Abstract
Spontaneous colour preferences have been extensively studied in flower-visiting insects and such preferences exhibited by inexperienced flower-visiting insects are proposed to be adaptive by guiding them to the most rewarding flowers. Thus, spontaneous preferences are hypothesised to reflect the floral reward properties of the habitats in which these insects evolved. However, little is known about colour preferences in non-flower-visiting insects, and the ecological significance of such preferences. We investigated spontaneous colour preferences in the context of feeding and colour learning in the obligate fruit-feeding satyrine butterfly Mycalesis mineus. We report that M. mineus has true colour vision and naive butterflies, both males and females, did not prefer any colour in the absence of olfactory cues in a four-colour test array. Interestingly, females preferred yellow in the presence of food odour, indicating the modulatory effect of olfactory cues on spontaneous colour preferences. Further, when yellow was replaced with orange, female preference shifted to red, demonstrating the influence of colour combinations used in the test. We also report that M. mineus females rapidly learn to associate colour, both the preferred yellow and the non-preferred blue, with fermented banana as reward. Thus, for the first time, we report spontaneous colour preferences and colour learning in a non-flower-visiting butterfly. We also demonstrate that the colour preferences are sexually dimorphic in M. mineus and argue that multimodal stimuli are important for foraging decisions in fruit-feeding butterflies.
Significance statement
Spontaneous colour preferences exhibited by naive flower-visiting insects are thought to reflect sensory biases and are hypothesised to be adaptive as they guide insects to rewarding flowers. However, such colour preferences in non-flower-visiting insects and their adaptive significance remain unclear. We demonstrate that Mycalesis mineus, a fruit-feeding butterfly, has true colour vision and exhibits spontaneous colour preferences and these preferences are sexually dimorphic. We also demonstrate that colour preferences are modulated by olfactory cues and are influenced by colour combinations presented in tests. We also report that female butterflies rapidly learn to associate colour with rewards. Our results demonstrate that naive fruit-feeding butterflies rely on both visual and olfactory modalities and depend on spontaneous and learnt behaviours while making foraging decisions.
Similar content being viewed by others
References
Aduse-Poku K, Brattström O, Kodandaramaiah U, Lees DC, Brakefield PM, Wahlberg N (2015) Systematics and historical biogeography of the old world butterfly subtribe Mycalesina (Lepidoptera: Nymphalidae: Satyrinae). BMC Evol Biol 15:167
Andersson S (2003) Foraging responses in the butterflies Inachisio,Aglaisurticae (Nymphalidae), and Gonepteryx rhamni (Pieridae) to floral scents. Chemoecology 13:1–11
Andersson S, Dobson HEM (2003) Behavioral foraging responses by the butterfly Heliconius melpomene to Lantana camara floral scent. J Chem Ecol 29:2303–2318
Arikawa K, Wakakuwa M, Qiu X et al (2005) Sexual dimorphism of short-wavelength photoreceptors in the small white butterfly Pieris rapae. J Neurosci 25:5935–5942
Baker HG (1961) The adaptation of flowering plants to nocturnal and crepuscular pollinators. Q Rev Biol 36:64–73
Balamurali GS, Nicholls E, Somanathan H, Hempel de Ibarra N (2018) A comparative analysis of colour preferences in temperate and tropical social bees. Sci Nat 105
Balkenius A, Kelber A (2006) Colour preferences influences odour learning in the hawkmoth, Macroglossum stellatarum. Naturwissenschaften 93:255–258
Bernard GD, Remington CL (1991) Color vision in Lycaena butterflies: spectral tuning of receptor arrays in relation to behavioral ecology. Proc Natl Acad Sci U S A 88:2783–2787
Blackiston D, Briscoe AD, Weiss MR (2011) Color vision and learning in the monarch butterfly, Danaus plexippus (Nymphalidae). J Exp Biol 214:509–520
Chittka L, Thomson JD, Waser NM (1999) Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86:361–377
Cunningham JP (2004) Learning, odour preference and flower foraging in moths. J Exp Biol 207:87–94
DeVries PJ, Walla TR, Greeney HF (1999) Species diversity in spatial and temporal dimensions of fruit- feeding butterflies from two Ecuadorian rainforests. Biol J Linn So c68:333–353
Everett A, Tong X, Briscoe AD, Monteiro A (2012) Phenotypic plasticity in opsin expression in a butterfly compound eye complements sex role reversal. BMC Evol Biol 12:232–242
Giurfa M, Nunez J, Chittka L, Menzel R (1995) Colour preferences of flower-naive honeybees. J Comp Physiol A 177:247–259
Goyret J, Pfaff M, Raguso RA, Kelber A (2008) Why do Manduca sexta feed from white flowers? Innate and learnt colour preferences in a hawkmoth. Naturwissenschaften 95:569–576
Gumbert A (2000) Color choices by bumble bees (Bombus terrestris): innate preferences and generalization after learning. BehavEcol Sociobiol 48:36–43
Honda K, Omura H, Hayashi N (1998) Identification of floral volatiles from Ligustrum japonicum that stimulate flower-visiting by cabbage butterfly, Pieris rapae. J ChemEcol 24:2167–2180
Ilse D (1928) Llber den Farbensinn der Tagfalter. Z Vergl Physiol 8:658–692
Ilse D (1937) New observations on responses to colours in egg-laying butterflies. Nature 140:544–545
Ilse D (1949) Colour discrimination in the Dronefly, Eristalis tenax. Nature 163:255–256
Ilse D, Vaidya VG (1956) Spontaneous feeding response to colours in Papilio demoleus L. Proc Indian Acad Sci Sect B 43:23–31
Kandori I, Yamaki T (2012) Reward and non-reward learning of flower colours in the butterfly Byasa alcinous (lepidoptera: Papilionidae). Naturwissenschaften 99:705–713
Kandori I, Yamaki T, Okuyama S, Sakamoto N, Yokoi T (2009) Interspecific and intersexual learning rate differences in four butterfly species. J Exp Biol 212:3810–3816
Kay QON (1976) Preferential pollination of yellow-flowered morphs of Raphanus raphanistrum by Pieris and Eristalis. Nature 261:230–232
Kelber A (1997) Innate preferences for flower features in the hawkmoth Macroglossum stellatarum. J Exp Biol 200:827–836
Kinoshita M, Shimada N, Arikawa K (1999) Colour vision of the foraging swallowtail butterfly Papilio xuthus. J Exp Biol 202:95–102
Kinoshita M, Stewart FJ, Ômura H (2017) Multisensory integration in Lepidoptera: insights into flower-visitor interactions. Bio Essays 39:93–98
Kolb G, Scherer C (1982) Experiments on wavelength specific behavior of Pieris brassicae L. during drumming and egglaying. J Comp Physiol 149:325–332
Krenn HW, Zulka KP, Gatschnegg T (2001) Proboscis morphology and food preferences in nymphalid butterflies (Lepidoptera : Nymphalidae). J Zool 254:17–26
Kühn A, llse D (1925) Die Anlockung von Tagfalterndurch Pigmentfarben. Biol Zbl 45:144–149
Lehrer M, Horridge GA, Zhang SW, Gadagkar R (1995) Shape vision in bees: innate preference for flower-like patterns. Philos Trans R Soc B Biol Sci 347:123–137
Linnaeus C (1758) Systema naturae. Vol.1. Ed.10. L. Salvii, Stockholm
Lunau K (2014) Visual ecology of flies with particular reference to colour vision and colour preferences. J Comp Physiol A 200:497–512
Lunau K, Maier EJ (1995) Innate color preferences of flower visitors. J Comp Physiol A 177(1):–19
Lunau K, Wacht S (1994) Optical releasers of the innate proboscis extension in the hoverfly Eristalis tenax L. (Syrphidae, Diptera). J Comp Physiol A 174:575–579
McCulloch KJ, Osorio D, Briscoe AD (2016) Sexual dimorphism in the compound eye of nymphalid butterfly with at least five spectral classes of photoreceptor. J Exp Biol 219:2377 LP–2372387. https://doi.org/10.1242/jeb.136523
Molleman F, van Alphen ME, Brakefield PM, Zwaan BJ (2005) Preferences and food quality of fruit-feeding butterflies in Kibale forest, Uganda. Biotropica 37:657–663
Moré M, Sérsic AN, Cocucci AA (2007) Restriction of pollinator assemblage through flower length and width in three long tongued hawkmoth-pollinated species of Mandevilla (Apocynaceae, Apocynoideae). Ann Mo Bot Gard 94:485–504
Naumann CM, Ockenfels P, Schmitz J, Schmidt F, Francke W (1991) Reactions of Zygaena moths to volatile compounds of Knautia arvensis (Lepidoptera: Zygaenidae). Entomol Gen 15:255–264
Ogawa Y, Kinoshita M, Stavenga DG, Arikawa K (2013) Sex-specific retinal pigmentation results in sexually dimorphic long-wavelength-sensitive photoreceptors in the eastern pale clouded yellow butterfly. J Exp Biol 216:1916 LP–1911923. https://doi.org/10.1242/jeb.083485
Ômura H, Honda K (2005) Priority of color over scent during flower visitation by adult Vanessa indica butterflies. Oecologia 142:588–596
Osorio D, Vorobyev M (1996) Colour vision as an adaptation to frugivory in primates. Proc Soc B 263:593–599
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.URL http://www.R-project.org/
Raguso RA, Willis MA (2002) Synergy between visual and olfactory cues in nectar feeding by naïve hawkmoths, Manduca sexta. Anim Behav 64:685–695
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 2(6):1–8
Saji K, Kalesh S (2019) Mycalesis mineus Linnaeus, 1758 – dark-branded Bushbrown. Kunte K, Sondhi S, Roy P, (Es). Butterflies of India, v. 2.53. Indian Foundation for Butterflies. http://www.ifoundbutterflies.org/sp/768/Mycalesis-mineus
Satoh A, Kinoshita M, Arikawa K (2016) Innate preference and learning of colour in the male cotton bollworm moth, Helicoverpa armigera. J Exp Biol 219:3857–3860
Shihan TR (2016) An observation on the fruit feeding behavior of butterflies in some areas of Bangladesh. J Threat Taxa 8:9479–9485
Silberglied RE (1984) Visual communication and sexual selection among butterflies. In: Vane-Wright RI, Ackery PR (eds) The Biology of Butterflies (Symposium of the Royal Entomological Society of London, number 11). Academic Press, London, pp 207–223
Sourakov A, Sourakov A, Duehl A (2012) Foraging behavior of the blue morpho and other tropical butterflies: the chemical and electrophysiological basis of olfactory preferences and the role of color. Psyche 2012:1–10
Stanton ML, Snow AA, Handel SN (1986) Floral evolution: attractiveness to pollinators increases male fitness. Science 232(80):1625 LP–1621627. https://doi.org/10.1126/science.232.4758.1625
Swihart CA (1971) Colour discrimation by the butterfly Heliconius charitoniuslinn. Anim Behav 19:156–164
Tinbergen N (1951) The study of instinct. Clarendon Press, Oxford
Valenta K, Kalbitzer U, Razafimandimby D, Omeja P, Ayasse M, Chapman CA, Nevo O (2018) The evolution of fruit colour: phylogeny, abiotic factors and the role of mutualists. Sci Rep 8:14302. https://doi.org/10.1038/s41598-018-32604-x
Weiss MR (1997) Innate colour preferences and flexible colour learning in the pipevine swallowtail. Anim Behav 53:1043–1052
Weiss MR, Papaj DR (2003) Colour learning in two behavioural contexts: how much can a butterfly keep in mind? Anim Behav 65:425–434
Yoshida M, Itoh Y, Ômura H, Arikawa K, Kinoshita M (2015) Plant scents modify innate colour preference in foraging swallowtail butterflies. Biol Lett 11:1–19
Zaccardi G, Kelber A, Sison-Mangus MP, Briscoe AD (2006) Color discrimination in the red range with only one long-wavelength sensitive opsin. J Exp Biol 209:1944 LP–1941955. https://doi.org/10.1242/jeb.02207
Acknowledgements
BGS was supported by a grant (Project A3: DBT/PR12720/COE/34/21/2015) from the Department of Biotechnology. We also acknowledge Harshad Vijay Mayekar for his advice and help provided in rearing and maintaining the butterflies.
Funding
The work was funded by intra-mural grants from IISER Thiruvananthapuram and the INSPIRE Faculty Award to UK (DST/INSPIRE/04/2013/000476) from the Department of Science and Technology.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Giurfa
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 391 kb)
Rights and permissions
About this article
Cite this article
Balamurali, G.S., Edison, A., Somanathan, H. et al. Spontaneous colour preferences and colour learning in the fruit-feeding butterfly, Mycalesis mineus. Behav Ecol Sociobiol 73, 39 (2019). https://doi.org/10.1007/s00265-019-2648-1
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-019-2648-1