson N (1969) A brush with life. Seeley Service & Co, London

    Google Scholar 

  • Wilkinson D, Sherratt TN (2008) The art of concealment. Biologist 55:10–15

    Google Scholar 

  • Williams D (2001) Naval camouflage 1914–1945. A complete visual reference. Naval Institute Press, Annapolis

    Google Scholar 

  • Yamazaki K (2010) Leaf mines as visual defensive signals to herbivores. Oikos 119:796–801

    Google Scholar 

  • Yu F, Fu A, Aluru M, Park S, Xu Y, Liu H, Liu X, Foudree A, Nambogga M, Rodermel S (2007) Variegation mutants and mechanisms of chloroplast biogenesis. Plant Cell Environ 30:350–365

    PubMed  CAS  Google Scholar 

  • Zheng S-J, Snoeren TAL, Hogewoning SW, van Loon JJA, Dicke M (2010) Disruption of plant carotenoid biosynthesis through virus-induced gene silencing affects oviposition behaviour of the butterfly Pieris rapae. New Phytol 186:733–745

    PubMed  CAS  Google Scholar 

  • Zohary M (1962) Plant life of Palestine. Israel and Jordan. Ronald Press, New York, NY

    Google Scholar 

  • Zohary M (1973) Geobotanical foundations of the Middle East. Gustav Fischer, Stuttgart

    Google Scholar 

  • Zohary M (1983) Man and vegetation in the Middle East. In: Holzner W, Werger MJA, Ikusima I (eds) Man’s impact on vegetation. Dr W. Junk, The Hague, pp 287–295

    Google Scholar 

  • Zohary D, Hopf M, Weiss E (2012) Domestication of plants in the Old World, 4th edn. Clarendon, Oxford

    Google Scholar 

Download references

Acknowledgments

I thank Moshe Flaishman, Amots Dafni, Shahal Abbo, Ron Sederoff, Gidi Ne’eman, Moshe Inbar, Gadi Katzir, Ido Izhaki, Michal Ronel, Malka Halpern, Kevin Gould, Pilli Urbas, Martin Schaeffer, Marco Archetti, Pekka Niemelä, Jarmo Holopainen, Tamar Keasar, Aki Sinkkonen, and Kazuo Yamazaki for stimulating discussions and for field work or trips concerning defensive plant coloration. I thank Professor Lüttge and an anonymous reviewer for their valuable comments and suggestions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Simcha Lev-Yadun .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Lev-Yadun, S. (2015). The Proposed Anti-herbivory Roles of White Leaf Variegation. In: Lüttge, U., Beyschlag, W. (eds) Progress in Botany. Progress in Botany, vol 76. Springer, Cham. https://doi.org/10.1007/978-3-319-08807-5_10

Download citation

Publish with us

Policies and ethics