The tripping mechanism of flowers affects pollen transfer dynamics
DOI:
https://doi.org/10.26786/1920-7603(2023)770Keywords:
Bumble bee, Flower visits, Pollen deposition, Pollen grains on the bee's body, Medicago sativa, Tripped flowersAbstract
Insect pollinators affect pollen transfer dynamics, with consequences for pollen movement and the genetic structure of plant populations. Pollen transfer dynamics has not been previously examined in flowers with a tripping mechanism. Here we examine whether pollen accumulated on a bee’s body increases with the number of Medicago sativa L. flowers tripped by Bombus impatiens Cresson during a foraging bout, while controlling for bee body size and number of visited flowers. In a second experiment, we determine whether the number of revisits to a tripped flower increases pollen deposition onto the stigmas. We set up three M. sativa plants with a controlled number of racemes in a greenhouse room, and followed individual bees as they foraged, recording each plant, raceme, and flower visited. For pollen accumulated, we collected bees at the end of their foraging bout and counted pollen grains on their body. For pollen deposition, we collected flowers with between 0 and 6 revisits and counted the pollen grains on the stigmas. The number of pollen grains on a bee’s body increased with the number of flowers tripped in a foraging bout, but was not affected by the number of flowers visited or the size of individual bees. The number of pollen grains deposited on a stigma did not increase with the number of revisits to a tripped flower. This latter result contrasts with plants without a tripping mechanism where the number of visits increases pollen deposition and seed set. Tripping affects pollen transfer dynamics and we discuss how its effect may vary with the mode of tripping.
References
Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics International 11(7): 36-42.
Abrol DP (2007) Honeybees and rapeseed: A pollinator-plant interaction. Advances in Botanical Research 45: 337-367. https://doi.org/10.1016/S0065-2296(07)45012-1 DOI: https://doi.org/10.1016/S0065-2296(07)45012-1
Adler LS, Irwin RE (2006) Comparison of pollen transfer dynamics by multiple floral visitors: Experiments with pollen and fluorescent dye. Annals of Botany 97(1): 141-150. https://doi.org/10.1093/aob/mcj012 DOI: https://doi.org/10.1093/aob/mcj012
Armstrong JM, White WJ (1935) Factors influencing seed setting in alfalfa. Journal of Agricultural Science 25: 161-79. DOI: https://doi.org/10.1017/S0021859600009667
Bohart GE (1957) Pollination of alfalfa and red clover. Annual Review of Entomology 2: 255-380. https://doi.org/10.1146/annurev.en.02.010157.002035 DOI: https://doi.org/10.1146/annurev.en.02.010157.002035
Boyer KJ, Fragoso FP, Dieterich Mabin ME, Brunet J (2020) Netting and pan traps fail to identify the pollinator guild of an agricultural crop. Scientific Reports 10: 13819. https://doi.org/10.1038/s41598-020-70518-9 DOI: https://doi.org/10.1038/s41598-020-70518-9
Boyle NK, Kesoju SR, Greene SL, Martin RC, Walsh DB (2017) Migratory bee hive transportation contributes insignificantly to transgenic pollen movement between spatially isolated alfalfa seed fields. Journal of Economic Entomology 110(1): 6-12. https://doi.org/10.1093/jee/tow243 DOI: https://doi.org/10.1093/jee/tow243
Brunet J, Stewart CM (2010) Impact of bee species and plant density on alfalfa pollination and potential for gene flow. Psyche: A Journal of Entomology 2010: Article ID 201858. https://doi.org/10.1155/2010/201858 DOI: https://doi.org/10.1155/2010/201858
Brunet J, Thairu MW, Henss JM, Link RI, Kluever JA (2015) The effects of flower, floral display and reward sizes on bumblebee foraging behavior when pollen is the reward and plants are dichogamous. International Journal of Plant Sciences 176(9): 811-819. https://doi.org/10.1086/683339 DOI: https://doi.org/10.1086/683339
Brunet J, Zhao Y, Clayton MK (2019a) Linking the foraging behavior of three bee species to pollen dispersal and gene flow. PloS ONE 14(2): e0212561. https://doi.org/10.1371/journal.pone.0212561 DOI: https://doi.org/10.1371/journal.pone.0212561
Brunet J, Ziobro R, Osvatic J, Clayton MK (2019b) The effects of time, temperature and plant variety on pollen viability and its implications for gene flow risk. Plant Biology 21(4): 715-722. https://doi.org/10.1111/plb.12959 DOI: https://doi.org/10.1111/plb.12959
Brunet J, Minahan DF (2023) Honey bee pollination ecology. In “Purdy J, (ed), The foraging behavior of the Honey bee (Apis mellifera L.). Elsevier, New York, New York, pp. 121-150. https://doi.org/10.1016/C2021-0-00252-2 DOI: https://doi.org/10.1016/B978-0-323-91793-3.00004-3
Castellanos MC, Wilson P, Thomson JD (2003) Pollen transfer by hummingbirds and bumblebees, and the divergence of pollination modes in Penstemon. Evolution 57(12): 2742-2752. https://doi.org/10.1111/j.0014-3820.2003.tb01516.x DOI: https://doi.org/10.1111/j.0014-3820.2003.tb01516.x
Cresswell JE (1990) How and why do nectar-foraging bumblebees initiate movements between inflorescence of wild bergamot Monarda fistulosa (Lamiaceae)? Oecologia 82: 450-460. https://doi.org/10.1007/BF00319785 DOI: https://doi.org/10.1007/BF00319785
Cresswell JE (1999) The influence of nectar and pollen availability on pollen transfer by individual flowers of oil-seed rape (Brassica napus) when pollinated by bumblebees (Bombus lapidarius). Journal of Ecology 87: 670-677. https://doi.org/10.1046/j.1365-2745.1999.00385.x DOI: https://doi.org/10.1046/j.1365-2745.1999.00385.x
Engel EC, Irwin RE (2003) Linking pollinator visitation rate and pollen receipt. American Journal of Botany 90(11): 1612-1618. https://doi.org/10.3732/ajb.90.11.1612 DOI: https://doi.org/10.3732/ajb.90.11.1612
Foldesi R, Howlett BG, Grass I, Batáry P (2020) Larger pollinators deposit more pollen on stigmas across multiple plant species – A meta-analysis. Journal of Applied Ecology 58: 699-707. https://doi.org/10.1111/1365-2664.13798 DOI: https://doi.org/10.1111/1365-2664.13798
Fragoso FP, Brunet J (2023) Differential ability of three bee species to move genes via pollen. PLoS ONE 18(4): e0271780. https://doi.org/10.1371/journal.pone.0271780 DOI: https://doi.org/10.1371/journal.pone.0271780
Ge Y, Fu C, Bhandari H, Bouton J, Brummer EC, Wang Z-Y (2011) Pollen viability and longevity of switchgrass (Panicum virgatum L.). Crop Science 51(6): 2698-2705. https://doi.org/10.2135/cropsci2011.01.0057 DOI: https://doi.org/10.2135/cropsci2011.01.0057
Goulson D, Hawson SA, Stout JC (1998) Foraging bumblebees avoid flowers already visited by conspecifics or by other bumblebee species. Animal Behavior 55: 199-206. https://doi.org/10.1006/anbe.1997.0570 DOI: https://doi.org/10.1006/anbe.1997.0570
Harder LD (1990) Behavioral responses by bumble bees to variation in pollen availability. Oecologia 85: 41-47. https://doi.org/10.1007/BF00317341 DOI: https://doi.org/10.1007/BF00317341
Harder LD, Thomson JD (1989) Evolutionary options for maximizing pollen dispersal of animal-pollinated plants. The American Naturalist 133(3): 323-344. https://doi.org/10.1086/284922 DOI: https://doi.org/10.1086/284922
Harder LD, Wilson WG (1998) Theoretical consequences of heterogeneous transport conditions for pollen dispersal by animals. Ecology 79(8): 2789-2807. https://doi.org/10.1890/0012-9658(1998)079[2789:TCOHTC]2.0.CO;2 DOI: https://doi.org/10.1890/0012-9658(1998)079[2789:TCOHTC]2.0.CO;2
Irwin RE, Brody AK (1999) Nectar-robbing bumble bees reduce the fitness of Ipomopsis aggregata (Polemoniaceae). Ecology 80(5): 1703-1712. https://doi.org/10.1890/0012-9658(1999)080[1703:NRBBRT]2.0.CO;2 DOI: https://doi.org/10.1890/0012-9658(1999)080[1703:NRBBRT]2.0.CO;2
Karron JD, Mitchell RJ, Bell JM (2006) Multiple pollinator visits to Mimulus ringens (Phrymaceae) flowers increase mate number and seed set within fruits. American Journal of Botany 93(9): 1306-1312. https://doi.org/10.3732/ajb.93.9.1306 DOI: https://doi.org/10.3732/ajb.93.9.1306
Kawai Y, Kudo G (2009) Effectiveness of buzz pollination in Pedicularis chamissonis: Significance of multiple visits by bumblebees. Ecological Research 24(1): 215-223. https://doi.org/10.1007/s11284-008-0500-6 DOI: https://doi.org/10.1007/s11284-008-0500-6
Kearns CA, Inouye DW (1993) Techniques for Pollination Biologists. University Press of Colorado, Colorado.
Kershen DL, McHughen A (2005) Adventitious Presence: Inadvertent commingling and coexistence among farming methods. Council for Agricultural Science and Technology (CAST) Commentary QTA 2005; CAST, Ames, Iowa.
Klein AM, Steffan-Dewenter I, Tscharntke T (2003) Fruit set of highland coffee increases with the diversity of pollinating bees. Proceedings of the Royal Society B 270: 955-961. https://doi.org/10.1098/rspb.2002.2306 DOI: https://doi.org/10.1098/rspb.2002.2306
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(9): e0182522. https://doi.org/10.1371/journal.pone.0182522 DOI: https://doi.org/10.1371/journal.pone.0182522
Lang GA, Danka RG (1991) Honey-bee-mediated cross- versus self-pollination of ‘Sharpblue’ blueberry increases fruit size and hastens ripening. Journal of the American Society for Horticultural Science 116(5): 770-773. https://doi.org/10.21273/JASHS.116.5.770 DOI: https://doi.org/10.21273/JASHS.116.5.770
Larkin RA, Graumann HO (1954) Anatomical structure of the alfalfa flower and an explanation of the tripping mechanism. Botanical Gazette 116(1): 40-52. https://doi.org/10.1086/335845 DOI: https://doi.org/10.1086/335845
Lehman WF, Puri YP, Garber MJ (1969) Effect of environment on quality characteristics of alfalfa (Medicago sativa L.) pollen. Crop Science 9: 560-563. https://doi.org/10.2135/cropsci1969.0011183X000900050012x DOI: https://doi.org/10.2135/cropsci1969.0011183X000900050012x
Lin L (1967) A study of factors affecting the germination of alfalfa and safflower pollen. M.S. thesis, Utah State University. https://doi.org/10.26076/c5d5-130b
Luna VS, Figueroa MJ, Baltazar MB, Gomez LR, Townsend R, Schoper JB (2001) Maize pollen longevity and distance isolation requirements for effective pollen control. Crop Science 41(5): 1551-1557. https://doi.org/10.2135/cropsci2001.4151551x DOI: https://doi.org/10.2135/cropsci2001.4151551x
Marden JH (1984) Remote perception of floral nectar by bumblebees. Oecologia 64: 232-240. https://doi.org/10.1007/BF00376876 DOI: https://doi.org/10.1007/BF00376876
McGregor SE (1976) Insect pollination of cultivated crop plants. United States Department of Agriculture – Agricultural Research Service. Agriculture Handbook No. 496. https://handle.nal.usda.gov/10113/CAT76674944
Minaar C, Anderson B, de Jager ML, Karron JD (2019) Plant-pollinator interactions along the pathway to paternity. Annals of Botany 123(2): 225-245. https://doi.org/10.1093/aob/mcy167 DOI: https://doi.org/10.1093/aob/mcy167
Nooten SS, Rehan SM (2020) Historical changes in bumble bee body size and range shift of declining species. Biodiversity and Conservation 29: 451-467. https://doi.org/10.1007/s10531-019-01893-7 DOI: https://doi.org/10.1007/s10531-019-01893-7
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120: 321–326. https://doi.org/10.1111/j.1600-0706.2010.18644.x DOI: https://doi.org/10.1111/j.1600-0706.2010.18644.x
Portman ZM, Orr MC, Griswold T (2019) A review and updated classification of pollen gathering behavior in bees (Hymenoptera, Apoidea). Journal of Hymenoptera Research 71: 171-208. https://doi.org/10.3897/jhr.71.32671 DOI: https://doi.org/10.3897/jhr.71.32671
Prasad PVV, Boote KJ, Allen Jr. LH (2011) Longevity and temperature response of pollen as affected by elevated growth temperature and carbon dioxide in peanut and grain sorghum. Environmental and Experimental Botany 70(1): 51-57. https://doi.org/10.1016/j.envexpbot.2010.08.004 DOI: https://doi.org/10.1016/j.envexpbot.2010.08.004
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing.
Rang ZW, Jagadish SVK, Zhou QM, Craufurd PQ, Heuer S (2011) Effect of high temperature and water stress on pollen germination and spikelet fertility in rice. Environmental and Experimental Botany 70(1): 58-65. https://doi.org/10.1016/j.envexpbot.2010.08.009 DOI: https://doi.org/10.1016/j.envexpbot.2010.08.009
Rasheed S, Harder L (2003) Economic motivation for plant species preferences of pollen-collecting bumble bees. Ecological Entomology 22(2): 209-219. https://doi.org/10.1046/j.1365-2311.1997.t01-1-00059.x DOI: https://doi.org/10.1046/j.1365-2311.1997.t01-1-00059.x
Ratto F, Simmons BI, Spake R, Zamora-Gutierrez V, MacDonald MA, Merriman JC, Tremlett CJ, Poppy GM, Peh KS-H, Dicks LV (2018) Global importance of vertebrate pollinators for plant reproductive success: a meta-analysis. Frontiers in Ecology and the Environment. 16(2): 82-90. https://doi.org/10.1002/fee.1763 DOI: https://doi.org/10.1002/fee.1763
Richards SA, Williams NM, Harder LD (2009) Variation in pollination: Causes and consequences for plant reproduction. American Naturalist 174(3): 382-398. https://doi.org/10.1086/603626 DOI: https://doi.org/10.1086/603626
Santa-Martinez E, Cardoso Castro C, Flick A, Sullivan M, Riday H, Clayton MK, Brunet J (2021) Bee species visiting Medicago sativa differ in pollen deposition curves with consequences for gene flow. American Journal of Botany 108(6): 1016-1028. https://doi.org/10.1002/ajb2.1683 DOI: https://doi.org/10.1002/ajb2.1683
SAS Institute (2016). Statistical Analysis Software (SAS) User’s Guide Version 9.4. Cary, NC: SAS Institute, Inc. https://www.sas.com/en_us/home.html
Slatkin M (1987) Gene flow and the geographic structure of plant populations. Science 236(4803): 787-792. https://www.jstor.org/stable/1699930 DOI: https://doi.org/10.1126/science.3576198
Snow AA, Roubik DW (1987) Pollen deposition and removal by bees visiting two tree species in Panama. Biotropica 19(1): 57-63. https://doi.org/10.2307/2388460 DOI: https://doi.org/10.2307/2388460
Stavert JR, Bailey C, Kirkland L, Rader R (2020) Pollen tube growth from multiple pollinator visits more accurately quantifies pollinator performance and plant reproduction. Scientific Reports 10: 16958. https://doi.org/10.1038/s41598-020-73637-5 DOI: https://doi.org/10.1038/s41598-020-73637-5
Thomson DM (2019) Effects of long-term variation in pollinator abundance and diversity on reproduction of a generalist plant. Journal of Ecology 107: 491-502. https://doi.org/10.1111/1365-2745.13055 DOI: https://doi.org/10.1111/1365-2745.13055
Thomson JD (1986) Pollen transport and deposition by bumble bees in Erythronium: Influences of floral nectar and bee grooming. Journal of Ecology 74(2): 329-341. https://doi.org/10.2307/2260258 DOI: https://doi.org/10.2307/2260258
Thomson JD, Goodell K (2001) Pollen removal and deposition by honeybee and bumblebee visitors to apple and almond flowers. Journal of Applied Ecology 38(5): 1032-1044. https://doi.org/10.1046/j.1365-2664.2001.00657.x DOI: https://doi.org/10.1046/j.1365-2664.2001.00657.x
Thomson JD, Plowright RC (1980) Pollen carryover, nectar rewards, and pollinator behavior with special reference to Diervilla lonicera. Oecologia 46: 68-74. https://doi.org/10.1007/BF00346968 DOI: https://doi.org/10.1007/BF00346968
Thomson JD, Price MV, Waser NM, Stratton DA (1986) Comparative studies of pollen and fluorescent dye transport by bumble bees visiting Erythronium grandiflorum. Oecologia 69(4): 561-566. https://doi.org/10.1007/BF00410363 DOI: https://doi.org/10.1007/BF00410363
Tondini F, Tavoletti S, Mariani A, Veronesi F (1993) A statistical approach to estimate the frequency of n, 2n and 4n pollen grains in diploid alfalfa. Euphytica 69: 109-114. https://doi.org/10.1007/BF00021733 DOI: https://doi.org/10.1007/BF00021733
Tong Z-Y, Huang S-Q (2018) Safe sites of pollen placement: A conflict of interest between plants and bees? Oecologia 186: 163-171. https://doi.org/10.1007/s00442-017-3999-9 DOI: https://doi.org/10.1007/s00442-017-3999-9
Wang Z-Y, Ge Y, Scott M, Spangenberg G (2004) Viability and longevity of pollen from transgenic and nontransgenic tall fescue (Festuca arundinacea) (Poaceae) plants. American Journal of Botany 91(4): 523-530. https://doi.org/10.3732/ajb.91.4.523 DOI: https://doi.org/10.3732/ajb.91.4.523
Waser NM (1988) Comparative pollen and dye transfer by pollinators of Delphinium nelsonii. Functional Ecology 2(1): 41-48. https://doi.org/10.2307/2389458 DOI: https://doi.org/10.2307/2389458
Wilson P, Thomson JD (1991) Heterogeneity among floral visitors leads to discordance between removal and deposition of pollen. Ecology 72: 1503-1507. https://doi.org/10.2307/1941124 DOI: https://doi.org/10.2307/1941124
Young HJ, Dunning DW, von Hasseln KW (2007) Foraging behavior affects pollen removal and deposition in Impatiens capensis (Balsaminaceae). American Journal of Botany 94: 1267-1271. https://doi.org/10.3732/ajb.94.7.1267 DOI: https://doi.org/10.3732/ajb.94.7.1267
Downloads
Additional Files
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Molly Dieterich Mabin , Connor Slawin, Amy-Mei Lynch, Fabiana Fragoso , Johanne Brunet
This work is licensed under a Creative Commons Attribution 4.0 International License.
JPE is an open access journal which means that all content is freely available without charge to the user or his/her institution.
Authors who publish with this journal agree to the following terms:
1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
To assure a broader targeted audience, content will be included into databases (such as EBSCO) and directories (such as DOAJ).
