Abstract
Experimental studies of the use of visual and olfactory cues by flower-visiting animals can shed light on the evolution of floral signalling traits. We examined the functional significance of floral traits in Clivia miniata (Amaryllidaceae). This forest lily with large orange trumpet-shaped flowers is pollinated mainly by swallowtail butterflies and belongs to a lineage with ancestral bird pollination. We used C. miniata flowers varying in colour, orientation and scent, and arrays of artificial flowers varying in colour, pattern, orientation, size, shape, and scent to assess foraging preferences of the butterflies that pollinate C. miniata. Butterflies preferred orange over yellow colour morphs of C. miniata and preferred red and orange model flowers over yellow ones. Orange models with a central yellow target ‘nectar guide’ were favoured over plain orange models. Butterflies also favoured large over small model flowers and preferred to alight on upward-facing flowers. Addition of scent compounds emitted by C. miniata flowers increased butterfly visitation to model and natural flowers. These results identify the importance of particular combinations of visual and olfactory signals for attraction of swallowtail butterflies and shed light on the floral modifications associated with a shift from bird to butterfly pollination.
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References
Andersson S, Dobson HEM (2003) Behavioral foraging responses by the butterfly Heliconius melpomene to Lantana camara floral scent. J Chem Ecol 29:2303–2318
Andersson S, Nilsson LA, Groth I, Bergstrom G (2002) Floral scents in butterfly-pollinated plants: possible convergence in chemical composition. Bot J Linn Soc 140:129–153
Armbruster WS (1996) Evolution of floral morphology and function: an integrative approach to adaptation, constraint, and compromise in Dalechampia (Euphorbiaceae). In: Lloyd DG, Barrett SCH (eds) Floral biology: studies on floral evolution in animal-pollinated plants. Chapman and Hall, New York, pp 241–272
Arroyo MK, Till-Bottraud I, Torres C, Henriquez CA, Martinez J (2007) Display size preferences and foraging habits of high Andean butterflies pollinating Chaetanthera lycopodioides (Asteraceae) in the subnival of the central Chilean Andes. Arct Antarct Alp Res 39:347–352
Balamurali GS, Rose S, Somanathan H, Kodandaramaiah U (2020) Complex multi-modal sensory integration and context specificity in colour preferences of a pierid butterfly. J Exp Biol 223:jeb223271
Bell G (1985) On the function of flowers. Proc R Soc Lond B 224:223–265
Blackiston DJ, Briscoe AD, Weiss MR (2011) Colour vision and learning in the monarch butterfly, Danaus plexippus (Nymphalidae). J Exp Biol 214:509–520
Borges RM, Gowda V, Zacharias M (2003) Butterfly pollination and high-contrast visual signals in a low-density distylous plant. Oecologia 136:571–573
Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510
Butler HC, Johnson SD (2020) Butterfly-wing pollination in Scadoxus and other South African Amaryllidaceae. Bot J Linn Soc 193:363–374
Campbell DR (2009) Using phenotypic manipulations to study multivariate selection of floral trait associations. Ann Bot 103:1557–1566
Campbell DR, Jürgens A, Johnson SD (2016) Reproductive isolation between Zaluzianskya species: the influence of volatiles and flower orientation on hawkmoth foraging choices. New Phytol 210:333–342
Caruso CM, Eisen KE, Martin RA, Sletvold N (2019) A meta-analysis of the agents of selection on floral traits. Evolution 73:4–14
Chittka L, Shmida A, Troje N, Menzel R (1994) Ultraviolet as a component of flower reflections, and the colour perception of Hymenoptera. Vision Res 34:1489–1508
Chittka L, Spaethe J, Schmidt A, Hickelsberger A (2001) Adaptation, constraint, and chance in the evolution of flower color and pollinator color vision. In: Chittka L, Thomson JD (eds) Cognitive ecology of pollination. Cambridge University Press, Cambridge, pp 106–126
Crane J (1955) Imaginal behavior of a Trinidad butterfly, Heliconius erato hydara Hewitson, with special reference to the social use of color. Zoologica 40:167–196
Dafni A, Giurfa M (1999) The functional ecology of floral guides in relation to insects behaviour and vision. In: Wasser SP (ed) Evolutionary theory and processes: modern perspectives. Springer, Dordrecht, pp 363–383
Daniels RJ, Johnson SD, Peter CI (2020) Flower orientation in Gloriosa superba (Colchicaceae) promotes cross-pollination via butterfly wings. Ann Bot 125:1137–1149
Dornhaus A, Chittka L (1999) Insect behaviour: evolutionary origins of bee dances. Nature 401:38–38
Drewniak ME, Briscoe AD, Cocucci AA, Beccacece HM, Zapata AI, Moré M (2020) From the butterfly’s point of view: learned colour association determines differential pollination of two co-occurring mock verbains by Agraulis vanillae (Nymphalidae). Biol J Linn Soc 130:715–725
Faegri K, van der Pijl L (1979) The principles of pollination ecology. Pergamon, Oxford
Franzke M et al (2020) Spatial orientation based on multiple visual cues in non-migratory monarch butterflies. J Exp Biol 223:jeb223800
Fulton M, Hodges SA (1999) Floral isolation between Aquilegia formosa and Aquilegia pubescens. Proc R Soc Lond Ser B 266:2247–2252
Gervasi DDL, Schiestl FP (2017) Real-time divergent evolution in plants driven by pollinators. Nat Commun 8:14691
Goulson D, Cory JS (1993) Flower constancy and learning in foraging preferences of the green-veined white butterfly Pieris napi. Ecol Entomol 18:315–320
Goyret J, Markwell PM, Raguso RA (2007) The effect of decoupling olfactory and visual stimuli on the foraging behavior of Manduca sexta. J Exp Biol 210:1398–1405
Hansen DM, Van der Niet T, Johnson SD (2012) Floral signposts: testing the significance of visual ‘nectar guides’ for pollinator behaviour and plant fitness. Proc R Soc B 279:634–639
Haverkamp A, Li X, Hansson BS, Baldwin IT, Knaden M, Yon F (2019) Flower movement balances pollinator needs and pollen protection. Ecology 100:e02553
Hirota SK, Miki N, Yasumoto AA, Yahara T (2019) UV bullseye contrast of Hemerocallis flowers attracts hawkmoths but not swallowtail butterflies. Ecol Evol 9:52–64
Ilse D, Vaidya VG (1956) Spontaneous feeding response to colours in Papilio demoleus L. Proc Indian Acad Sci Sect B 43:23–31
Johnson SD (1994) Evidence for Batesian mimicry in a butterfly-pollinated orchid. Biol J Lin Soc 53:91–104
Johnson SD, Bond WJ (1994) Red flowers and butterfly pollination in the fynbos of South Africa. In: Arianoutsou M, Groves RH (eds) Plant-animal interactions in Mediterranean-type ecosystems. Springer, Dordrecht, pp 137–148
Johnson SD, Dafni A (1998) Response of bee-flies to the shape and pattern of model flowers: implications for floral evolution in a Mediterranean herb. Funct Ecol 12:289–297
Johnson SD, Andersson S (2002) A simple field method for manipulating ultraviolet reflectance of flowers. Can J Bot 80:1325–1328
Johnson SD, Wester P (2017) Stefan Vogel’s analysis of floral syndromes in the South African flora: an appraisal based on 60 years of pollination studies. Flora 232:200–206
Kandori I, Ohsaki N (1998) Effect of experience on foraging behavior towards artificial nectar guide in the cabbage butterfly, Pieris rapae crucivora (Lepidoptera: Pieridae). Appl Entomol Zool 33:35–42
Kelber A (1997) Innate preferences for flower features in the hawkmoth Macroglossum stellatarum. J Exp Biol 200:827–836
Kelber A, Vorobyev M, Osorio D (2003) Animal colour vision—behavioral tests and physiological consepts. Biol Rev 78:81–118
Kiepiel I, Johnson SD (2014) Shift from bird to butterfly pollination in Clivia (Amaryllidaceae). Am J Bot 101:190–200
Kinoshita M, Shimada N, Arikawa K (1999) Colour vision of the foraging swallotail butterfly Papilio xunthus. J Exp Biol 202:95–102
Kinoshita M, Stewart FJ, Ômura H (2017) Multisensory integration in Lepidoptera: insights into flower-visitor interactions. BioEssays 39:1600086
Koshitaka H, Arikawa K, Kinoshita M (2011) Intensity contrast as a crucial cue for butterfly landing. J Comp Physiol A 197:1105
Koshitaka H, Kinoshita M, Vorobyev M, Arikawa K (2008) Tetrachromacy in a butterfly that has eight varieties of spectral receptors. Proc R Soc B 275:947–954
Lunau K, Maier EJ (1995) Innate colour preferences of flower visitors. J Comp Physiol A 177:1–19
Lunau K, Fieselmann G, Heuschen B, van de Loo A (2006) Visual targeting of components of floral colour patterns in flower-naive bumblebees (Bombus terrestris; Apidae). Naturewissenschaften 93:325–328
Metcalf RL, Metcalf ER (1992) Plant kairomones in insect ecology and control. Chapman & Hall, New York
Mitchell-Olds T, Shaw RG (1987) Regression analysis of natural selection: statistical inference and biological interpretation. Evolution 41:1149–1161
Newman E, Anderson B, Johnson SD (2012) Flower colour adaptation in a mimetic orchid. Proc R Soc B 279:2309–2313
Ômura H, Honda K (2005) Priority of color over scent during flower visitation by adult Vanessa indica butterflies. Oecologia 142:588–596
Pohl NB, Van Wyk J, Campbell DR (2011) Butterflies show flower colour preferences but not constancy in foraging at four plant species. Ecol Entomol 36:290–300
Policha T, Davis A, Barnadas M, Dentinger BT, Raguso RA, Roy BA (2016) Disentangling visual and olfactory signals in mushroom-mimicking Dracula orchids using realistic three-dimensional printed flowers. New Phytol 2100:1058–1071
Rader R et al (2016) Non-bee insects are important contributors to global crop pollination. Proc Natl Acad Sci USA 113:146–151
Raguso R (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Annu Rev Ecol Syst 39:549–569
Schemske DW, Bradshaw HD Jr (1999) Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proc Natl Acad Sci USA 96:11910–11915
Scherer C, Kolb G (1987) Behavioral experiments on the visual processing of color stimuli in Pieris brassicae L. (Lepidoptera). J Comp Physiol A 160:645–656
Schiestl FP, Johnson SD (2013) Pollinator-mediated evolution of floral signals. Trends Ecol Evol 28:307–315
Silberglied RE (1984) Visual communication and sexual selection amoung butterflies. In: Vane-Wright RI, Ackery PR (eds) The biology of butterflies. Academic Press, London, pp 207–223
Sletvold N, Ågren J (2010) Pollinator-mediated selection on floral display and spur length in the orchid Gymnadenia conopsea. Int J Plant Sci 171:999–1009
Sletvold N, Trunschke J, Smit M, Verbeek J, Ågren J (2016) Strong pollinator-mediated selection for increased flower brightness and contrast in a deceptive orchid. Evolution 70:716–724
Sprengel CK (1793) Das entdeckte Geheimnifs der Natur in Bau un in der Befruchtung der Blumen. Friedrich Vieweg dem aeltern, Berlin
Swihart SL (1970) The neural basis of colour vision in the butterfly, Papilio troilus. J Insect Physiol 16:1623–1636
Swihart CA, Swihart SL (1970) Colour selection and learned feeding preferences in the butterfly, Heliconius charitonius Linn. Anim Behav 18:60–64
Vaidya VG (1969) Form perception in Papilio demoleus L. (Papilionidae, Lepidoptera). Behaviour 33:212–221
Van der Niet T, Johnson SD (2012) Phylogenetic evidence for pollinator-driven diversification of angiosperms. Trends Ecol Evol 27:353–361
Vaughton G, Ramsey M (1998) Floral display, pollinator visitation and reproductive success in the dioecious perennial herb Wurmbea dioica (Liliaceae). Oecologia 115:93–101
Wang H, Xiao C-L, Gituru RW, Xiong Z, Yu D, Guo Y-H, Yang C-H (2014) Change of floral orientation affects pollinator diversity and their relative importance in an alpine plant with generalized pollination system, Geranium refractim (Geraniaceae). Plant Ecol 215:1211–1219
Waser NM, Price MV (1985) The effect of nectar guides on pollinator preference: experimental studies with a montane herb. Oecologia 67:121–126
Weiss MR (1995) Floral color change: a widespread functional convergence. Am J Bot 82:167–185
Weiss MR (1997) Innate colour preferences and flexible colour learning in the pipevine swallowtail. Anim Behav 53:1043–1052
Yoshida M, Itoh Y, Ômura H, Arikawa K, Kinoshita M (2015) Plant scents modify innate colour preference in foraging swllowtail butterflies. Biol Lett 11:20150390
Acknowledgements
We thank KZN Wildlife and Mbona Private Nature Reserve for permission to work in their Reserves. This study was funded by the National Research Foundation (Grant 46372 to SDJ) and the Gay Langmuir Bursary for Wildlife research (IK).
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This study was funded by the South African National Research Foundation (Grant 46372 to SDJ) and the Gay Langmuir Bursary for Wildlife research (IK).
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Supplementary file1 (EPS 4170 KB)
Fig. S1. Behavioural responses of Papilio ophidicephalus to two C. miniata-shaped model choices, differing only in size; plain orange versus plain orange reduced size (one-third scale) models. Bioassays conducted at the MPNR site in October 2010. Observations (n = 23) recorded over 4 full days, and over 10 unique time blocks. Approaches; n = 18 (brushes; n = 2, alights; n = 3).
Supplementary file2 (EPS 87888 KB)
Fig. S2. Behavioural responses of five butterfly species (Nepheronia argia, Papilio echerioides echerioides, P. euphranor, P. nireus lyaeus, and P. ophidicephalus) to two model flower arrays consisting of two distinct floral forms, representing two Clivia species; plain orange C. gardenii-shaped models versus plain orange C. miniata-shaped models. Experimental arrays conducted at the MPNR site in October 2010. Observations (n = 25) recorded over five full days, and over 13 unique time blocks. Approaches; n = 20 (brushes; n = 4, alights; n = 1).
Supplementary file3 (EPS 46048 KB)
Fig. S3. Behavioural responses of six butterfly species, across two sites, to model flower arrays consisting of two C. miniata-shaped choices (both orange with yellow target models); unscented (paraffin control) versus scent supplemented. Experimental arrays conducted at the MPNR site in 2010 and the UNR site in 2014. MPNR observations (n = 181) recorded over 6 full days, and over 18 unique time blocks. Approaches; n = 138, brushes; n = 29, alights; n = 14. UNR observations (n = 272) recorded over 4 full days, over 54 time blocks. Approaches; n = 186; brushes; n = 46, alights; n = 40.
Supplementary file4 (DOCX 245797 KB)
Fig. S4. Behavioural responses of Papilio dardanus cena and P. nireus lyaeus to two real flower arrays consisting of C. miniata flowers in their normal upright orientation versus C. miniata flowers manipulated into a pendulous orientation. Experimental arrays conducted at the UNR site in the flowering season of 2014. Observations (n = 326) recorded over 5 full days, and over 53 unique time blocks. Approaches; n = 185, brushes; n = 103, alights; n = 38
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Kiepiel, I., Johnson, S.D. Responses of butterflies to visual and olfactory signals of flowers of the bush lily Clivia miniata. Arthropod-Plant Interactions 15, 253–263 (2021). https://doi.org/10.1007/s11829-021-09813-9
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DOI: https://doi.org/10.1007/s11829-021-09813-9