Abstract
Altitudinal gradients are interesting models to test the effect of biotic and abiotic drivers of floral colour diversity, since an increase in UV irradiance, decrease of pollinator availability and shifts from bee- to fly-pollination in high relative to low altitudes are expected. We tested the effect of altitude and phylogeny, using several chromatic and achromatic colour properties, UV reflectance and pollinators’ discrimination capacity (Apis mellifera, Bombus terrestris, Musca domestica and Eristalis tenax), to understand the floral colour diversity in an alpine altitudinal gradient. All colour properties were weakly related to phylogeny. We found a shift from overdispersed floral colours and high chromatic contrast with the background (for bees) in the low altitude, to clustered floral colours (UV and green range for bees and flies) and clustered chromatic and achromatic properties in the high altitude. Different from flies, bees could discriminate floral colours in all altitudinal ranges. Low altitudes are likely to exhibit suitable conditions for more plant species, increasing competition for pollinators and floral colour divergence. Conversely, the increase in UV irradiance in high altitudes may filter plants with specific floral UV-reflectance patterns. Overall, floral colour diversity suggests that both biotic (pollinator fauna) and abiotic (UV irradiance) drivers shape floral communities, but their importance changes with altitude.
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References
Arnold SEJ, Savolainen V, Chittka L (2009) Flower colours along an alpine altitude gradient, seen through the eyes of fly and bee pollinators. Arthropod Plant Interact 3:27–43. https://doi.org/10.1007/s11829-009-9056-9
Arnold SEJ, Faruq S, Savolainen V, McOwan PW, Chittka L (2010) FReD: the floral reflectance database-a web portal for analysis of flower colour. PLoS One 5:e14287. https://doi.org/10.1371/journal.pone.0014287
Arroyo MTK, Primack R, Armesto J (1982) Community studies in pollination ecology in the high temperate Andes of central Chile I Pollination mechanisms and altitudinal variation. Am J Bot 69:82–97. https://doi.org/10.2307/2442833
Backhaus W (1991) Color opponent coding in the visual system of the honeybee. Vis Res 31:1381–1397. https://doi.org/10.1016/0042-6989(91)90059-E
Bergamo PJ, Rech AR, Brito VLG, Sazima M (2016) Flower colour and visitation rates of Costus arabicus support the “bee avoidance” hypothesis for red-reflecting hummingbird-pollinated flowers. Funct Ecol 30:710–720. https://doi.org/10.1111/1365-2435.12537
Bischoff M, Lord JM, Robertson AW, Dyer AG (2013) Hymenopteran pollinators as agents of selection on flower colour in the New Zealand mountains: salient chromatic signals enhance flower discrimination. NZ J Bot 51:181–193. https://doi.org/10.1080/0028825X.2013.806933
Blomberg SP, Garland Jr T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745. https://doi.org/10.1554/0014-3820(2003)057[0717:TFPSIC]2.0.CO;2
Briscoe Runquist R, Grossenbacher D, Porter S, Kay K, Smith J (2016) Pollinator-mediated assemblage processes in California wildflowers. J Evol Biol 29:1045–1058. https://doi.org/10.1111/jeb.12845
Brito VLG, Weynans K, Sazima M, Lunau K (2015) Trees as huge flowers and flowers as oversized floral guides: the role of floral color change and retention of old flowers in Tibouchina pulchra. Front Plant Sci 6:362. https://doi.org/10.3389/fpls.2015.00362
Bukovac Z, Shrestha M, Garcia JE, Burd M, Dorin A, Dyer AG (2017) Why background colour matters to bees and flowers. J Comp Physiol A 203:369–380. https://doi.org/10.1007/s00359-017-1175-7
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. https://doi.org/10.1007/BF00199331
Chittka L (1997) Bee color vision is optimal for coding flower color, but flower colors are not optimal for being coded—why? Isr J Plant Sci 45:115–127. https://doi.org/10.1080/07929978.1997.10676678
Chittka L, Kevan PG (2005) Flower colour as advertisement. In: Dafni A, Kevan PG, Husband BC (eds) Practical pollination biology. Environquest Ltd., Cambridge, pp 157–196
Chittka L, Gumbert A, Kunze J (1997) Foraging dynamics of bumble bees: correlates of movement within and between plant species. Behav Ecol 8:239–249. https://doi.org/10.1093/beheco/8.3.239
Chittka L, Thomson JD, Waser NM (1999) Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86:361–377. https://doi.org/10.1007/s001140050636
de Jager ML, Dreyer LL, Ellis AG (2011) Do pollinators influence the assembly of flower colours within plant communities? Oecologia 166:543–553. https://doi.org/10.1007/s00442-010-1879-7
Dyer AG, Chittka L (2004) Biological significance of distinguishing between similar colours in spectrally variable illumination: bumblebees (Bombus terrestris) as a case study. J Comp Physiol A 190:105–114. https://doi.org/10.1007/s00359-003-0475-2
Dyer AG, Spaethe J, Prack S (2008) Comparative psychophysics of bumblebee and honeybee colour discrimination and object detection. J Comp Physiol A 194:617–627. https://doi.org/10.1007/s00359-008-0335-1
Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15. https://doi.org/10.1086/284325
Garcia JE, Spaethe J, Dyer AG (2017) The path to colour discrimination is S-shaped: behavior determines the interpretation of colour models. J Comp Physiol A 203:983–997. https://doi.org/10.1007/s00359-017-1208-2
Garland T Jr, Dickerman AW, Janis CM, Jones JA (1993) Phylogenetic analysis of covariance by computer simulation. Syst Biol 42:265–292. https://doi.org/10.1093/sysbio/42.3.265
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. https://doi.org/10.1007/BF00227381
Gotelli NJ (2000) Null model analysis of species co-occurrence patterns. Ecology 81:2606–2621. https://doi.org/10.1890/0012-9658(2000)081[2606:NMAOSC]2.0.CO;2
Gray M, Stansberry MJ, Lynn JS, Williams CF, White TF, Whitney KD (2018) Consistent shifts in pollinator-relevant floral coloration along Rocky Mountain elevation gradients. J Ecol 00:1–15. https://doi.org/10.1111/1365-2745.12948
Gumbert A, Kunze J, Chittka L (1999) Floral colour diversity in plant communities, bee colour space and a null model. Proc R Soc B 266:1711–1716. https://doi.org/10.1098/rspb.1999.0836
Hardie RC (1986) The photoreceptor array of the dipteran retina. Trends Neurosci 9:419–423. https://doi.org/10.1016/0166-2236(86)90136-0
Hardie RC, Kirschfeld K (1983) Ultraviolet sensitivity of fly photoreceptors R7 and R8: evidence for a sensitising function. Biophys Struct Mech 9:171–180. https://doi.org/10.1007/BF00537814
Hegland SJ, Nielsen A, Lázaro A, Bjerknes AL, Totland Ø (2009) How does climate warming affect plant–pollinator interactions? Ecol Lett 12:184–195. https://doi.org/10.1111/j.1461-0248.2008.01269.x
Hempel de Ibarra N, Giurfa M, Vorobyev M (2002) Discrimination of coloured patterns by honeybees through chromatic and achromatic cues. J Comp Physiol A 188:503–512. https://doi.org/10.1007/s00359-002-0322-x
Hoiss B, Krauss J, Potts SG, Roberts S, Steffan-Dewenter I (2012) Altitude acts as an environmental filter on phylogenetic composition, traits and diversity in bee communities. Proc R Soc B. https://doi.org/10.1098/rspb.2012.1581
Jersáková J, Jürgens A, Šmilauer P, Johnson SD (2012) The evolution of floral mimicry: identifying traits that visually attract pollinators. Funct Ecol 26:1381–1389. https://doi.org/10.1111/j.1365-2435.2012.02059.x
Kantsa A, Raguso RA, Dyer AG, Sgardelis SP, Olesen JM, Petanidou T (2017) Community-wide integration of floral colour and scent in a Mediterranean scrubland. Nat Ecol Evol 1:1502–1510. https://doi.org/10.1038/s41559-017-0298-0
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: r tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. https://doi.org/10.1093/bioinformatics/btq166
Kevan PG (1972) Floral colors in the high arctic with reference to insect–flower relations and pollination. Can J Bot 50:2289–2316. https://doi.org/10.1139/b72-298
Koethe S, Bossems J, Dyer AG, Lunau K (2016) Colour is more than hue: preferences for compiled colour traits in the stingless bees Melipona mondury and M. quadrifasciata. J Comp Physiol A 202:615–627. https://doi.org/10.1007/s00359-016-1115-y
Kooi CJ, Pen I, Staal M, Stavenga DG, Elzenga JT (2016) Competition for pollinators and intra-communal spectral dissimilarity of flowers. Plant Biol 18:56–62. https://doi.org/10.1111/plb.12328
Körner C (2007) The use of ‘altitude’ in ecological research. Trends Ecol Evol 22:569–574. https://doi.org/10.1016/j.tree.2007.09.006
Koski MH, Ashman TL (2015) An altitudinal cline in UV floral pattern corresponds with a behavioral change of a generalist pollinator assemblage. Ecology 96:3343–3353. https://doi.org/10.1890/15-0242.1
Koski MH, Ashman TL (2016) Reproductive character displacement and environmental filtering shape floral variation between sympatric sister taxa. Evolution 70:2616–2622. https://doi.org/10.1111/evo.13042
Kraft NJB, Adler PB, Godoy O, James EC, Fuller S, Levine JM (2015) Community assembly, coexistence and the environmental filtering metaphor. Funct Ecol 29:592–599. https://doi.org/10.1111/1365-2435.12345
Lázaro A, Hegland SJ, Totland Ø (2008) The relationships between floral traits and specificity of pollination systems in three Scandinavian plant communities. Oecologia 157:249–257. https://doi.org/10.1007/s00442-008-1066-2
Lázaro A, Lundgren R, Totland Ø (2014) Experimental reduction of pollinator visitation modifies plant–plant interactions for pollination. Oikos 123:1037–1048. https://doi.org/10.1111/oik.01268
Lunau K (2014) Visual ecology of flies with particular reference to colour vision and colour preferences. J Comp Physiol 200:497–512. https://doi.org/10.1007/s00359-014-0895-1
Lunau K, Wacht S, Chittka L (1996) Colour choices of naive bumble bees and their implications for colour perception. J Comp Physiol A 178:477–489. https://doi.org/10.1007/BF00190178
Makino TT, Yokoyama J (2015) Nonrandom composition of flower colors in a plant community: mutually different co-flowering natives and disturbance by aliens. PLoS One 10:e0143443. https://doi.org/10.1371/journal.pone.0143443
McEwen JR, Vamosi JC (2010) Floral colour versus phylogeny in structuring subalpine flowering communities. Proc R Soc B. https://doi.org/10.1098/rspb.2010.0501
Moré M, Cocucci AA, Raguso RA (2013) The importance of oligosulfides in the attraction of fly pollinators to the brood-site deceptive species Jaborosa rotacea (Solanaceae). Int J Plant Sci 174:1–15. https://doi.org/10.1086/670367
Muchhala N, Brown Z, Armbruster WS, Potts MD (2010) Competition drives specialization in pollination systems through costs to male fitness. Am Nat 176:732–743. https://doi.org/10.1086/657049
Muchhala N, Johnsen S, Smith SD (2014) Competition for hummingbird pollination shapes flower color variation among in Andean Solanaceae. Evolution 68:2275–2286. https://doi.org/10.1111/evo.12441
Peitsch D, Fietz A, Hertel H, Souza J, Ventura DF, Menzel R (1992) The spectral input systems of hymenopteran insects and their receptor-based colour vision. J Comp Physiol A 170:23–40. https://doi.org/10.1007/BF00190398
Ratchke B (1983) Competition and facilitation among plants for pollinators. In: Real L (ed) Pollination biology. Academic Press, New York, pp 309–329
Rausher MD (2008) Evolutionary transitions in floral color. Int J Plant Sci 169:7–21. https://doi.org/10.1086/523358
Renoult JP, Blüthgen N, Binkenstein J, Weiner CN, Werner M, Schaefer HM (2015) The relative importance of color signaling for plant generalization in pollination networks. Oikos 124:347–354. https://doi.org/10.1111/oik.01361
Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
Rohde K, Papiorek S, Lunau K (2013) Bumblebees (Bombus terrestris) and honeybees (Apis mellifera) prefer similar colours of higher spectral purity over trained colours. J Comp Physiol A 199:197–210. https://doi.org/10.1007/s00359-012-0783-5
Schemske DW, Bradshaw HD (1999) Pollinator preference and the evolution of floral traits in monkey flowers (Mimulus). Proc Natl Acad Sci 96:11910–11915. https://doi.org/10.1073/pnas.96.21.11910
Schnaitmann C, Garbers C, Wachtler T, Tanimoto H (2013) Color discrimination with broadband photoreceptors. Curr Biol 23:2375–2383. https://doi.org/10.1016/j.cub.2013.10.037
Seifan M, Hoch EM, Hanoteaux S, Tielbörger K (2014) The outcome of shared pollination services is affected by the density and spatial pattern of an attractive neighbor. J Ecol 102:953–962. https://doi.org/10.1111/1365-2745.122256
Shrestha M, Dyer AG, Bhattarai P, Burd M (2014) Flower colour and phylogeny along an altitudinal gradient in the Himalayas of Nepal. J Ecol 102:126–135. https://doi.org/10.1111/1365-2645.12185
Shrestha M, Lunau K, Dorin A, Schulze B, Bischoff M, Burd M, Dyer AG (2016) Floral colours in a world without birds and bees: the plants of Macquarie Island. Plant Biol 18:842–850. https://doi.org/10.1111/plb/12456
Skorupski P, Döring TF, Chittka L (2007) Photoreceptor spectral sensitivity in island and mainland populations of the bumblebee, Bombus terrestris. J Comp Physiol A 193:485–494. https://doi.org/10.1007/s00359-006-0206-6
Telles FJ, Rodríguez-Gironés MA (2015) Insect vision models under scrutiny: what bumblebees (Bombus terrestris L.) can still tell us. Sci Nat 102:1–13. https://doi.org/10.1007/s00114-014-1256-1
Totland Ø (1993) Pollination in alpine Norway: flowering phenology, insect visitors, and visitation rates in two plant communities. Can J Bot 71:1072–1079. https://doi.org/10.1139/b93-124
Troje N (1993) Spectral categories in the learning behaviour of blowflies. Zeitschrift für Naturforschung C 48:96–104. https://doi.org/10.1515/znc-1993-1-218
Tur C, Sáez A, Traveset A, Aizen MA (2016) Evaluating the effects of pollinator-mediated interactions using pollen transfer networks: evidence of widespread facilitation in south Andean plant communities. Ecol Lett 19:576–586. https://doi.org/10.1111/ele.12594
Valiente-Banuet A, Aizen MA, Alcántara JM, Arroyo J, Cocucci A, Galetti M, García MB, García D, Gómez JM, Jordano P, Medel R, Navarro L, Obeso JR, Oviedo R, Ramírez N, Rey PJ, Traveset A, Verdú M, Zamora R (2015) Beyond species loss: the extinction of ecological interactions in a changing world. Funct Ecol 29:299–307. https://doi.org/10.1111/1365-2435.12356
Vasas V, Hanley D, Kevan PG, Chittka L (2017) Multispectral images of flowers reveal the adaptive significance of using long-wavelength-sensitive receptors for edge detection in bees. J Comp Physiol A 203:301–311. https://doi.org/10.1007/s00359-017-1156-x
Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc B 265:351–358. https://doi.org/10.1098/rspb.1998.0302
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505. https://doi.org/10.1146/annurev.ecolsys.33.010802.150448
Wolowski M, Carvalheiro LG, Freitas L (2017) Influence of plant–pollinator interactions on the assembly of plant and hummingbird communities. J Ecol 105:332–344. https://doi.org/10.1111/1365.2745.12684
Wyszecki G, Stiles WS (1982) Color science. Wiley, New York
Acknowledgements
PJB thanks the National Council for Scientific and Technological Development (CNPq, Grant 140254/2016-1) and São Paulo Research Foundation (FAPESP, Grant 2016/06434-0), FJT thanks the Coordination for the Improvement of Higher Education Personnel (CAPES-1659767) for the Postdoctoral grant (PNPD), VLGB thanks Minas Gerais State Agency for Research and Development (FAPEMIG, grant APQ-02497-16). The raw data collection for this manuscript was supported by a Leibniz Award from the DFG. SEJA’s previous analysis was carried out supported by the Biotechnology and Biological Sciences Research Council (BBSRC) CASE studentship in association with the Royal Botanic Gardens, Kew, BS/S/L/2005/12155A. We thank Prof. Dr. Klaus Lunau for providing spectral sensitivity of Eristalis tenax and helping with fly model calculations.
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PJB, FJT and VLGB performed analyses. SEJA performed original analysis and processing of reflectance data. All authors conceived the study and contributed to the writing of the manuscript.
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Communicated by Amy Parachnowitsch.
We used floral colour within communities to understand the role of biotic and abiotic drivers. Patterns matched well-known shifts in pollinator fauna and UV-irradiance along altitudinal gradients.
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Bergamo, P.J., Telles, F.J., Arnold, S.E.J. et al. Flower colour within communities shifts from overdispersed to clustered along an alpine altitudinal gradient. Oecologia 188, 223–235 (2018). https://doi.org/10.1007/s00442-018-4204-5
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DOI: https://doi.org/10.1007/s00442-018-4204-5