Abstract
SUMMARY Australian crab spiders Thomisus spectabilis ambush pollinating insects, such as honeybees (Apis mellifera) on flowers, and can change their body colour between yellow and white. It is traditionally assumed that the spiders change their colour to match the flower colour, thus rendering them cryptic to insect prey. Here, we test this assumption combining state-of-the-art knowledge of bee vision and behavioural experiments. In the field, yellow spiders are only found on yellow daisies(Chrysanthemum frutescens), whereas white spiders are found on yellow and white daisies. These field patterns were confirmed in the laboratory. When given the choice between white and yellow daisies, yellow spiders preferred yellow daisies, whereas white spiders showed only a slight but non-significant preference for white flowers. Thus, T. spectabilis select background colours according to their own body colour. When viewed from a distance, bees use an achromatic signal produced by their green receptors for target detection. Through this visual channel, white spiders on white flowers, and yellow spiders on yellow flowers are virtually undetectable. From a closer distance of a few centimetres, when bees evaluate colour contrast, the combination of spider colour against different flower backgrounds affected the response of honeybees, but not in ways predicted by a classical crypsis/conspicuousness interpretation. Yellow spiders on yellow flowers are not perfectly matched when interpreted through the colour vision of a honeybee. Nevertheless, honeybees showed indifference to the presence of a spider, equally landing on vacant or spider-occupied flowers. Likewise, white spiders are poorly hidden on white flowers, as white spiders reflect ultraviolet light strongly, while white flowers do not. Surprisingly, bees are attracted to this contrast, and significantly more honeybees preferred white flowers occupied by white spiders. White spiders on yellow flowers produce the highest colour contrast and bees again preferred spider-occupied flowers. Yellow spiders on white flowers were the only pairing where bees rejected spider-occupied flowers, especially in cases where the contrast between the two was relatively strong. Thus, T. spectabilis select flower colours adaptively in a way that deceives honeybees, or at least does not deter them.
References
54
Referenced
91
-
Backhaus, W. (1991). Color opponent coding in the visual system of the honeybee. Vision Res.31,1381-1397.
(
10.1016/0042-6989(91)90059-E
) - Barth, F. G., Makagawa, T. and Eguchi, E.(1993). Vision in the ctenid spider Cupiennius salei:spectral range and absolute sensitivity (ERG). J. Exp. Biol.181,187-193.
-
Briscoe, A. D. and Chittka, L. (2001). The evolution of colour vision in insects. Ann. Rev. Entomol.46,471-510.
(
10.1146/annurev.ento.46.1.471
) -
Bruce, M. J., Herberstein, M. E. and Elgar, M. A.(2001). Signalling conflict between prey and predator attraction. J. Evol. Biol.14,786-794.
(
10.1046/j.1420-9101.2001.00326.x
) - Chien, S. A. and Morse, D. H. (1998). The role of prey and flower quality in the choice of hunting sites by adult male crab spiders Misumena vatia (Araneae, Thomisidae). J. Arachnol.26,238-243.
-
Chittka, L. (1996). Optimal sets of colour receptors and opponent processes for coding of natural objects in insect vision. J. Theor. Biol.181,179-196.
(
10.1006/jtbi.1996.0124
) -
Chittka, L. (2001). Camouflage of predatory crab spiders on flowers and the colour perception of bees (Aranida:Thomisidae/Hymenoptera: Apidae). Entomol. Gener.25,181-187.
(
10.1127/entom.gen/25/2001/181
) -
Chittka, L. and Menzel, R. (1992). The evolutionary adaptation of flower colours and the insect pollinators' colour vision. J. Comp. Physiol. A171,171-181.
(
10.1007/BF00188925
) -
Chittka, L. and Tautz, J. (2003). The spectral input to honeybee visual odometry. J. Exp. Biol.206,2393-2397.
(
10.1242/jeb.00436
) -
Chittka, L., Shmida, A., Troje, N. and Menzel, R.(1994). Ultraviolet as a component of flower reflections, and the colour perception of hymenoptera. Vision Res.34(11),1489-1508.
(
10.1016/0042-6989(94)90151-1
) -
Corronca, J. A. and Teran, H. R. (2000). Optical structure of the crab spider Misumenops pallens (Araneae,Thomisidae). J. Arachnol.28(1),16-22.
(
10.1636/0161-8202(2000)028[0016:OSOTCS]2.0.CO;2
) -
De Voe, R. (1975). Ultraviolet and green receptors in principal eyes of jumping spiders. J. Gener. Physiol.66,193-207.
(
10.1085/jgp.66.2.193
) -
Dyer, A. G. and Chittka, L. (2004). Biological significance of discriminating between similar colours in spectrally variable illumination: bumblebees as a study case. J. Comp. Physiol.A190,105-114.
(
10.1007/s00359-003-0475-2
) -
Endler, J. A. (1991). Variation in the appearance of guppy color patterns to guppies and their predators under different visual conditions. Vision Res.31,587-608.
(
10.1016/0042-6989(91)90109-I
) - Endler, J. A. (1993). Some general comments on the evolution and design of animal communication systems. Phil. Trans. R. Soc. Lond. B340,215-225.
- Endler, J. A. (1999). Evolutionary implications of the interaction between animal signals and the environment. In Animal Signals. Signalling and Signal Design in Animal Communication (ed. Y. Espmark, T. Amundsen and G. Rosenqvist),pp. 11-46. Trondheim, Norway: The Royal Norwegian Society of Science and Letters, The Foundation Tapir Publishers.
-
Endler, J. A. and Théry, M. (1996). Interacting effects of lek placement, display behavior, ambient light, and color patterns in three Neotropical forest-dwelling birds. Am. Nat.148,421-452.
(
10.1086/285934
) -
Endler, J. A. and Basolo, A. L. (1998). Sensory ecology, receiver biases and sexual selection. Trends Ecol. Evol.13,415-420.
(
10.1016/S0169-5347(98)01471-2
) -
Gamble, S., Lindholm, A. K., Endler, J. A. and Brooks, R.(2003). Environmental variation and the maintenance of polymorphism: the effect of ambient light spectrum on the mating behaviour and sexual selection in guppies. Ecol. Lett.6, 463-472.
(
10.1046/j.1461-0248.2003.00449.x
) -
Giurfa, M. and Lehrer, M. (2001). Honeybee vision and floral displays: From detection to close-up recognition. In Cognitive Ecology of Pollination (ed. L. Chittka and J. D. Thomson), pp. 61-82. Cambridge: Cambridge University Press.
(
10.1017/CBO9780511542268.005
) -
Giurfa, M., Vorobyev, M., Kevan, P. and Menzel, R.(1996). Detection of coloured stimuli by honeybees: Minimum visual angles and receptor specific contrasts. J. Comp. Physiol. A178,699-709.
(
10.1007/BF00227381
) -
Giurfa, M., Vorobyev, M., Brandt, R., Posner, B. and Menzel,R. (1997). Discrimination of coloured stimuli by honeybees:Alternative use of achromatic and chromatic signals. J. Comp. Physiol. A180,235-243.
(
10.1007/s003590050044
) -
Gumbert, A., Kunze, J. and Chittka, L. (1999). Floral colour diversity in plant communities, bee colour space and a null model. Proc. R. Soc. Lond. B266,1711-1716.
(
10.1098/rspb.1999.0836
) -
Harder, L. D., Williams, N. M., Jordan, C. Y. and Nelson, W. A. (2001). The effects of floral design and display on pollinator economics and pollen dispersal. In Cognitive Ecology of Pollination (ed L. Chittka and J. D. Thomson), pp.297-317. Cambridge: Cambridge University Press.
(
10.1017/CBO9780511542268.016
) -
Hauber, M. E. (1998). Web decorations and alternative foraging tactics of the spider Argiope appensa. Ethol. Ecol. Evol.10,47-54.
(
10.1080/08927014.1998.9522870
) - Heiling, A. M. and Herberstein, M. E. (2004a). Floral quality signals lure pollinators and their predators. Ann. Zool. Fennici41,421-428.
-
Heiling, A. M. and Herberstein, M. E. (2004b). Predator-prey co-evolution: Australian native bees avoid their spider predators. Proc. R. Soc. Lond. B271,196-198.
(
10.1098/rsbl.2003.0138
) -
Heiling, A. M., Herberstein, M. E. and Chittka, L.(2003). Crab spiders manipulate flower signals. Nature421,334.
(
10.1038/421334a
) -
Heiling, A. M., Cheng, K. and Herberstein, M. E.(2004). Exploitation of flower signals by crab spiders. Behav. Ecol.15,321-326.
(
10.1093/beheco/arh012
) -
Heindl, M. and Winkler, H. (2003). Interacting effects of ambient light and plumage color patterns in displaying wire-tailed Manakins (Aves, Pipridae). Behav. Ecol. Sociobiol.53,153-162.
(
10.1007/s00265-002-0562-3
) -
Hoffmeister, T. S. and Roitberg, B. D. (1998). Evolution of signal persistence under predator exploitation. Ecosci.5,312-320.
(
10.1080/11956860.1998.11682470
) -
Johnson, S. D. (2000). Batesian mimicry in the non-rewarding orchid, Disa pulchra, and its consequences for pollinator behaviour. Biol. J. Linn. Soc.71,119-132.
(
10.1006/bijl.1999.0430
) -
Johnstone, R. A. (1997). The tactics of mutual mate choice and competitive search. Behav. Ecol. Sociobiol.40,51-59.
(
10.1007/s002650050315
) - Krebs, J. R. and Dawkins, R. (1984). Animal signals: mind-reading and manipulation. In Behavioural Ecology: An Evolutionary Approach, 2nd edn (ed. J. R. Krebs and N. B. Davies), pp. 380-402. Oxford, UK:Blackwell.
- Lehrer, M., Horridge, G. A., Zhang, S. W. and Gadagkar, R.(1995). Shape vision in bees: innate preference for flower-like patterns. Phil. Trans. R. Soc. Lond. B347,123-137.
-
Lloyd, J. E. and Wing, S. R. (1983). Nocturnal aerial predation of fireflies by light-seeking fireflies. Science222,634-635.
(
10.1126/science.222.4624.634
) - Lunau, K. (1996). Signalling function of floral colour patterns for insect flower visitors. Zool. Anz.235, 11-30.
-
Lunau, K. (2000). The ecology and evolution of visual pollen signals. Plant Syst. Evol.222,89-111.
(
10.1007/BF00984097
) -
Nakamura, T. and Yamashita, S. (2000). Learning and discrimination of colored papers in jumping spiders (Araneae, Salticidae). J. Comp. Physiol. A186,897-901.
(
10.1007/s003590000143
) -
Oxford, G. S. and Gillespie, R. G. (1998). Evolution and Ecology of spider coloration. Annu. Rev. Entomol.43,619-643.
(
10.1146/annurev.ento.43.1.619
) -
Schaefer, H. M., Schaefer, V. and Levey, D. J.(2004). How plant-animal interactions signal new insights in communication. Trends Ecol. Evol.19,577-584.
(
10.1016/j.tree.2004.08.003
) - Schmalhofer, V. R. (1999). Thermal tolerances and preferences of the crab spiders Misumenops asperatus and Misumenoides formosipes (Araneae, Thomisidae). J. Arachnol.27,470-480.
-
Seah, W. K. and Li, D. (2001). Stabilimenta attract unwelcome predators to orb-webs. Proc. R. Soc. Lond. B268,1553-1558.
(
10.1098/rspb.2001.1709
) -
Silberglied, R. E. (1979). Communication in the ultraviolet. Ann. Rev. Ecol. Syst.10,373-398.
(
10.1146/annurev.es.10.110179.002105
) -
Smith, C., Barber, I., Wootton, R. J. and Chittka, L.(2004). A receiver bias in the origin of threespine stickleback mate choice. Proc. R. Soc. Lond. B271,949-955.
(
10.1098/rspb.2004.2690
) -
Spaethe, J. and Chittka, L. (2003). Interindividual variation of eye optics and signal object resolution in bumblebees. J. Exp. Biol.206,3447-3453.
(
10.1242/jeb.00570
) -
Spaethe, J., Tautz, J. and Chittka, L. (2001). Visual constraints in foraging bumblebees: Flower size and color affect search time and flight behavior. Proc. Nat. Acad. Sci. USA98,3898-3903.
(
10.1073/pnas.071053098
) -
Théry, M. and Casas, J. (2002). Predator and prey views of spider camouflage. Nature415, 133.
(
10.1038/415133a
) -
Théry, M., Debut, M., Gomez, D. and Casas, J.(2005). Specific color sensitivities of prey and predator explain camouflage in different visual systems. Behav. Ecol.16, 25-29.
(
10.1093/beheco/arh130
) -
Tso, I. M., Lin, C. W. and Yang, E. C. (2004). Colourful orb-weaving spiders, Nephila pilipes, through a bee's eyes. J. Exp. Biol.207,2631-2637.
(
10.1242/jeb.01068
) - Tuttle, M. D. and Ryan, M. J. (1981). Bat predation and the evolution of frog vocalisation in the Neotropics. Nature214,677-678.
-
Vorobyev, M. and Osorio, D. (1998). Receptor noise as a determinant of colour thresholds. Proc. R. Soc. Lond.265,351-358.
(
10.1098/rspb.1998.0302
) -
Vorobyev, M., Brandt, R., Peitsch, D., Laughlin, S. B. and Menzel, R. (2001). Colour thresholds and receptor noise:behaviour and physiology compared. Vision Res.41,639-653.
(
10.1016/S0042-6989(00)00288-1
) -
Yamashita, S. and Tadeda, H. (1983). Cerebral photosensitive neurons in the orb weaving spiders, Argiope bruennichiand A. amoena. J. Comp. Physiol. A150,467-472.
(
10.1007/BF00609572
)
Dates
Type | When |
---|---|
Created | 20 years, 3 months ago (May 5, 2005, 2:13 p.m.) |
Deposited | 4 years, 3 months ago (April 25, 2021, 7:20 a.m.) |
Indexed | 1 year ago (Aug. 17, 2024, 1:09 p.m.) |
Issued | 20 years, 3 months ago (May 15, 2005) |
Published | 20 years, 3 months ago (May 15, 2005) |
Published Print | 20 years, 3 months ago (May 15, 2005) |
@article{Heiling_2005, title={Colouration in crab spiders: substrate choice and prey attraction}, volume={208}, ISSN={0022-0949}, url={http://dx.doi.org/10.1242/jeb.01585}, DOI={10.1242/jeb.01585}, number={10}, journal={Journal of Experimental Biology}, publisher={The Company of Biologists}, author={Heiling, Astrid M. and Chittka, Lars and Cheng, Ken and Herberstein, Marie E.}, year={2005}, month=may, pages={1785–1792} }