Visitation of plants by different pollinators depends on individual plant traits, spatial context, and other factors. A neglected aspect of small-scale variation of plant-pollinator interactions is the role of vertical position of flowers. We conducted a series of experiments to study vertical stratification of plant-pollinator interactions in a dry grassland. We observed flower visitors on cut inflorescences of Centaurea scabiosa and Inula salicina placed at different heights above ground in two types of surrounding vegetation: short and tall. Even at such a small-scale, we detected significant shift in total visitation rate of inflorescences in response to their vertical position. In short vegetation, inflorescences close to the ground were visited more frequently, while in tall vegetation, inflorescences placed higher received more visits. Moreover, we found major differences in the composition of the pollinator community on flowers at different heights. In a second experiment, we measured flower visitation rate in inflorescences of Salvia verticillata of variable height. Total flower visitation rate increased markedly with inflorescence height in this case. Data on seed set of individual plants provide evidence for a corresponding positive pollinator-mediated selection on increased inflorescence height. Overall, our results demonstrate strong vertical stratification of plant-pollinator interactions at the scale of mere decimetres. This may have important ecological as well as evolutionary implications.

Czech Academy of Sciences Biology Centre Institute of Entomology České Budějovice Czech Republic

Department of Zoology Faculty of Science Charles University Prague Czech Republic

See more in PubMed

Ågren J, Fortunel C, Ehrlén J. Selection on floral display in insect-pollinated Primula farinosa: effects of vegetation height and litter accumulation. Oecologia. 2006;150(2):225–232. doi: 10.1007/s00442-006-0509-x. PubMed DOI

Akter A, Biella P, Klecka J. Effects of small-scale clustering of flowers on pollinator foraging behaviour and flower visitation rate. PLOS ONE. 2017;12(11):e0187976. doi: 10.1371/journal.pone.0187976. PubMed DOI PMC

Andersson S. Floral variation in Saxifraga granulata: phenotypic selection, quantitative genetics and predicted responses to selection. Heredity. 1996;77(2):217–223. doi: 10.1038/hdy.1996.127. DOI

Bartkowska MP, Johnston MO. The sexual neighborhood through time: competition and facilitation for pollination in Lobelia cardinalis. Ecology. 2014;95(4):910–919. doi: 10.1890/13-0447.1. PubMed DOI

Bascompte J, Jordano P, Melián CJ, Olesen JM. The nested assembly of plant–animal mutualistic networks. Proceedings of the National Academy of Sciences of the United States of America. 2003;100(16):9383–9387. doi: 10.1073/pnas.1633576100. PubMed DOI PMC

Bascompte J, Jordano P, Olesen JM. Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science. 2006;312(5772):431–433. doi: 10.1126/science.1123412. PubMed DOI

Bascompte J, Jordano P. Plant-animal mutualistic networks: the architecture of biodiversity. Annual Review of Ecology Evolution and Systematics. 2007;38(1):567–593. doi: 10.1146/annurev.ecolsys.38.091206.095818. DOI

Bronstein JL, Alarcón R, Geber M. The evolution of plant–insect mutualisms. New Phytologist. 2006;172(3):412–428. doi: 10.1111/j.1469-8137.2006.01864.x. PubMed DOI

Caraballo-Ortiz MA, Santiago-Valentin E, Carlo TA. Flower number and distance to neighbours affect the fecundity of Goetzea elegans (Solanaceae) Journal of Tropical Ecology. 2011;27(5):521–528. doi: 10.1017/s0266467411000289. DOI

Červenková Z, Münzbergová Z. Pollen limitation and pollinator preferences in Scorzonera hispanica. Plant Biology. 2014;16(5):967–972. doi: 10.1111/plb.12142. PubMed DOI

de Jong TJ, Waser NM, Klinkhamer PG. Geitonogamy: the neglected side of selfing. Trends in Ecology & Evolution. 1993;8(9):321–325. doi: 10.1016/0169-5347(93)90239-l. PubMed DOI

Dupont YL, Trøjelsgaard K, Hagen M, Henriksen MV, Olesen JM, Pedersen NM, Kissling WD. Spatial structure of an individual-based plant–pollinator network. Oikos. 2014;123(11):1301–1310. doi: 10.1111/oik.01426. DOI

Ehrlén J, Käck S, Ågren J. Pollen limitation, seed predation and scape length in Primula farinosa. Oikos. 2002;97(1):45–51. doi: 10.1034/j.1600-0706.2002.970104.x. DOI

Espíndola A, Pellissier L, Alvarez N. Variation in the proportion of flower visitors of Arum maculatum along its distributional range in relation with community-based climatic niche analyses. Oikos. 2011;120(5):728–734. doi: 10.1111/j.1600-0706.2010.18937.x. DOI

Faulkner G. Honeybee behaviour as affected by plant height and flower colour in brussels sprouts. Journal of Apicultural Research. 1976;15(1):15–18. doi: 10.1080/00218839.1976.11099827. DOI

Gerber MA. The relationship of plant size to self-pollination in Mertensia ciliata. Ecology. 1985;66(3):762–772. doi: 10.2307/1940537. DOI

Grant V, Grant KA. Flower Pollination in the Phlox Family. New York: Columbia University Press; 1965.

Gumbert A, Kunze J. Inflorescence height affects visitation behavior of bees–a case study of an aquatic plant community in Bolivia. Biotropica. 1999;31(3):466–477. doi: 10.1111/j.1744-7429.1999.tb00389.x. DOI

Hoehn P, Tscharntke T, Tylianakis JM, Steffan-Dewenter I. Functional group diversity of bee pollinators increases crop yield. Proceedings of the Royal Society B: Biological Sciences. 2008;275(1648):2283–2291. doi: 10.1098/rspb.2008.0405. PubMed DOI PMC

Jiang X-F, Li Q-J. Self-and intra-morph incompatibility and selection analysis of an inconspicuous distylous herb growing on the Tibetan plateau (Primula tibetica) Ecology and Evolution. 2017;7(15):5746–5753. doi: 10.1002/ece3.3151. PubMed DOI PMC

Junker RR, Blüthgen N, Brehm T, Binkenstein J, Paulus J, Schaefer HM, Stang M. Specialization on traits as basis for the niche-breadth of flower visitors and as structuring mechanism of ecological networks. Functional Ecology. 2013;27(2):329–341. doi: 10.1111/1365-2435.12005. DOI

King C, Ballantyne G, Willmer PG. Why flower visitation is a poor proxy for pollination: measuring single-visit pollen deposition, with implications for pollination networks and conservation. Methods in Ecology and Evolution. 2013;4(9):811–818. doi: 10.1111/2041-210x.12074. DOI

Lande R, Arnold SJ. The measurement of selection on correlated characters. Evolution. 1983;37(6):1210–1226. doi: 10.2307/2408842. PubMed DOI

Levin DA, Kerster HW. Assortative pollination for stature in Lythrum salicaria. Evolution. 1973;27(1):144–152. doi: 10.2307/2407128. PubMed DOI

Morris WF, Price MV, Waser NM, Thomson JD, Thomson B, Stratton DA. Systematic increase in pollen carryover and its consequences for geitonogamy in plant populations. Oikos. 1994;71(3):431–440. doi: 10.2307/3545831. DOI

Nagamitsu T, Momose K, Inoue T, Roubik DW. Preference in flower visits and partitioning in pollen diets of stingless bees in an Asian tropical rain forest. Researches on Population Ecology. 1999;41(2):195–202. doi: 10.1007/s101440050023. DOI

Newman E, Manning J, Anderson B. Local adaptation: mechanical fit between floral ecotypes of Nerine humilis (Amaryllidaceae) and pollinator communities. Evolution. 2015;69(9):2262–2275. doi: 10.1111/evo.12736. PubMed DOI

Ohashi K, Yahara T. Effects of variation in flower number on pollinator visits in Cirsium purpuratum (Asteraceae) American Journal of Botany. 1998;85(2):219–224. doi: 10.2307/2446309. PubMed DOI

Olesen JM, Bascompte J, Elberling H, Jordano P. Temporal dynamics in a pollination network. Ecology. 2008;89(6):1573–1582. doi: 10.1890/07-0451.1. PubMed DOI

Paton DC. Honeybees in the Australian environment. Bioscience. 1993;43(2):95–103. doi: 10.2307/1311970. DOI

Peakall R, Handel SN. Pollinators discriminate among floral heights of a sexually deceptive orchid: implications for selection. Evolution. 1993;47(6):1681–1687. doi: 10.2307/2410212. PubMed DOI

Pyke GH. Optimal foraging: movement patterns of bumblebees between inflorescences. Theoretical Population Biology. 1978;13(1):72–98. doi: 10.1016/0040-5809(78)90036-9. PubMed DOI

R Core Team . R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing; 2015.

Ramalho M. Stingless bees and mass flowering trees in the canopy of atlantic forest: a tight relationship. Acta Botanica Brasilica. 2004;18(1):37–47. doi: 10.1590/s0102-33062004000100005. DOI

Roubik DW. Tropical pollinators in the canopy and understory: field data and theory for stratum “preferences”. Journal of Insect Behavior. 1993;6(6):659–673. doi: 10.1007/bf01201668. DOI

Ruane LG, Hancock LM, Rotzin AT, Luce CN. Pollen viability and the potential for self-pollen interference in Phlox hirsuta, an endangered species. International Journal of Plant Sciences. 2013;174(9):1251–1258. doi: 10.1086/673244. DOI

Ruane LG, Rotzin AT, Congleton PH. Floral display size, conspecific density and florivory affect fruit set in natural populations of Phlox hirsuta, an endangered species. Annals of Botany. 2014;113(5):887–893. doi: 10.1093/aob/mcu007. PubMed DOI PMC

Schlinkert H, Westphal C, Clough Y, Grass I, Helmerichs J, Tscharntke T. Plant size affects mutualistic and antagonistic interactions and reproductive success across 21 Brassicaceae species. Ecosphere. 2016;7(12):e01529. doi: 10.1002/ecs2.1529. DOI

Sletvold N, Grindeland JM, Ågren J. Pollinator-mediated selection on floral display, spur length and flowering phenology in the deceptive orchid Dactylorhiza lapponica. New Phytologist. 2010;188(2):385–392. doi: 10.1111/j.1469-8137.2010.03296.x. PubMed DOI

Sletvold N, Grindeland JM, Ågren J. Vegetation context influences the strength and targets of pollinator-mediated selection in a deceptive orchid. Ecology. 2013;94(6):1236–1242. doi: 10.1890/12-1840.1. PubMed DOI

Sletvold N, Grindeland JM. Floral herbivory increases with inflorescence size and local plant density in Digitalis purpurea. Acta Oecologica. 2008;34(1):21–25. doi: 10.1016/j.actao.2008.03.002. DOI

Suchan T, Alvarez N. Fifty years after Ehrlich and Raven, is there support for plant–insect coevolution as a major driver of species diversification? Entomologia Experimentalis et Applicata. 2015;157(1):98–112. doi: 10.1111/eea.12348. DOI

Thomson JD, Plowright R. Pollen carryover, nectar rewards, and pollinator behavior with special reference to Diervilla lonicera. Oecologia. 1980;46(1):68–74. doi: 10.1007/bf00346968. PubMed DOI

Toräng P, Ehrlén J, Ågren J. Facilitation in an insect-pollinated herb with a floral display dimorphism. Ecology. 2006;87(8):2113–2117. doi: 10.1890/0012-9658(2006)87[2113:fiaihw]2.0.co;2. PubMed DOI

Trunschke J, Sletvold N, Ågren J. Interaction intensity and pollinator-mediated selection. New Phytologist. 2017;214(3):1381–1389. doi: 10.1111/nph.14479. PubMed DOI

Ulyshen MD, Soon V, Hanula JL. On the vertical distribution of bees in a temperate deciduous forest. Insect Conservation and Diversity. 2010;3(3):222–228. doi: 10.1111/j.1752-4598.2010.00092.x. DOI

Waser NM, Price MV. Reproductive costs of self-pollination in Ipomopsis aggregata (Polemoniaeae): are ovules usurped? American Journal of Botany. 1991;78(8):1036–1043. doi: 10.2307/2444892. DOI

Wood S. Generalized Additive Models: An Introduction with R. Boca Raton: CRC press; 2006.

Individual-level specialisation and interspecific resource partitioning in bees revealed by pollen DNA metabarcoding

Water stress and nitrogen supply affect floral traits and pollination of the white mustard, Sinapis alba (Brassicaceae)

Flower visitation by hoverflies (Diptera: Syrphidae) in a temperate plant-pollinator network