PREMISE: Animal-pollinated plants face a high risk of pollen loss during its transfer. To limit the negative effect of pollen losses by pollen consumption and heterospecific transfer, plant species may adjust and stratify their pollen availability during the day (i.e., "schedule" their pollen presentation) and attract pollinators in specific time frames. METHODS: We investigated diurnal patterns of pollen availability and pollinator visitation in three coflowering plant species: Succisa pratensis with open flowers and accessible pollen, pollinated mainly by pollen-feeding hoverflies; Centaurea jacea with open flowers and less accessible pollen, pollinated mainly by pollen-collecting bees; and Trifolium hybridum with closed flowers and pollen accessible only after the active opening of the flower, pollinated exclusively by bees. RESULTS: The three plant species differed in the peak pollen availability, tracked by the visitation activity of their pollinators. Succisa pratensis released all pollen in the morning, while pollinator activity was still low and peaked with a slight delay. In contrast, C. jacea and T. hybridum had distinct pollen presentation schedules, peaking in the early afternoon. The pollinator visitation to both of these species closely matched their pollen availability. CONCLUSIONS: Stratifying pollen availability to pollinators during the day may be one of several mechanisms that allow coflowering plants to share their pollinators and decrease the probability of heterospecific pollen transfer.

Department of Biology Faculty of Science York University 4700 Keele Street 203D M3J 1P3 Toronto Canada

Department of Botany Faculty of Science Charles University Benátská 2 CZ 128 41 Prague Czech Republic

Department of General Zoology Faculty of Natural Sciences 1 Biosciences Martin Luther University Hoher Weg 8 06100 Halle Germany

Department of Zoology Faculty of Science Charles University Viničná 7 CZ 128 41 Prague Czech Republic

Svatý Jan t Krsovice 1 285 04 Uhlířské Janovice Czech Republic

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Aluri, R. J. S., and C. S. Reddi. 1995. Explosive pollen release and pollination in flowering plants. Proceedings of Indian National Science Academy 61: 323-332.

Arceo-Gómez, G., L. Abdala-Roberts, A. Jankowiak, C. Kohler, G. A. Meindl, C. M. Navarro-Fernández, V. Parra-Tabla, et al. 2016. Patterns of among- and within-species variation in heterospecific pollen receipt: the importance of ecological generalization. American Journal of Botany 103: 396-407.

Ballantyne, G., K. C. R. Baldock, L. Rendell, and P. G. Willmer. 2017. Pollinator importance networks illustrate the crucial value of bees in a highly speciose plant community. Scientific Reports 7: 1-13.

Baude, M., É. Danchin, M. Mugabo, and I. Dajoz. 2011. Conspecifics as informers and competitors: an experimental study in foraging bumble-bees. Proceedings of the Royal Society, B, Biological Sciences 278: 2806-2813.

Berg, S., D. Kutra, T. Kroeger, C. N. Straehle, B. X. Kausler, C. Haubold, M. Schiegg, et al. 2019. Ilastik: interactive machine learning for (bio)image analysis. Nature Methods 16: 1226-1232.

Brosi, B. J. 2016. Pollinator specialization: from the individual to the community. New Phytologist 210: 1190-1194.

Castellanos, M. C., P. Wilson, S. J. Keller, A. D. Wolfe, and J. D. Thomson. 2006. Anther evolution: pollen presentation strategies when pollinators differ. American Naturalist 167: 288-296.

Castellanos, M. C., P. Wilson, and J. D. Thomson. 2004. “Anti-bee” and “pro-bird” changes during the evolution of hummingbird pollination in Penstemon flowers. Journal of Evolutionary Biology 17: 876-885.

Charnov, E. L. 1976. Optimal foraging, the marginal value theorem. Theoretical Population Biology 9: 129-136.

Chittka, L., and A. Brockmann. 2005. Perception space-the final frontier. PLoS Biology 3: e137.

Chittka, L., A. Gumbert, and J. Kunze. 1997. Foraging dynamics of bumble bees: correlates of movements within and between plant species. Behavioral Ecology 8: 239-249.

Dukas, R., and L. A. Real. 1993. Effects of recent experience on foraging decisions by bumble bees. Oecologia 94: 244-246.

Dupont, Y. L., K. Trøjelsgaard, and J. M. Olesen. 2011. Scaling down from species to individuals: a flower-visitation network between individual honeybees and thistle plants. Oikos 120: 170-177.

Eisen, K., A. L. Case, and C. M. Caruso. 2017. Variation in pollen-dispensing schedules of Lobelia siphilitica. International Journal of Plant Sciences 178: 79-84.

Erbar, C., and P. Leins. 1995. Portioned pollen release and the syndromes of secondary pollen presentation in the Campanulales-Asterales-complex. Flora 190: 323-338.

Galloni, M., L. Podda, D. Vivarelli, and G. Cristofolini. 2007. Pollen presentation, pollen-ovule ratios, and other reproductive traits in Mediterranean legumes (fam. Fabaceae-subfam Faboideae). Plant Systematics and Evolution 266: 147-164.

Gong, Y. B., and S. Q. Huang. 2014. Interspecific variation in pollen-ovule ratio is negatively correlated with pollen transfer efficiency in a natural community. Plant Biology 16: 843-847.

Gregg, K. B. 1991. Reproductive strategy of Cleistes divaricata (Orchidaceae). American Journal of Botany 78: 350-360.

Harder, L. D., C. Y. Jordan, W. E. Gross, and M. B. Routley. 2004. Beyond floricentrism: the pollination function of inflorescences. Plant Species Biology 19: 137-148.

Harder, L. D., and J. D. Thomson. 1989. Evolutionary options for maximizing pollen dispersal of animal-pollinated plants. American Naturalist 133: 323344.

Harder, L. D., and W. G. Wilson. 1994. Floral evolution and male reproductive success: optimal dispensing schedules for pollen dispersal by animal-pollinated plants. Evolutionary Ecology 8: 542-559.

Harder, L. D., and W. G. Wilson. 1998. Theoretical consequences of heterogeneous transport conditions for pollen dispersal by animals. Ecology 79: 2789-2807.

Hegland, S. J., J. A. Grytnes, and Ø. Totland. 2009. The relative importance of positive and negative interactions for pollinator attraction in a plant community. Ecological Research 24: 929-936.

Heinrich, B. 1976. Bumblebee foraging and the economics of sociality. American Scientist 64: 384-395.

Herrera, C. M. 1990. Daily patterns of pollinator activity, differential pollinating effectiveness, and floral resource availability, in a summer-flowering Mediterranean shrub. Oikos 58: 277.

Hersch, E. I., and B. A. Roy. 2007. Context-dependent pollinator behavior: an explanation for patterns of hybridization among three species of Indian paintbrush. Evolution 61: 111-124.

Holmquist, K. G., R. J. Mitchell, and J. D. Karron. 2012. Influence of pollinator grooming on pollen-mediated gene dispersal in Mimulus ringens (Phrymaceae). Plant Species Biology 27: 77-85.

Huang, S.-Q., and X.-Q. Shi. 2013. Floral isolation in pedicularis: how do congeners with shared pollinators minimize reproductive interference? New Phytologist 199: 858-865.

Huang, Z.-H., H.-L. Liu, and S.-Q. Huang. 2015. Interspecific pollen transfer between two coflowering species was minimized by bumblebee fidelity and differential pollen placement on the bumblebee body. Journal of Plant Ecology 8: 109-115.

Ishii, H. S., and S. Sakai. 2001. Effects of display size and position on individual floral longevity in racemes of Narthecium asiaticum (Liliaceae). Functional Ecology 15: 396-405.

Janovský, Z., M. Mikát, J. Hadrava, E. Horčičková, K. Kmecová, D. Požárová, J. Smyčka, and T. Herben. 2013. Conspecific and heterospecific plant densities at small-scale can drive plant-pollinator interactions. PLoS One 8: 77361.

Karron, J. D., R. J. Mitchell, K. G. Holmquist, J. M. Bell, and B. Funk. 2004. The influence of floral display size on selfing rates in Mimulus ringens. Heredity 92: 242-248.

Koch, L., K. Lunau, and P. Wester. 2017. To be on the safe site-ungroomed spots on the bee's body and their importance for pollination. PLoS One 12: e0182522.

Koski, M. H., J. L. Ison, A. Padilla, A. Q. Pham, and L. F. Galloway. 2018. Linking pollinator efficiency to patterns of pollen limitation: small bees exploit the plant-pollinator mutualism. Proceedings of the Royal Society, B, Biological Sciences 285: 20180635.

Kudo, G., and L. D. Harder. 2005. Floral and inflorescence effects on variation in pollen removal and seed production among six legume species. Functional Ecology 19: 245-254.

Kunin, W. E. 1993. Sex and the single mustard: population density and pollinator behavior effects on seed-set. Ecology 74: 2145-2160.

Lebuhn, G., and G. J. Anderson. 1994. Anther tripping and pollen dispensing in Berberis thunbergii. American Midland Naturalist 131: 257-265.

LeBuhn, G., and K. Holsinger. 1998. A sensitivity analysis of pollen-dispensing schedules. Evolutionary Ecology 12: 111-121.

Liao, W.-J., and L. D. Harder. 2014. Consequences of multiple inflorescences and clonality for pollinator behavior and plant mating. American Naturalist 184: 580-592.

Lloyd, D. G., and J. M. A. Yates. 1982. Intrasexual selection and the segregation of pollen and stigmas in hermaphrodite plants, exemplified by Wahlenbergia albomarginata (Campanulaceae). Evolution 36: 903-913.

Lucas, A., O. Bodger, B. J. Brosi, C. R. Ford, D. W. Forman, C. Greig, M. Hegarty, et al. 2018. Floral resource partitioning by individuals within generalised hoverfly pollination networks revealed by DNA metabarcoding. Scientific Reports 8: 1-11.

Moreira-Hernández, J. I., and N. Muchhala. 2019. Importance of pollinator-mediated interspecific pollen transfer for angiosperm evolution. Annual Review of Ecology, Evolution, and Systematics 50: 191-217.

Nansen, C., and S. Korie. 2000. Determining the time delay of honey bee (Apis mellifera) foraging response to hourly pollen release in a typical pollen flower (Cistus salvifolius). Journal of Apicultural Research 39: 93101.

Parker, A. J., N. M. Williams, and J. D. Thomson. 2016. Specialist pollinators deplete pollen in the spring ephemeral wildflower Claytonia virginica. Ecology and Evolution 6: 5169-5177.

Percival, M. 1950. Pollen presentation and pollen collection. New Phytologist 49: 40-63.

Peuker, M. A., H. Burger, S. Krausch, U. Neumüller, M. Ayasse, and J. Kuppler. 2020. Floral traits are associated with the quality but not quantity of heterospecific stigmatic pollen loads. BMC Ecology 20: 1-11.

Popic, T. J., G. M. Wardle, and Y. C. Davila. 2013. Flower-visitor networks only partially predict the function of pollen transport by bees. Austral Ecology 38: 76-86.

Pyke, G. H. 1978. Optimal foraging: movement patterns of bumblebees between inflorescences. Theoretical Population Biology 13: 7298.

Pyke, G. H. 2019. Optimal foraging theory: an introduction, 2nd ed. Elsevier, Amsterdam, Netherlands.

Queiroz, J. A., Z. G. M. Quirino, and I. C. Machado. 2015. Floral traits driving reproductive isolation of two co-flowering taxa that share vertebrate pollinators. AoB Plants 7: plv127.

R Core Team. 2022. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Website: https://www.r-project.org

Rademaker, M. C. J., T. J. de Jong, and P. G. L. Klinkhamer. 1997. Pollen dynamics of bumble-bee visitation on Echium vulgare. Functional Ecology 11: 554-563.

Rader, R., B. G. Howlett, S. A. Cunningham, D. A. Westcott, and W. Edwards. 2012. Spatial and temporal variation in pollinator effectiveness: Do unmanaged insects provide consistent pollination services to mass flowering crops? Journal of Applied Ecology 49: 126-134.

Ren, M. X., and Z. J. Bu. 2014. Is there ‘anther-anther interference’ within a flower? Evidences from one-by-one stamen movement in an insect-pollinated plant. PLoS One 9: 1-7.

Schindelin, J., I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, et al. 2012. Fiji: an open-source platform for biological-image analysis. Nature Methods 9: 676-682.

Schwarz, B., C. F. Dormann, D. P. Vázquez, and J. Fründ. 2021. Within-day dynamics of plant-pollinator networks are dominated by early flower closure: an experimental test of network plasticity. Oecologia 196: 781-794.

Stanghellini, M. S., J. T. Ambrose, and J. R. Schultheis. 2002a. Diurnal activity, floral visitation and pollen deposition by honey bees and bumble bees on field-grown cucumber and watermelon. Journal of Apicultural Research 41: 27-34.

Stanghellini, M. S., J. R. Schultheis, and J. T. Ambrose. 2002b. Pollen mobilization in selected Cucurbitaceae and the putative effects of pollinator abundance on pollen depletion rates. Journal of the American Society for Horticultural Science 127: 729-736.

Stone, G. N., P. Willmer, and J. Alexandra Rowe. 1998. Partitioning of pollinators during flowering in an African Acacia community. Ecology 79: 2808-2827.

Thomson, J. D. 2006. Tactics for male reproductive success in plants: contrasting insights of sex allocation theory and pollen presentation theory. Integrative and Comparative Biology 46: 390397.

Thomson, J. D., M. A. McKenna, and M. B. Cruzan. 1989. Temporal patterns of nectar and pollen production in Aralia hispida: implications for reproductive success. Ecology 70: 1061-1068.

Tur, C., B. Vigalondo, K. Trøjelsgaard, J. M. Olesen, and A. Traveset. 2014. Downscaling pollen-transport networks to the level of individuals. Journal of Animal Ecology 83: 306-317.

Waddington, K. D. 1980. Flight patterns of foraging bees relative to density of artificial flowers and distribution of nectar. Oecologia 44: 199-204.

Wang, X., T. Zeng, M. Wu, and D. Zhang. 2021. A half-day flowering pattern helps plants sharing pollinators in an oceanic island community. Journal of Tropical Ecology 37: 16-25.

Waser, N. M. 1986. Flower constancy: definition, cause, and measurement. American Naturalist 127: 593-603.

Willmer, P., and K. Finlayson. 2014. Big bees do a better job: intraspecific size variation influences pollination effectiveness. Journal of Pollination Ecology 14: 244-254.

Young, H. J., D. W. Dunning, and K. W. Von Hasseln. 2007. Foraging behavior affects pollen removal and deposition in Impatiens capensis (Balsaminaceae). American Journal of Botany 94: 1267-1271.

Young, H. J., and M. L. Stanton. 1990. Temporal patterns of gamete production within individuals of Raphanus sativus (Brassicaceae). Canadian Journal of Botany 68: 480-486.

Zhang, T., X. Tang, and Q. Fang. 2021. Pollinator sharing among co-flowering plants mediates patterns of pollen transfer. Alpine Botany 131: 125-133.