Abstract
Visual cues are known to be used by numerous animal taxa to gather information on quality and localisation of resources. Because environmental lighting can interfere with the spectral features of visual cues, the specific characteristics of the colour signals that promote forager decision and learning are still not known in the majority of insects (excepted in bees). We analysed the effect of previous experience on the use of visual information by the wasp Venturia canescens, a parasitoid of pyralidae, in the context of host searching. These parasitoids search for hosts concealed in several fruit species, so visual cues from the host microhabitat could play a key role in host finding. We also investigated the type of visual cues on which wasps based their decision. We tested whether wasps are able to associate an achromatic cue (brightness) or a chromatic one (hue, i.e. dominant wavelength and/or chroma) with the presence of hosts. Our results show that in the context of host foraging, chromatic cues are more reliable than brightness in achieving the associative learning process. Therefore, understanding the behavioural ecology of foraging should make use of the knowledge about the visual information used.
Similar content being viewed by others
References
Amat I, Bernstein C, Van Alphen JJM (2003) Does a deletion in a virus-like particle protein have pleiotropic effects on the reproductive biology of a parasitoid wasp? J Insect Physiol 49:1183–1188
Arthur AP (1971) Associative learning by Nemeritis canescens (Hymenoptera: Ichneumonidae). Can Entomol 103:1137–1141
Backhaus W, Menzel R (1987) Color distance derived from a receptor model of color vision in the honeybee. Biol Cybern 55:321–331
Baeder JM, King BH (2004) Associative learning of color by males of the parasitoid wasp Nasonia vitripennis (Hymenoptera: Pteromalidae). J Insect Behav 17:201–213
Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Ann Rev Entomol 46:471–510
Campbell SA, Borden JH (2009) Additive and synergistic integration of multimodal cues of both hosts and non-hosts during host selection by woodboring insects. Oikos 118:553–563
Castelo M, Corley JC, Desouhant E (2003) Conspecific avoidance during foraging in Venturia canescens (Hymenoptera: Ichneumonidae): the roles of host presence and conspecific densities. J Insect Behav 16:307–318
Chittka L (1992) The colour hexagon: a chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. J Comp Physiol A 170:533–543
Chittka L (1996) Does bee colour vision predate the evolution of flower colour? Naturwissenschaftern 83:136–138
Chittka L (1999) Bees, white flowers, and the color hexagon—a reassessment? No, not yet—comments on the contribution by Vorobyev et al. Naturwissenschaften 86:595–597
Chittka L, Waser NM (1997) Why red flowers are not invisible to bees. Isr J Plant Sci 45:169–183
Chittka L, Wells H (2004) Color vision in bees: mechanisms, ecology, and evolution. In: Prete FR (ed) Complex worlds from simpler nervous systems. Bradford Book, The MIT Press, Cambridge, pp 165–191
Chittka L, Beier W, Hertel H, Steinmann E, Menzel R (1992) Opponent color coding is a universal strategy to evaluate the photoreceptor inputs in Hymenoptera. J Comp Physiol A 170:545–563
Chittka L, Shmida A, Troje N, Manzel R (1994) Ultraviolet as a component of flower relections and the colour perception of hymenoptera. Vis Res 34:1489–1508
Corbet SA (1971) Mandibular gland secretion of larvae of the flour moth, Anagasta kuehniella, contains an epideictic pheromone and elicits oviposition movements in a Hymenopteran parasite. Nature 232:481–484
Desouhant E, Driessen G, Wielaard B, Lapchin L, Bernstein C (2003) Dispersal between host populations in field conditions: navigation rules in the parasitoid Venturia canescens. Ecol Entomol 28:257–267
Desouhant E, Driessen G, Amat I, Bernstein C (2005) Host and food searching in a parasitic wasp Venturia canescens: a trade-off between current and future reproduction? Anim Behav 70:145–152
Dyer AG (1998) The colour of flowers in spectrally variable illumination and insect pollinator vision. J Comp Physiol A 183:203–212
Dyer AG (2006) Bumblebees directly perceive variations in the spectral quality of illumination. J Comp Physiol A 192:333–338
Dyer AG, Whitney HM, Arnold SEJ, Glover BJ, Chittka L (2006) Bees associate warmth with floral colour. Nature 442:525
Endler JA (1990) On the measurement and classification of color in studies of animal color patterns. Biol J Linnean Soc 41:315–352
Endler JA (1993) The color of light in forests and its implications. Ecol Monogr 63:1–27
Endler JA, 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
Fisher S, Samietz J, Wackers FL, Dorn S (2003) Perception of achromatic cues during host location of pupal parasitoid. Entomol Exp Appl 106:63–66
Geervliet JBF, Vreugdenhil AI, Dicke M, Vet LEM (1998) Learning to discriminate between infochemicals from different plant-host complexes by the parasitoids Cotesia glomerata and C. rubecula. Entomol Exp Appl 86:241–252
Giurfa M, Vorobyev M (1998) The angular range of achromatic target detection by honey bees. J Comp Physiol A 183:101–110
Giurfa M, Vorobyev M, Kevan P, Menzel R (1996) Detection of coloured stimuli by honeybees: minimum visual angles and receptor specific contrasts. J Comp Physiol A 178:699–709
Gould JL (1993) Ethological and comparative perspectives on honey bee learning. In: Papaj DR, Lewis AC (eds) Insect learning: ecological and evolutionary perspectives. Chapman & Hall, New York, pp 18–50
Gray SM, McKinnon JS (2007) Linking color polymorphism maintenance and speciation. Trends Ecol Evol 22:71–79
Harvey JA, Thompson DJ (1995) Host behaviour and its influence on foraging and acceptance by the solitary parasitoid wasp, Venturia canescens (Hym: Ichneumonidae). Entomophaga 40:193–210
Håstad O, Victorsson J, Ödeen A (2005) Differences in color vision make passerines less conspicuous in the eyes of their predators. Proc Natl Acad Sci USA 102:6391–6394
Hawryshyn CW (1982) Studies of animal color-vision—comments on some important theoretical considerations. Can J Zool-Rev Can Zool 60:2968–2970
Horridge A (2009) What does an insect see? J Exp Bio 212:2721–2729
Kelber A, Vorobyev M, Osorio D (2003) Animal colour vision—behavioural tests and physiological concepts. Biol Rev 78:81–118
Kilkenny FF, Galloway LF (2008) Reproductive success in varying light environments: direct and indirect effects of light on plants and pollinators. Oecologia 155:247–255
Land MF (1997) Visual acuity in insects. Ann Rev Entomol 42:147–177
Lotto RB, Chittka L (2005) Seeing the light: illumination as a contextual cue to color choice behavior in bumblebees. Proc Natl Acad Sci USA 102:3852–3856
Lucchetta P, Bernstein C, Théry M, Lazzari C, Desouhant E (2008) Foraging and associative learning of visual signals in a parasitic wasp. Anim Cogn 11:525–533
Menzel R, Backhaus W (1991) Colour vision in insects. In: Gouras P (ed) Vision and visual dysfunction, Vol 6 the perception of colour. Macmillan, London, UK, pp 262–293
Menzel R, Greggers H, Hammer M (1993) Functional organization of appetitive learning and memory in a generalist pollinator, the honey bee. In: Papaj DR, Lewis AC (eds) Insect learning: ecological and evolutionary perspectives. Chapman & Hall, New York, pp 79–125
Messing RH, Jang EB (1992) Response of the fruit-fly parasitoid Diachasmimorpha longicaudata (Hymenoptera, Braconidae) to host-fruit stimuli. Env Entomol 21:1189–1195
Neumeyer C (1981) Chromatic adaptation in the honey bee: successive color contrast and color constancy. J Comp Physiol A 144:543–553
Oliai SE, King BH (2000) Associative learning in response to color in the parasitoid wasp Nasonia vitripennis (Hymenoptera: Pteromalidae). J Insect Behav 13:55–69
Papaj DJ, Lewis AC (1993) Insect learning. Ecological and evolutionary perspectives. Chapman & Hall, London
Papaj DR, Vet LEM (1990) Odor learning and foraging success in the parasitoid, Leptopilina heterotoma. J Chem Ecol 16:3137–3150
Peitsch D, Fietz A, Hertel H, Desouza J, Ventura DF, Menzel R (1992) The spectral input systems of Hymenopteran insects and their receptor-based color-vision. J Comp Physiol A 170:23–40
Raine NE, Chittka L (2007) The adaptive significance of sensory bias in a foraging context: floral colour preferences in the bumblebee Bombus terrestris. PLoS ONE 6:e556
Rogers D (1972) The ichneumon wasp Venturia canescens: oviposition and avoidance of superparasitism. Entomol Exp Appl 15:190–194
Salt G (1976) The hosts of Nemeritis canescens: a problem in the host specificity of insect parasitoids. Ecol Entomol 1:63–67
Segura DF, Viscarret MM, Carabajal Paladino LZ, Ovruski SM, Cladera JL (2007) Role of visual information and learning in habitat selection by a generalist parasitoid foraging for concealed hosts. Anim Behav 74:131–142
Shafir S (1996) Color discrimination conditioning of a wasp, Polybia occidentalis (Hymenoptera: Vespidae). Biotropica 28:243–251
Shafir S, Bechar A, Weber EU (2003) Cognition-mediated coevolution—context-dependent evaluations and sensitivity of pollinators to variability in nectar rewards. Plant Syst Evol 238:195–209
Spaethe J, Tautz J, Chittka L (2001) Visual constraints in foraging bumblebees: flower size and color affect search time and flight behavior. Proc Natl Acad Sci USA 98:3898–3903
Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, Princeton
R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org
Thorpe WH, Jones BA (1937) Olfactory conditioning in a parasitic insect and its relation to the problem of host selection. Proc R Soc B Biol Sci 124:56–81
Traynier RMM (1984) Associative learning in the ovipositional behavior of the cabbage butterfly, Pieris rapae. Phyiol Ent 9:465–472
Uy JAC, Endler JA (2004) Modification of the visual background increases the conspicuousness of golden-collared manakin displays. Behav Ecol 15:1003–1010
von Helversen O (1972) Zur spektralen Unterschiedsempfindlichkeit der Honigbiene. J Comp Physiol A 80:439–472
Vorobyev M, Brandt R (1997) How do insects discriminate colours? Israel J Plant Sci 45:103–113
Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc B Biol Sci 265:351–358
Wäckers FL, Lewis WJ (1999) A comparison of color-, shape- and pattern-learning by the hymenopteran parasitoid Microplitis croceipes. J Comp Physiol A 184:387–393
Wardle AR (1990) Learning of host microhabitat colour by Exeristes roborator (F.) (Hymenoptera: Ichneumonidae). Anim Behav 39:914–923
Acknowledgments
We are grateful to I. Amat for comments on the first version of the manuscript. We also thank A. Heizmann and F. Debias for keeping the wasp culture, R. Botalla for building the LEDs intensity controller and D. Gomez for the Avicol software used to compute visual contrasts and S. Dray. This work was supported by a grant allocated to E. Desouhant (ANR “jeunes chercheuses, jeunes chercheurs”, no. JCJC06_138616) and by CNRS UMR 7179. Experiments of this study comply with the current laws of the country (France) in which they were performed.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Desouhant, E., Navel, S., Foubert, E. et al. What matters in the associative learning of visual cues in foraging parasitoid wasps: colour or brightness?. Anim Cogn 13, 535–543 (2010). https://doi.org/10.1007/s10071-009-0304-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-009-0304-2