Evolutionary Ecology

, Volume 31, Issue 1, pp 1–20 | Cite as

The perceptual similarity of orb-spider prey lures and flower colours

  • Thomas E. White
  • Rhiannon L. Dalrymple
  • Marie E. Herberstein
  • Darrell J. Kemp
Original Paper

Abstract

Receiver biases offer opportunities for the evolution of deception in signalling systems. Many spiders use conspicuous body colouration to lure prey, yet the perceptual basis of such deception remains largely unknown. Here we use knowledge of visual perception in key pollinator groups (bees and flies) to test whether colour-based lures resemble floral signals. We addressed this question at two levels: first according to the spectral reflectance of Australian orb-web spiders and flowers across a broad continental range, and second in reference to polymorphic variation in the species Gasteracantha fornicata. Analysis at the community level supported the hypotheses for broad-scale convergence among spider and flower signals. Moreover, data for G. fornicata indicate that each lure morph presents a signal biased towards the colouration of sympatric flowers. This analysis identified fly- and/or bee-pollinated plants whose flowers are likely to be indistinguishable from each G. fornicata colour morph. Our findings support the hypothesis that deceptive colour-based lures exploit prey preferences for floral resources. Further, the evidence implies a greater role for specific model/mimic relationships over generalised resemblance to flower-like stimuli as a driver of lure colouration and diversity.

Keywords

Deception Communication Signal Predation Flower Spider Mimicry 

Notes

Acknowledgements

TEW was supported by an Australian Postgraduate Award and the Australasian Evolution Society, and thanks Elizabeth Mulvenna for all her support. DJK was supported by the Australian Research Council (Grant DP140104107). RLD was supported by an Australian Postgraduate Award, UNSW Research Excellence Award, an E&ERC Postgraduate Research Start-Up Grant, and the Wiley Blackwell fundamental ecology award. We thank Manuel Leal, John Endler, and anonymous reviewers for valuable comments.

Supplementary material

10682_2016_9876_MOESM1_ESM.pdf (284 kb)
Supplementary material 1 (PDF 283 kb)

References

  1. Adams DC, Anthony CD (1996) Using randomization techniques to analyse behavioural data. Anim Behav 51:733–738CrossRefGoogle Scholar
  2. Ames A (2000) CNS energy metabolism as related to function. Brain Res Rev 34:42–68CrossRefPubMedGoogle Scholar
  3. Avarguès-Weber A, de Brito Sanchez MG, Giurfa M, Dyer AG (2010) Aversive reinforcement improves visual discrimination learning in free-flying honeybees. PLoS ONE 5:e15370CrossRefPubMedPubMedCentralGoogle Scholar
  4. Basset Y (2001) Invertebrates in the canopy of tropical rain forests how much do we really know? In: Linsenmair KE, Davis CM, Fiala B, Speight MR (eds) Tropical forest canopies: ecology and management. Springer, Berlin, pp 87–107CrossRefGoogle Scholar
  5. Basset Y, Cizek L, Cuénoud P, Didham RK, Guilhaumon F, Missa O, Novotny V et al (2012) Arthropod diversity in a tropical forest. Science 338:1481–1484CrossRefPubMedGoogle Scholar
  6. Bernhardt P (1984) The pollination biology of Hibbertia stricta (dilleniaceae). Plant Syst Evol 147:267–277CrossRefGoogle Scholar
  7. Bernhardt P (1986) Bee-pollination in Hibbertia fasciculata (dilleniaceae). Plant Syst Evol 152:231–241CrossRefGoogle Scholar
  8. Blamires SJ, Hou C, Chen L-F, Liao CP, Tso I-M (2014) A predator’s body coloration enhances its foraging profitability by day and night. Behav Ecol Sociobiol 8:1253–1260CrossRefGoogle Scholar
  9. Brembs B, de Ibarra NH (2006) Different parameters support generalization and discrimination learning in Drosophila at the flight simulator. Learn Memory 13:629–637CrossRefGoogle Scholar
  10. Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510CrossRefPubMedGoogle Scholar
  11. Burley NT, Symanski R (1998) A taste for the beautiful: latent aesthetic mate preferences for white crests in two species of Australian grassfinches. Am Nat 152:792–802PubMedGoogle Scholar
  12. Bush AA, Yu DW, Herberstein ME (2008) Function of bright coloration in the wasp spider Argiope bruennichi (Araneae : Araneidae). Proc R Soc B 275:1337–1342CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chiao C-C, Wu W-Y, Chen S-H, Yang E-C (2009) Visualization of the spatial and spectral signals of orb-weaving spiders, Nephila pilipes, through the eyes of a honeybee. J Exp Biol 212:2269–2278CrossRefPubMedGoogle Scholar
  14. Chittka L (1992) The colour hexagon: a chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. J Comp Physiol A 170:533–543Google Scholar
  15. Chittka L, Döring TF (2007) Are autumn foliage colors red signals to aphids? PLoS Biol 5:e187CrossRefPubMedPubMedCentralGoogle Scholar
  16. Chittka L, Shmida A, Troje N, Menzel R (1994) Ultraviolet as a component of flower reflections, and the colour perception of hymenoptera. Vis Res 34:1489–1508CrossRefPubMedGoogle Scholar
  17. Chittka L, Dyer AG, Bock F, Dornhaus A (2003) Psychophysics: bees trade off foraging speed for accuracy. Nature 424:388CrossRefPubMedGoogle Scholar
  18. Chittka L, Skorupski P, Raine NE (2009) Speed–accuracy tradeoffs in animal decision making. Trends Ecol Evol 24:400–407CrossRefPubMedGoogle Scholar
  19. Christy JH (1995) Mimicry, mate choice, and the sensory trap hypothesis. Am Nat 146:171–181CrossRefGoogle Scholar
  20. Christy JH, Backwell PRY (1995) The sensory exploitation hypothesis. Trends Ecol Evol 10:417CrossRefPubMedGoogle Scholar
  21. Christy JH, Baum JK, Backwell PR (2003a) Attractiveness of sand hoods built by courting male fiddler crabs, Uca musica: test of a sensory trap hypothesis. Anim Behav 66:89–94CrossRefGoogle Scholar
  22. Christy J, Backwell P, Schober U (2003b) Interspecific attractiveness of structures built by courting male fiddler crabs: experimental evidence of a sensory trap. Behav Ecol Sociobiol 53:84–91Google Scholar
  23. Chuang CY, Yang EC, Tso I-M (2008) Deceptive color signaling in the night: a nocturnal predator attracts prey with visual lures. Behav Ecol 19:237–244CrossRefGoogle Scholar
  24. Craig CL (1994) Limits to learning—effects of predator pattern and color on perception and avoidance learning by prey. Anim Behav 47:1087–1099CrossRefGoogle Scholar
  25. Craig CL, Ebert K (1994) Colour and pattern in predator–prey interactions: the bright body colours and patterns of a tropical orb-spinning spider attract flower-seeking prey. Funct Ecol 8:616–620CrossRefGoogle Scholar
  26. Craig CL, Weber RS, Bernard GD (1996) Evolution of predator-prey systems: spider foraging plasticity in response to the visual ecology of prey. Am Nat 147:205–229CrossRefGoogle Scholar
  27. Cummings ME (2007) Sensory trade-offs predict signal divergence in surfperch. Evolution 61:530–545CrossRefPubMedGoogle Scholar
  28. Dalrymple R, Kemp D, Flores-Moreno H, Laffan S, White T, Hemmings F, Tindall M, Moles AT (2015) Birds, butterflies and flowers in the tropics are not more colourful than those in higher latitudes. Global Ecol Biogeogr 24:848–860CrossRefGoogle Scholar
  29. Department of Primary Industries, Parks, Water and Environment, Tasmania (2012) Listing Statement for Zieria veronicea subsp. veronicea (pink zieria), pp 1–5Google Scholar
  30. Dyer AG, Chittka L (2004a) Bumblebees (Bombus terrestris) sacrifice foraging speed to solve difficult colour discrimination tasks. J Comp Physiol A 190:759–763Google Scholar
  31. Dyer AG, Chittka L (2004b) Fine colour discrimination requires differential conditioning in bumblebees. Naturwissenschaften 91:224–227CrossRefPubMedGoogle Scholar
  32. Dyer AG, Murphy AH (2009) Honeybees choose “incorrect” colors that are similar to target flowers in preference to novel colors. Isr J Plant Sci 57:203–210CrossRefGoogle Scholar
  33. Dyer A, Neumeyer C (2005) Simultaneous and successive colour discrimination in the honeybee (Apis mellifera). J Comp Physiol A 191:547–557CrossRefGoogle Scholar
  34. Dyer AG, Spaethe J, Prack S (2008) Comparative psychophysics of bumblebee and honeybee colour discrimination and object detection. J Comp Physiol A 194:617–627CrossRefGoogle Scholar
  35. Dyer AG, Boyd-Gerny S, McLoughlin S, Rosa MGP, Simonov V, Wong BBM (2012) Parallel evolution of angiosperm colour signals: Common evolutionary pressures linked to hymenopteran vision. Proc R Soc B 279:3606–3615CrossRefPubMedPubMedCentralGoogle Scholar
  36. Elliott NB, Elliott WM (1991) Effect of an ambush predator, Phymata americana melin, on behavior of insects visiting Daucus carota. Am Midl Nat 126:198–202CrossRefGoogle Scholar
  37. Endler JA, Basolo AL (1998) Sensory ecology, receiver biases and sexual selection. Trends Ecol Evol 13:415–420CrossRefPubMedGoogle Scholar
  38. Endler JA, Mielke PW (2005) Comparing entire colour patterns as birds see them. Biol J Linn Soc 86:405–431CrossRefGoogle Scholar
  39. Fukushi T (1994) Colour perception of single and mixed monochromatic lights in the blowfly Lucilia cuprina. J Comp Physiol A 175:15–22CrossRefGoogle Scholar
  40. Fuller RC (2002) Lighting environment predicts the relative abundance of male colour morphs in bluefin killifish (Lucania goodei) populations. Proc R Soc Lond Ser B 269:1457–1465CrossRefGoogle Scholar
  41. Gaskett AC, Herberstein ME (2010) Colour mimicry and sexual deception by tongue orchids (cryptostylis). Naturwissenschaften 97:97–102CrossRefPubMedGoogle Scholar
  42. Gaskett A, Winnick C, Herberstein ME (2008) Orchid sexual deceit provokes ejaculation. Am Nat 171:E206–E212CrossRefPubMedGoogle Scholar
  43. Gigord LDB, Macnair MR, Stritesky M, Smithson A (2002) The potential for floral mimicry in rewardless orchids: an experimental study. Proc R Soc B 269:1389–1395CrossRefPubMedPubMedCentralGoogle Scholar
  44. Govardovskii V, Fyhrquist N, Reuter T, Kuzmin D, Donner K (2000) In search of the visual pigment template. Vis Neurosci 17:509–528CrossRefPubMedGoogle Scholar
  45. Gumbert A (2000) Color choices by bumble bees (Bombus terrestris): innate preferences and generalization after learning. Behav Ecol Sociobiol 48:36–43CrossRefGoogle Scholar
  46. Hauber ME (2002) Conspicuous colouration attracts prey to a stationary predator. Ecol Entomol 27:686–691CrossRefGoogle Scholar
  47. Heiling AM, Herberstein ME (2004) Predator-prey coevolution: Australian native bees avoid their spider predators. Proc R Soc B 271:S196–S198CrossRefPubMedPubMedCentralGoogle Scholar
  48. Heiling AM, Chittka L, Cheng K, Herberstein ME (2005) Colouration in crab spiders: substrate choice and prey attraction. J Exp Biol 208:1785–1792CrossRefPubMedGoogle Scholar
  49. Herberstein M, Craig C, Coddington J, Elgar M (2000) The functional significance of silk decorations of orb-web spiders: a critical review of the empirical evidence. Biol Rev 75:649–669CrossRefPubMedGoogle Scholar
  50. Herberstein ME, Heiling AM, Cheng K (2009) Evidence for UV-based sensory exploitation in Australian but not European crab spiders. Evol Ecol 23:621–634CrossRefGoogle Scholar
  51. Hoese F, Law E, Rao D, Herberstein M (2006) Distinctive yellow bands on a sit-and-wait predator: Prey attractant or camouflage? Behaviour 143:763–781CrossRefGoogle Scholar
  52. Internicola AI, Page PA, Bernasconi G, Gigord LDB (2007) Competition for pollinator visitation between deceptive and rewarding artificial inflorescences: an experimental test of the effects of floral colour similarity and spatial mingling. Funct Ecol 21:864–872CrossRefGoogle Scholar
  53. Kagawa K, Takimoto G (2016) Inaccurate color discrimination by pollinators promotes evolution of discrete color polymorphism in food-deceptive flowers. Am Nat 187:194–204CrossRefPubMedGoogle Scholar
  54. Keighery G (1975) Pollination of Hibbertia hypericoides (dilleniaceae) and its evolutionary significance. Journal of Natural History 9:681–684CrossRefGoogle Scholar
  55. Kemp DJ, Holmes C, Congdon BC, Edwards W (2013) Color polymorphism in spiny spiders (Gasteracantha fornicata): testing the adaptive significance of a geographically clinal lure. Ethology 119:1126–1137CrossRefGoogle Scholar
  56. Kelly M, Gaskett A (2014) UV reflectance but no evidence for colour mimicry in a putative brood-deceptive orchid Corybas cheesemanii. Curr Zool 60:104–113CrossRefGoogle Scholar
  57. Kemp DJ, Herberstein ME, Fleishman LJ, Endler JA, Bennett ATD, Dyer AG, Hart NS, Marshal J, Whiting MJ (2015) An integrative framework for the appraisal of coloration in nature. Am Nat 185:705–724CrossRefPubMedGoogle Scholar
  58. Kirschfeld K, Feiler R, Franceschini N (1978) A photostable pigment within the rhabdomere of fly photoreceptors no. 7. J Comp Physiol 125:275–284CrossRefGoogle Scholar
  59. Leal M, Fleishman LJ (2002) Evidence for habitat partitioning based on adaptation to environmental light in a pair of sympatric lizard species. Proc R Soc Lond B 269:351–359CrossRefGoogle Scholar
  60. Levi HW (1978) The American orb-weaver genera Colphepeira, Micrathena, and Gasteracantha north of mexico (Araneae, Araneidae). Bull Mus Comp Zool 148:417–442Google Scholar
  61. Lunau K (2014) Visual ecology of flies with particular reference to colour vision and colour preferences. J Comp Physiol A 200:1–16CrossRefGoogle Scholar
  62. Maia R, Eliason CM, Bitton P-P, Doucet SM, Shawkey MD (2013) Pavo: an r package for the analysis, visualization and organization of spectral data. Methods Ecol Evol 4:906–913Google Scholar
  63. Moran D, Softley R, Warrant EJ (2015) The energetic cost of vision and the evolution of eyeless Mexican cavefish. Sci Adv 1:e1500363CrossRefPubMedPubMedCentralGoogle Scholar
  64. Morante J, Desplan C (2008) The color-vision circuit in the medulla of Drosophila. Curr Biol 18:553–565CrossRefPubMedPubMedCentralGoogle Scholar
  65. Morawetz L, Svoboda A, Spaethe J, Dyer AG (2013) Blue colour preference in honeybees distracts visual attention for learning closed shapes. J Comp Physiol A 199:817–827CrossRefGoogle Scholar
  66. Nentwig W (1987) The prey of spiders. In: Nentwig W (ed) Ecophysiology of spiders. Springer, Berlin, pp 249–263Google Scholar
  67. Niven JE, Anderson JC, Laughlin SB (2007) Fly photoreceptors demonstrate energy-information trade-offs in neural coding. PLoS Biol 5:e116CrossRefPubMedPubMedCentralGoogle Scholar
  68. O’Hanlon JC, Holwell GI, Herberstein ME (2014a) Predatory pollinator deception: Does the orchid mantis resemble a model species? Curr Zool 60:90–103CrossRefGoogle Scholar
  69. O’Hanlon JC, Holwell GI, Herberstein ME (2014b) Pollinator deception in the orchid mantis. Am Nat 183:126–132CrossRefPubMedGoogle Scholar
  70. O’Hanlon J, Herberstein M, Holwell G (2014c) Habitat selection in a deceptive predator: maximizing resource availability and signal efficacy. Behav Ecol 26:194–199CrossRefGoogle Scholar
  71. Peng P, Blamires SJ, Agnarsson I, Lin H-C, Tso I-M (2013) A color-mediated mutualism between two arthropod predators. Curr Biol 23:172–176CrossRefPubMedGoogle Scholar
  72. Peter CI, Johnson SD (2008) Mimics and magnets: the importance of color and ecological facilitation in floral deception. Ecology 89:1583–1595CrossRefPubMedGoogle Scholar
  73. Poisot T (2011) The digitize Package: extracting numerical data from scatterplots. R J 25:3–5Google Scholar
  74. Prokopy RJ, Owens ED (1983) Visual detection of plants by herbivorous insects. Annu Rev Entomol 28:337–364CrossRefGoogle Scholar
  75. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  76. Rao D, Castañeda-Barbosa E, Nuñez-Beverido N, Díaz-Fleischer F (2015) Foraging benefits in a colour polymorphic neotropical orb web spider. Ethology 121:187–195CrossRefGoogle Scholar
  77. Renoult JP, Valido A, Jordano P, Schaefer HM (2014) Adaptation of flower and fruit colours to multiple, distinct mutualists. New Phytol 201:678–686CrossRefPubMedGoogle Scholar
  78. Ryan MJ, Cummings ME (2013) Perceptual biases and mate choice. Annu Rev Ecol Evol Syst 44:437–459CrossRefGoogle Scholar
  79. Salcedo E, Huber A, Henrich S, Chadwell LV, Chou WH, Paulsen R, Britt SG (1999) Blue-and green-absorbing visual pigments of Drosophila: ectopic expression and physiological characterization of the r8 photoreceptor cell-specific rh5 and rh6 rhodopsins. J Neurosci 19:10716–10726PubMedGoogle Scholar
  80. Skorupski P, Spaethe J, Chittka L (2006) Visual search and decision making in bees: time, speed, and accuracy. Int J Comp Psychol 19:342–357Google Scholar
  81. Spaethe J, Streinzer M, Eckert J, May S, Dyer A (2014) Behavioural evidence of colour vision in free flying stingless bees. J Comp Physiol A 200:485–496CrossRefGoogle Scholar
  82. Stevens M, Cuthill IC, Windsor AMM, Walker HJ (2006) Disruptive contrast in animal camouflage. Proc R Soc B 273:2433–2438CrossRefPubMedPubMedCentralGoogle Scholar
  83. Stoddard MC, Stevens M (2011) Avian vision and the evolution of egg color mimicry in the common cuckoo. Evolution 65:2004–2013CrossRefPubMedGoogle Scholar
  84. Stork NE (1988) Insect diversity: facts, fiction and speculation. Biol J Linn Soc 35:321–337CrossRefGoogle Scholar
  85. Stuart-Fox D, Moussalli A, Whiting MJ (2007) Natural selection on social signals: signal efficacy and the evolution of chameleon display coloration. Am Nat 170:916–930CrossRefPubMedGoogle Scholar
  86. Sutherland JP, Sullivan MS, Poppy GM (1999) The influence of floral character on the foraging behaviour of the hoverfly, Episyrphus balteatus. Entomol Exp Appl 93:157–164CrossRefGoogle Scholar
  87. Troje N (1993) Spectral categories in the learning behaviour of blowflies. Zeitschrift fur Naturforschung C 48:96Google Scholar
  88. Tso I-M, Tai P-L, Ku T-H, Kuo C-H, Yang E-C (2002) Colour-associated foraging success and population genetic structure in a sit-and-wait predator Nephila maculata (Araneae: Tetragnathidae). Anim Behav 63:175–182CrossRefGoogle Scholar
  89. Tso I-M, Lin C-W, Yang E-C (2004) Colourful orb-weaving spiders, Nephila pilipes, through a bee’s eyes. J Exp Biol 207:2631–2637CrossRefPubMedGoogle Scholar
  90. Tso I-M, Wu H-C, Hwang I-R (2005) Giant wood spider Nephila pilipes alters silk protein in response to prey variation. J Exp Biol 208:1053–1061CrossRefPubMedGoogle Scholar
  91. Tso I-M, Liao CP, Huang RP, Yang EC (2006) Function of being colorful in web spiders: Attracting prey or camouflaging oneself? Behav Ecol 17:606–613CrossRefGoogle Scholar
  92. Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc Lond Ser B 265:351–358CrossRefGoogle Scholar
  93. Vorobyev M, Brandt R, Peitsch D, Laughlin SB, Menzel R (2001) Colour thresholds and receptor noise: behaviour and physiology compared. Vis Res 41:639–653CrossRefPubMedGoogle Scholar
  94. Warrant EJ (2008) Seeing in the dark: vision and visual behaviour in nocturnal bees and wasps. J Exp Biol 211:1737–1746CrossRefPubMedGoogle Scholar
  95. White TE, Kemp DJ (2015) Technicolour deceit: a sensory basis for the study of colour-based lures. Anim Behav 105:231–243CrossRefGoogle Scholar
  96. White TE, Kemp DJ (2016) Colour polymorphic lures target different visual channels in prey. Evolution 70:1398–1408CrossRefPubMedGoogle Scholar
  97. White TE, Dalrymple RL, Noble DWA, O’Hanlon JC, Zurek DB, Umbers KDL (2015) Reproducible research in the study of biological coloration. Anim Behav 106:51–57CrossRefGoogle Scholar
  98. Wood B, Wood D (1998) Flowers of the south coast and ranges of New South Wales: a field guide. Wood’s BooksGoogle Scholar
  99. Yamaguchi S, Desplan C, Heisenberg M (2010) Contribution of photoreceptor subtypes to spectral wavelength preference in Drosophila. Proc Natl Acad Sci 107:5634–5639CrossRefPubMedPubMedCentralGoogle Scholar
  100. Zschokke S, Hénaut Y, Benjamin SP, García-Ballinas JA (2006) Prey-capture strategies in sympatric web-building spiders. Can J Zool 84:964–973CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Thomas E. White
    • 1
  • Rhiannon L. Dalrymple
    • 1
    • 2
  • Marie E. Herberstein
    • 1
  • Darrell J. Kemp
    • 1
  1. 1.Department of Biological ScienceMacquarie UniversitySydneyAustralia
  2. 2.Evolution and Ecology Research Centre, School of Biological, Earth, and Environmental SciencesUniversity of New South WalesSydneyAustralia

Personalised recommendations