The tripping mechanism of flowers affects pollen transfer dynamics

Authors

  • Molly Dieterich Mabin Vegetable Crops Research Unit, USDA Agricultural Research Service Madison, WI https://orcid.org/0000-0001-6545-1927
  • Connor Slawin University of Wisconsin Madison https://orcid.org/0000-0001-8803-3015
  • Amy-Mei Lynch Agricultural Research Service Research Participation Program, Oak Ridge Institute for Science and Education (ORISE), Madison, Wisconsin, USA https://orcid.org/0000-0001-7171-6442
  • Fabiana Fragoso Agricultural Research Service Research Participation Program, Oak Ridge Institute for Science and Education (ORISE), Madison, Wisconsin, USA
  • Johanne Brunet Brunet Research https://orcid.org/0000-0003-4555-7411

DOI:

https://doi.org/10.26786/1920-7603(2023)770

Keywords:

Bumble bee, Flower visits, Pollen deposition, Pollen grains on the bee's body, Medicago sativa, Tripped flowers

Abstract

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.

Author Biographies

Molly Dieterich Mabin , Vegetable Crops Research Unit, USDA Agricultural Research Service Madison, WI

Molly was a research technician in the laboratory of Dr. Johanne Brunet in Madison, Wisconson, when this work was performed.

Connor Slawin, University of Wisconsin Madison

Connor was an undergraduate at the University of Wisconsin-Madison when this research was performed, he was doing an Honors thesis in Dr. Brunet's laboratory.

Amy-Mei Lynch, Agricultural Research Service Research Participation Program, Oak Ridge Institute for Science and Education (ORISE), Madison, Wisconsin, USA

Amy was a trainee with ORISE when this research was performed, in the Brunet laboratory.

Fabiana Fragoso , Agricultural Research Service Research Participation Program, Oak Ridge Institute for Science and Education (ORISE), Madison, Wisconsin, USA

Dr. Fragoso was a postdoctoral traineed with ORISE in the Brunet laboratory when this work was performed.

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

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2024-01-19

How to Cite

Dieterich Mabin , M., Slawin, C., Lynch, A.-M., Fragoso , F., & Brunet, J. (2024). The tripping mechanism of flowers affects pollen transfer dynamics. Journal of Pollination Ecology, 36, 1–13. https://doi.org/10.26786/1920-7603(2023)770

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