Abstract
A fundamental question in pollination ecology is how pollinators affect the evolution of different floral forms. Yet functional effects of shifts in floral form for plant and pollinator are frequently unclear. For instance, flowers that conceal pollen within tube-like anthers that are spread apart and move freely (free architecture) or are tightly joined together (joined architecture) have evolved independently across diverse plant families and are geographically widespread. Surprisingly, how their bee pollinators affect the function of both architectures remains unknown. We hypothesised that bee body size would affect foraging success and pollination differently for free and joined anther architectures. Therefore, we modified the anther architecture of a single plant species (Solanum elaeagnifolium) and used a single species of generalist bumble bee (Bombus impatiens), which varies greatly in body size. We found that on free anther architecture, larger bees were better pollinators. More pollen on their bodies was available for pollination and they deposited more pollen on stigmas. Conversely, on joined anther architecture, smaller bees were better pollinators. They collected less pollen into their pollen baskets, had more pollen on their bodies available for pollination, and deposited more pollen on stigmas. While we also found modest evidence that plants benefit more from joined versus free anther architecture, further investigation will likely reveal this also depends on pollinator traits. We discuss potential mechanisms by which pollinator size and anther architecture interact and implications for floral evolution.
Similar content being viewed by others
Data and code accessibility
The code and datasets supporting this article are available as electronic supplementary material.
Change history
08 July 2023
A Correction to this paper has been published: https://doi.org/10.1007/s00442-023-05413-x
References
Barrett SCH (2010) Darwin’s legacy: the forms, function and sexual diversity of flowers. Philos Trans r Soc B 365:351–368. https://doi.org/10.1098/rstb.2009.0212
Betts MG, Hadley AS, Kress WJ (2015) Pollinator recognition by a keystone tropical plant. PNAS 112:3433–3438. https://doi.org/10.1073/pnas.1419522112
Brito VLG, Nunes CEP, Resende CR, Montealegre-Zapata F, Vallejo-Marín M (2020) Biomechanical properties of a buzz-pollinated flower. Royal Soc Open Sci 7:1–9. https://doi.org/10.1098/rsos.201010
Buchmann SL, Shipman CW, Hansen HW (1990) Pollen residing in safe sites on honey bee foragers. Am Bee J 130:798–799
Cardinal S, Buchmann SL, Russell AL (2018) The evolution of floral sonication, a pollen foraging behavior used by bees (Anthophila). Evolution 72:590–600. https://doi.org/10.1111/evo.13446
Cariveau DP, Nayak GK, Bartomeus I, Zientek J, Ascher JS, Gibbs J, Winfree R (2016) The allometry of bee proboscis length and its uses in ecology. PLoS ONE 11:e0151482. https://doi.org/10.1371/journal.pone.0151482
Corbet SA, Huang S-H (2014) Buzz pollination in eight bumblebee-pollinated Pedicularis species: does it involve vibration-induced triboelectric charging of pollen grains? Ann Bot 114:1665–1674. https://doi.org/10.1093/aob/mcu195
Couvillon MJ, Jandt JM, Duong N, Dornhaus A (2010) Ontogeny of worker body size distribution in bumble bee (Bombus impatiens) colonies. Ecol Entomol 35:424–435. https://doi.org/10.1111/j.1365-2311.2010.01198.x
Cullen N, Xia J, Wei N, Kaczorowski R, Arceo-Gómez G, O’Neill E, Hayes R, Ashman T-L (2021) Diversity and composition of pollen loads carried by pollinators are primarily driven by insect traits, not floral community characteristics. Oecologia. https://doi.org/10.1007/s00442-021-04911-0
Dafni A (1992) Pollination ecology: a practical approach. Oxford University Press, Oxford
Darwin C (1877) The various contrivances by which orchids are fertilised by insects, 2nd edn. D Appleton and Company, New York
De Luca PA, Vallejo-Marín M (2013) What’s the ‘buzz’ about? The ecology and evolutionary significance of buzz-pollination. Curr Opin Plant Biol 16:429–435. https://doi.org/10.1016/j.pbi.2013.05.002
De Kock C, Minnaar C, Lunau K, Wester P, Verhoeven C, Schulze MJ, Randle MR, Robson C, Bolus RH, Anderson B (2018) The functional role of the keel crest in Polygala myrtifolia (Polygalaceae) and its effects on pollinator visitation success. S Afr J Bot 118:105–111. https://doi.org/10.1016/j.sajb.2018.06.011
De Luca PA, Bussière LF, Souto-Vilaros D, Goulson D, Mason AC, Vallejo-Marín M (2013) Variability in bumblebee pollination buzzes affects the quantity of pollen released from flowers. Oecologia 172:805–816. https://doi.org/10.1007/s00442-012-2535-1
De Luca PA, Cox DA, Vallejo-Marin M (2014) Comparison of pollination and defensive buzzes in bumblebees indicates species-specific and context-dependent vibrations. Naturwissenschaften 101:331–338
De Luca PA, Buchmann S, Galen C, Mason AC, Vallejo-Marín M (2019) Does body size predict the buzz-pollination frequencies used by bees? Ecol and Evol. https://doi.org/10.1002/ece3.5092
Endress PK (2012) The immense diversity of floral monosymmetry and asymmetry across angiosperms. Bot Rev 78:345–397. https://doi.org/10.1007/s12229-012-9106-3
Faegri K (1986) The solanoid flower. Trans & Proc Bot Soc Edinburgh 45:51–59. https://doi.org/10.1080/03746608608684993
Fox J (2015) Applied regression analysis and generalized linear models, 3rd edn. Sage Publications Inc., London
Fukuda Y, Suzuki K, Murata J (2001) The function of each sepal in pollinator behavior and effective pollination in Aconitum japonicum var. montanum. Plant Species Biol 16:151–157
Glover BJ, Bunnewell S, Martin C (2004) Convergent evolution within the genus Solanum: the specialised anther cone develops through alternative pathways. Gene 331:1–7. https://doi.org/10.1016/j.gene.2004.01.027
Grab H, Brokaw J, Anderson E, Gedlinske L, Gibbs J, Wilson J, Loeb G, Isaacs R, Poveda K (2019) Habitat enhancements rescue bee body size from the negative effects of landscape simplification. J Appl Ecol 56:2144–2154. https://doi.org/10.1111/1365-2664.13456
Harder LD (1985) Morphology as a predictor of flower choice by bumble bees. Ecology 66:198–210
Harder LD, Barclay RMR (1994) The functional significance of poricidal anthers and buzz pollination: controlled pollen removal from Dodecatheon. Funct Ecol 8:509–517
Harder LD, Wilson WG (1994) Floral evolution and male reproductive success: optimal dispensing schedules for pollen dispersal by animal-pollinated plants. Evol Ecol 8:542–559
Hartig F (2018) DHARMa: Residual diagnostics for hierarchical (multilevel/mixed) regression models. R package version 0.1.6. Available from: https://cran.r-project.org/web/packages/DHARMa/index.html. Accessed Apr 2022
Hazlehurst JA, Karubian JO (2016) Nectar robbing impacts pollinator behavior but not plant reproduction. Oikos 000:1–9. https://doi.org/10.1111/oik.03195
Herrera CM (1987) Components of pollinator “Quality”: comparative analysis of a diverse insect assemblage. Oikos 50:79–90
Hodges SA, Fulton M, Yang JY, Whittall JB (2003) Verne grant and evolutionary studies of Aquilegia. New Phyt 161:113–120. https://doi.org/10.1046/j.1469-8137.2003.00950.x
Hopkins R, Guerrero RF, Rausher MD, Kirkpatrick M (2014) Strong reinforcing selection in a Texas wildflower. Curr Biol 24:1995–1999. https://doi.org/10.1016/j.cub.2014.07.027
Huang Z-H, Liu H-L, Huang S-Q (2015) Interspecific pollen transfer between two coflowering species was minimized by bumble fidelity and differential pollen placement on the bumblebee body. J Plant Ecol 8:109–115. https://doi.org/10.1093/jpe/rtv015
Jankauski M, Ferguson R, Russell A, Buchmann S (2022) Structural dynamics of real and modelled Solanum stamens: implications for pollen ejection by buzzing bees. J Royal Soc Interface 19:1–10. https://doi.org/10.1098/rsif.2022.0040
Jauker F, Speckmann M, Wolters V (2016) Intra-specific body size determines pollination effectiveness. Basic Appl Ecol 17:714–719. https://doi.org/10.1016/j.baae.2016.07.004
Johnson SD, Anderson B (2010) Coevolution between food-rewarding flowers and their pollinators. Evol Educ Outreach 3:32–39. https://doi.org/10.1007/s12052-009-0192-6
Kaiser-Bunbury CN, Vázquez DP, Stang M, Ghazoul J (2014) Determinants of the microstructure of plant—pollinator networks. Ecology 95:3314–3324
Kelemen EP, Skyrm K, Dornhaus A (2022) Selection on size variation: more variation in bumble bee works and in the wild. Insectes Soc. https://doi.org/10.1007/s00040-022-00850-y
Klumpers SGT, Stang M, Klinkhamer PGL (2019) Foraging efficiency and size matching in a plant–pollinator community: the importance of sugar content and tongue length. Ecol Lett 22:469–479. https://doi.org/10.1111/ele.13204
Knapp S, Sagona E, Carbonell AKZ, Chiarini F (2017) A revision of the Solanum elaeagnifolium clade (Elaeagnifolium clade; subgenus Leptostemonum, Solanaceae). PhytoKeys 84:1–104. https://doi.org/10.3897/phytokeys.84.12695
Koch L, Lunau K, Wester P (2017) To be on the safe site—ungroomed spots on the bee’s body and their importance for pollination. PLoS ONE 12:1–16. https://doi.org/10.1371/journal.pone.0182522
Konzmann S, Hilgendorf F, Niester C, Rech AR, Lunau K (2020) Morphological specialization of heterantherous Rhynchanthera grandiflora (Melastomataceae) accommodates pollinator diversity. Plant Biol. https://doi.org/10.1111/plb.13102
Laverty TM (1994) Bumble bee learning and flower morphology. Anim Behav 47:531–545
Li J-K, Song Y-P, Xu H, Zhang Y-W, Zhu J-Y, Tang L-L (2015) High ratio of illegitimate visitation by small bees severely weakens the potential function of herteranthery. J of Plant Ecol 8:213–223. https://doi.org/10.1093/jpe/rtv021
Lichtenberg EM, Irwin RE, Bronstein JL (2018) Costs and benefits of alternative food handling tactics help explain facultative exploitation of pollination mutualisms. Ecology 99:1815–1824. https://doi.org/10.1002/ecy.02395
Macior LW (1968) Pollination adaption in Pedicularis groenlandica. Am J Bot 55:927–932
Magnusson A, Skaug H, Nielsen A, Berg C, Kristensen K, Maechler M, Bentham K von, Bolker, B, Sadat N, Lüdecke D, Lenth R, O'Brien J, Brooks M (2018) glmmTMB: generalized linear mixed models using template model builder. R package version 1.0.2.1. Available from: https://cran.r-project.org/web/packages/glmmTMB/index.html. Accessed Apr 2022
Mesquita-Neto JN, Viera AL, Schlindwein C (2021) Minimum size threshold of visiting bees of a buzz-pollinated plant species: consequences for pollination efficiency. Am J Bot 108:1–10. https://doi.org/10.1002/ajb2.1681
Minnaar C, Anderson B, Jager MLd, Karron JD (2018) Plant–pollinatorinteractions along the pathway to paternity. Ann Bot. https://doi.org/10.1093/aob/mcy167
Moreira-Hernández JI, Muchhala N (2019) Importance of pollinator-mediated interspecific pollen transfer for angiosperm evolution. Annu Rev Ecol Evol Syst 50:191–217. https://doi.org/10.1146/annurev-ecolsys-110218-024804)
Muchhala N, Thomson JD (2012) Interspecific competition in pollination systems: costs to male fitness via pollen misplacement. Func Ecol 26:476–482
Nevard L, Russell AL, Foord K, Vallejo-Marin M (2021) Transmission of bee-like vibrations in buzz-pollinated plants with different stamen architectures. Sci Rep 11:1–10. https://doi.org/10.1038/s41598-021-93029-7
Nooten SS, Rehan SM (2020) Historical changes in bumble bee body size and range shift of declining species. Biodivers Conserv 29:451–467. https://doi.org/10.1007/s10531-019-01893-7
Opedal ØH (2018) Herkogamy, a principal functional trait of plant reproductive biology. J Integr Plant Biol 179:677–687. https://doi.org/10.1086/700314
Papaj DR, Buchmann SL, Russell AL (2017) Division of labor of anthers in heterantherous plants: flexibility of bee pollen collection behavior may serve to keep plants honest. Arthropod-Plant Interact 00:1–9. https://doi.org/10.1007/s11829-017-9497-5
Parker AJ, Tran JL, Ison JL, Bai JDK, Weis AE, Thomson JD (2015) Pollen packing affects the function of pollen on corbiculate bees but not non-corbiculate bees. Arthropod-Plant Interact 9:197–203. https://doi.org/10.1007/s11829-015-9358-z
R Development Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rasband WS, ImageJ US (2011) National Institutes of Health, Bethesda, Maryland, USA. https://imagej.nih.gov/ij/. 1997–2021. Accessed Oct 2021
Russell AL, Golden RE, Leonard AS, Papaj DR (2016) Bees learn preferences for plant species that offer only pollen as a reward. Behav Ecol 27:731–740. https://doi.org/10.1093/beheco/arv213
Russell AL, Buchmann SL, Papaj DR (2017a) How a generalist bee achieves high efficiency of pollen collection on diverse floral resources. Behav Ecol. https://doi.org/10.1093/beheco/arx058
Russell AL, Morrison SJ, Moschonas EH, Papaj DR (2017b) Patterns of pollen and nectar foraging specialization by bumblebees over multiple timescales using RFID. Sci Rep 7:1–13. https://doi.org/10.1038/srep42448
Russell AL, Fetters AM, James EI, Ashman TL (2021) Pollinator effectiveness is affected by intraindividual behavioral variation. Oecologia. https://doi.org/10.1007/s00442-021-05016-4
Schiestl FP, Johnson SD (2013) Pollinator-mediated evolution of floral signals. TREE 28:307–315. https://doi.org/10.1016/j.tree.2013.01.019
Silberglied RE (1979) Communication in the ultraviolet. Annu Rev Ecol Evol Syst 10:373–398
Solis-Montero L, Vallejo-Marin M (2017) Does morphological fit between flowers and pollinators affect pollen deposition? An experimental test in a buzz-pollinated species with anther dimorphism. Ecol & Evol. https://doi.org/10.1002/ece3.2897
Sponsler D, Kallnik K, Requier F, Classen A, Maihoff AF, Sieger J, Steffan-Dewenter I (2022) Floral functional traits of mountain bumble bees are constrained but flexible through elevation and season. Oikos. https://doi.org/10.1111/oik.05876
Stout JC (1999) Does size matter? Bumblebee behavior and the pollination of Cytisus scoparius L doi: Fabaceae). Apidologie 31:129–139
Switzer CM, Russell AL, Papaj DR, Combes SA, Hopkins R (2019) Curr Zool 65:425–436. https://doi.org/10.1093/cz/zoz013
Tong Z-Y, Huang S-Q (2017) Safe sites of pollen placement: a conflict of interest between plants and bees? Oecologia. https://doi.org/10.1007/s00442-017-3999-9
Vallejo-Marín M (2019) Buzz pollination: studying bee vibrations on flowers. New Phyt. https://doi.org/10.1111/nph.15666
Vallejo-Marín M, Nunes CEP, Russell AL (2022) Anther cones increase pollen release in buzz-pollinated Solanum flowers. Evolution. https://doi.org/10.1111/evo.14485
van der Kooi CJ, Dyer AG, Kevan PG, Lunau K (2019) Functional significance of the optical properties of flowers for visual signalling. Ann Bot 123:1–14. https://doi.org/10.1093/aob/mcy119
Vlašánková A, Padyšáková E, Bartoš M, Mengual X, Janečková P, Janeček S (2017) The nectar spur is not only a simple specialization for long-proboscid pollinators. New Phyt 215:1574–1581. https://doi.org/10.1111/nph.14677
Vogel S (1978) Evolutionary shifts from reward to deception in pollen flowers. In: Richards AJ (ed) The pollination of flowers by insects. Academic Press Inc, Cambridge, MA, pp 89–96
Webb CJ, Lloyd DG (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms II. Herkogamy n z J Bot 24:163–178. https://doi.org/10.1080/0028825X.1986.10409726
Willmer PG, Finlayson K (2014) Big bees do a better job: intraspecific size variation influences pollination effectiveness. J Pollinat Ecol 14:244–254
Acknowledgements
We are grateful to Koppert Biologicals for bee colonies, Steve Buchmann for seeds, Abilene Mosher for greenhouse care, Jenny Burrow for assistance with pollen counting, and Russell lab members for discussion. We acknowledge this work was performed on unceded traditional territory of the Kiikaapoi, Sioux, and Osage.
Funding
Not applicable.
Author information
Authors and Affiliations
Contributions
RVW, MVM, and ALR: conceived and designed the experiments. RVW, MMM, and ALR: performed the experiments and collected the data. ALR and MVM analysed the data. RVW and ALR: wrote the original draft of the manuscript; the other authors provided editorial advice.
Corresponding author
Ethics declarations
Conflict of interest
Not applicable.
Ethical approval
All bumble bee experimentations were carried out in accordance with the legal and ethical standards of the USA.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Communicated by Jared Gregory Ali.
The original online version of this article was revised: Error in Figure 1 legend updated.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Wilkins, R.V., Mayberry, M.M., Vallejo-Marín, M. et al. Hold tight or loosen up? Functional consequences of a shift in anther architecture depend substantially on bee body size. Oecologia 200, 119–131 (2022). https://doi.org/10.1007/s00442-022-05246-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-022-05246-0