Sending private messages: Floral ultraviolet signals are correlated with pollination syndromes in Erica

Sam McCarren; Jeremy Midgley; Anina Coetzee

doi:10.26786/1920-7603(2021)648

Authors

Sam McCarren University of Cape Town
Jeremy Midgley University of Cape Town, Department of Biological Sciences
Anina Coetzee Fitzpatrick Institute of African Ornithology, University of Cape Town Nelson Mandela University, Department of Conservation Management

DOI:

https://doi.org/10.26786/1920-7603(2021)648

Keywords:

Flower colour, Fynbos, Long-proboscid fly, Nectariniidae, UV, Vision ecology

Abstract

The presence of ultraviolet (UV, wavelengths between 300-400 nm) reflectance in insect-pollinated flowers has been linked to pollination efficiency and pollination shifts, but little is known about its prevalence and function in other pollination systems and African species. We chose the genus Erica for studying the prevalence of UV because of its extreme radiation (c. 680 species) in the Cape, South Africa, with a diversity of pollination syndromes. This study quantified the prevalence and brightness of UV reflectance for five Erica pollination syndromes and tested pollinator preferences for UV reflectance in the two groups with the highest prevalence: sunbirds and long-proboscid flies. Our results show that UV colouration is absent or rare in Erica species pollinated by unclassified insects, rodents or wind. About 17 % of bird-pollinated species reflected UV but choice experiments revealed that free-ranging sunbirds showed no preference for UV signals. All sampled long-proboscid fly-pollinated species reflected UV and its experimental removal decreased seed set drastically, suggesting that long-proboscid flies in the Cape strongly prefer or depend on UV and thereby contributed to selecting for the evolution of this signal.

Author Biographies

Sam McCarren, University of Cape Town

PhD candidate

Jeremy Midgley, University of Cape Town, Department of Biological Sciences

Anina Coetzee, Fitzpatrick Institute of African Ornithology, University of Cape Town Nelson Mandela University, Department of Conservation Management

References

Bouman RW, Steenhuisen SL, van der Niet T (2017) The role of the pollination niche in community assembly of Erica species in a biodiversity hotspot. Journal of Plant Ecology. DOI: https://doi.org/10.1093/jpe/rtw068

Chen Z, Liu C-Q, Sun H, Niu Y (2020) The ultraviolet colour component enhances the attractiveness of red flowers of a bee-pollinated plant. Journal of Plant Ecology 13:354–360. DOI: https://doi.org/10.1093/jpe/rtaa023

Coetzee A, Seymore C, Spottiswoode C (2021) Facilitation and competition shape a geographical mosaic of flower colour polymorphisms. Functional Ecology 35:1914-1924. DOI: https://doi.org/10.1111/1365-2435.13851

de Camargo MGG, Lunau K, Batalha MA, Brings S, de Brito VLG, Morellato LPC (2019) How flower colour signals allure bees and hummingbirds: a community-level test of the bee avoidance hypothesis. New Phytologist 222:1112–1122. DOI: https://doi.org/10.1111/nph.15594

Geerts S, Pauw A (2011) Easy technique for assessing pollination rates in the genus Erica reveals road impact on bird pollination in the Cape fynbos, South Africa. Austral Ecology 36:656–662. DOI: https://doi.org/10.1111/j.1442-9993.2010.02201.x

Goldblatt P, Manning JC (2000) The Long-Proboscid Fly Pollination System in Southern Africa. Annals of the Missouri Botanical Garden 87:146. DOI: https://doi.org/10.2307/2666158

Hansen DM, van der Niet T, Johnson SD (2012) Floral signposts: testing the significance of visual ‘nectar guides’ for pollinator behaviour and plant fitness. Proceedings of the Royal Society B: Biological Sciences 279:634–639. DOI: https://doi.org/10.1098/rspb.2011.1349

Heystek A, Geerts S, Barnard P, Pauw A (2014) Pink flower preference in sunbirds does not translate into plant fitness differences in a polymorphic Erica species. Evolutionary Ecology 28:457–470. DOI: https://doi.org/10.1007/s10682-014-9693-z

Hirota SK, Miki N, Yasumoto AA, Yahara T (2019) UV bullseye contrast of Hemerocallis flowers attracts hawkmoths but not swallowtail butterflies. Ecology and Evolution 9:52–64. DOI: https://doi.org/10.1002/ece3.4604

Jackson S, Nicolson SW (1998) Sugar Preferences and “Side Bias” in Cape Sugarbirds and Lesser Double-Collared Sunbirds. The Auk 115:156–165. DOI: https://doi.org/10.2307/4089120

Jacobs G, Neitz J, Deegan JF (1991) Retinal receptors in rodents maximally sensitive to ultraviolet light. Nature 354: 56-58. DOI: https://doi.org/10.1038/353655a0

Johnson SD, Andersson S (2003) A simple field method for manipulating ultraviolet reflectance of flowers. Canadian Journal of Botany 80:1325–1328. DOI: https://doi.org/10.1139/b02-116

Junker RR, Blüthgen N, Brehm T, Binkenstein J, Paulus J, Schaefer HM, Stang M (2013) Specialization on traits as basis for the niche-breadth of flower visitors and as structuring mechanism of ecological networks. Functional Ecology 27:329–341. DOI: https://doi.org/10.1111/1365-2435.12005

Kaczorowski RL, Blumenfeld G, Koplovich A, Markman S (2014) Color and side preferences in Palestine sunbirds (Nectarinia osea). Israel Journal of Ecology & Evolution 60:35–40. DOI: https://doi.org/10.1080/15659801.2014.941237

Karalius V, Būda V (2007) Colour vision in currant clearwing moth (Synanthedon tipuliformis) (Lepidoptera: Sesiidae). Acta Zoologica Lituanica 17:198–202. DOI: https://doi.org/10.1080/13921657.2007.10512832

Kevan PG, Chittka L, Dyer AG (2001) Limits to the salience of ultraviolet: lessons from colour vision in bees and birds. The Journal of experimental biology 204:2571–2580. DOI: https://doi.org/10.1242/jeb.204.14.2571

Klomberg Y, Dywou Kouede R, Bartoš M, Mertens JEJ, Tropek R, Fokam EB, Janeček S (2019) The role of ultraviolet reflectance and pattern in the pollination system of Hypoxis camerooniana (Hypoxidaceae). AoB PLANTS 11:1-10. DOI: https://doi.org/10.1093/aobpla/plz057

Koski MH, Ashman TL (2014) Dissecting pollinator responses to a ubiquitous ultraviolet floral pattern in the wild. Functional Ecology 28:868–877. DOI: https://doi.org/10.1111/1365-2435.12242

Koski MH, Ashman TL (2016) Macroevolutionary patterns of ultraviolet floral pigmentation explained by geography and associated bioclimatic factors. New Phytologist 211: 708–718. DOI: https://doi.org/10.1111/nph.13921

Llorens L, Badenes-Pérez FR, Julkunen-Tiitto R, Zidorn C, Fereres A, Jansen MAK (2015) The role of UV-B radiation in plant sexual reproduction. Perspectives in Plant Ecology, Evolution and Systematics 17:243–254. DOI: https://doi.org/10.1016/j.ppees.2015.03.001

Lombardi GC, Midgley JJ, Turner RC, Peter CI (2021) Pollination biology of Erica aristata: First confirmation of long-proboscid fly-pollination in the Ericaceae. South African Journal of Botany 142: 403-408. DOI: https://doi.org/10.1016/j.sajb.2021.07.007

Lombardi GC, Peter CI, Turner RC, Midgley JJ (2017) The unusual, closed flowers of Erica lanuginosa (Ericaceae) are adapted for rodent-pollination and not cleistogamy. South African Journal of Botany 111:189–193. DOI: https://doi.org/10.1016/j.sajb.2017.03.020

Lunau K (2014) Visual ecology of flies with particular reference to colour vision and colour preferences. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 200:497–512. DOI: https://doi.org/10.1007/s00359-014-0895-1

Lunau K, Papiorek S, Eltz T, Sazima M (2011) Avoidance of achromatic colours by bees provides a private niche for hummingbirds. Journal of Experimental Biology 214:1607–1612. DOI: https://doi.org/10.1242/jeb.052688

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 in Ecology and Evolution 4: 906-913. DOI: https://doi.org/10.1111/2041-210X.12069

Manning JC, Goldblatt P (1997) The Moegistorhynchus longirostris (Diptera: Nemestrinidae) pollination guild: Long-tubed flowers and a specialized long-proboscid fly pollination system in southern Africa. Plant Systematics and Evolution 206:51–69. DOI: https://doi.org/10.1007/BF00987941

Martínez-Harms J, Hadar R, Márquez N, Menzel R, Shmida A, Stavenga DG, Vorobyev M (2020) Enhanced UV-Reflection Facilitated a Shift in the Pollination System of the Red Poppy, Papaver rhoeas (Papaveraceae). Plants 9:1–12. DOI: https://doi.org/10.3390/plants9080927

Moyers BT, Owens GL, Baute GJ, Rieseberg LH (2017) The genetic architecture of UV floral patterning in sunflower. Annals of Botany 120:39–50. DOI: https://doi.org/10.1093/aob/mcx038

Newman E, Johnson SD (2021) A shift in long-proboscid fly pollinators and floral tube length among populations of Erica junonia (Ericaceae). South African Journal of Botany 142:451–458. DOI: https://doi.org/10.1016/j.sajb.2021.07.014

Ödeen A, Håstad O (2010) Pollinating birds differ in spectral sensitivity. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 196:91–96. DOI: https://doi.org/10.1007/s00359-009-0474-z

Papiorek S, Junker RR, Alves-dos-Santos I, Melo GAR, Amaral-Neto LP, Sazima M, Wolowski M, Freitas L, Lunau K (2016) Bees, birds and yellow flowers: Pollinator-dependent convergent evolution of UV patterns. Plant Biology 16:46-55. DOI: https://doi.org/10.1111/plb.12322

Peitsch D, Fietz A, Hertel H, de Souza J, Ventura DF, Menzel R (1992) The spectral input systems of hymenopteran insects and their receptor-based colour vision. Journal of Comparative Physiology A 170:23–40. DOI: https://doi.org/10.1007/BF00190398

Peter CI, Dold AP, Barker NP, Ripley BS (2004) Pollination biology of Bergeranthus multiceps (Aizoaceae) with preliminary observations of repeated flower opening and closure. South African Journal of Science 100:624–629.

Peter CI, Johnson SD (2008) Mimics and magnets: The importance of color and ecological facilitation in floral deception. Ecology 89:1583–1595. DOI: https://doi.org/10.1890/07-1098.1

Pirie MD, Oliver EGH, Mugrabi de Kuppler A, Gehrke B, Le Maitre NC, Kandziora M, Bellstedt DU (2016) The biodiversity hotspot as evolutionary hot-bed: spectacular radiation of Erica in the Cape Floristic Region. BMC Evolutionary Biology 16:190. DOI: https://doi.org/10.1186/s12862-016-0764-3

Rebelo AG, Siegfried WR (1985) Colour and size of flowers in relation to pollination of Erica species. Oecologia 65:584–590. DOI: https://doi.org/10.1007/BF00379677

Rebelo AGG, Siegfried WRR, Oliver EGH (1985) Pollination syndromes of Erica species in the south-western Cape. South African Journal of Botany 51:270–280. DOI: https://doi.org/10.1016/S0254-6299(16)31657-X

Rodríguez-Gironés MA, Santamaría L (2004) Why are so many bird flowers red? PLoS Biology 2:e350. DOI: https://doi.org/10.1371/journal.pbio.0020350

Shawkey MD, Igic B, Rogalla S, Goldenberg J, Clusella-Trullas S, D’Alba L (2017) Beyond colour: consistent variation in near infrared and solar reflectivity in sunbirds (Nectariniidae). The Science of Nature 104:78. DOI: https://doi.org/10.1007/s00114-017-1499-8

Shrestha M, Burd M, Garcia JE, Dorin A, Dyer AG (2019) Colour evolution within orchids depends on whether the pollinator is a bee or a fly. Plant Biology 21:745–752. DOI: https://doi.org/10.1111/plb.12968

Shrestha M, Dyer AG, Boyd-Gerny S, Wong BBM, Burd M (2013) Shades of red: Bird-pollinated flowers target the specific colour discrimination abilities of avian vision. New Phytologist 198:301–310. DOI: https://doi.org/10.1111/nph.12135

Shrestha M, Dyer AG, Burd M (2016) Evaluating the spectral discrimination capabilities of different pollinators and their effect on the evolution of flower colors. Communicative & Integrative Biology 6:e24000. DOI: https://doi.org/10.4161/cib.24000

Streisfeld MA, Young WN, Sobel JM (2013) Divergent selection drives genetic differentiation in an R2R3-MYB transcription factor that contributes to incipient speciation in Mimulus aurantiacus. PLoS genetics 9:e1003385. DOI: https://doi.org/10.1371/journal.pgen.1003385

Troje N (1993) Spectral categories in the learning behaviour of blowflies. Zeitschrift fur Naturforschung - Section C Journal of Biosciences 48:96–104. DOI: https://doi.org/10.1515/znc-1993-1-218

Turner RC, Midgley JJ, Johnson SD (2011) Evidence for rodent pollination in Erica hanekomii (Ericaceae). Botanical Journal of the Linnean Society 166:163–170. DOI: https://doi.org/10.1111/j.1095-8339.2011.01139.x

Valentin S, Lunau K, Johnson S (2006) Choice Experiments Using Artificial Flowers Reveal Colour Preferences of Long-proboscid Flies (Diptera, Nemestrinidae) Under Field Conditions. Entomologie heute 18:113–122

van der Niet T (2021) Paucity of natural history data impedes phylogenetic analyses of pollinator-driven evolution. New Phytologist 229:1201–1205. DOI: https://doi.org/10.1111/nph.16813

van der Niet T, Pirie MD, Shuttleworth A, Johnson SD, Midgey JJ (2014) Do pollinator distributions underlie the evolution of pollination ecotypes in the Cape shrub Erica plukenetii? Annals of Botany 113:301–315. DOI: https://doi.org/10.1093/aob/mct193

Welsford MR, Johnson SD (2012) Solitary and social bees as pollinators of Wahlenbergia (Campanulaceae): Single-visit effectiveness, overnight sheltering and responses to flower colour. Arthropod-Plant Interactions 6:1–14. DOI: https://doi.org/10.1007/s11829-011-9149-0

Whitehead MR, Gaskett AC, Johnson SD (2019) Floral community predicts pollinators’ color preference: Implications for Batesian floral mimicry. Behavioral Ecology 30:213–222. DOI: https://doi.org/10.1093/beheco/ary138

Whitfield M, Köhler A, Nicolson SW (2014) Sunbirds increase foraging success by using color as a cue for nectar quality. Behavioral Ecology 25:328–334. DOI: https://doi.org/10.1093/beheco/art115