Pollenkitt is associated with the collectability of Malvoideae pollen for corbiculate bees

Authors

DOI:

https://doi.org/10.26786/1920-7603(2023)754

Keywords:

Apidae, floral filter, Malvaceae, pollen adhesion, pollen collection, pollenkitt

Abstract

Pollen grains of Malvoideae (Malvaceae) which corbiculate bees cannot collect constitute a floral filter that excludes pollen-collecting bumble bees and honey bees from exploiting pollen resources. Although large, spiny pollen grains are in fact harder to compact for collection by corbiculate bees, pollen morphology (e.g., grain diameter, spine length) is not by itself a reliable indicator of pollen collectability. In this study, we discovered that two Malvoideae species, Anoda cristata and Malope trifida, possess large, spiny pollen grains that can be groomed and collected by corbiculate bees. To gain insight into the underlying cause of collectability of Malvoideae pollen, we tested pollen adhesion to bumble bee setae and found that significantly less of the collectable pollen grains of A. cristata and M. trifida adhere to bees’ setae compared to uncollectable pollen grains of Hibiscus trionum. As the primary mediator of pollen adhesion is pollenkitt, a viscous lipid-rich substance covering pollen of zoophilous plants, we examined the surface of uncollectable and collectable Malvoideae pollen using cryo-SEM. Fresh pollen grains were abundantly covered with pollenkitt that also coated the long spines and formed liquid bridges between the grains. Washing pollen with hexane removed all pollenkitt, whereas washing pollen with water only removed pollenkitt on the collectable pollen grains of M. trifida, but not the uncollectable pollen grains of Hibiscus syriacus. We hypothesise that pollenkitt composition differs between Malvoideae species with uncollectable and collectable pollen. Specific pollenkitt properties might elicit excessive viscidity which affects adhesion to insect visitors but prevents pollen collection by corbiculate bees.

References

Adam NK (1952) The physics and chemistry of surfaces. Oxford University Press, London.

Amador GJ, Matherne M, Waller D, Mathews M, Gorb SN, Hu DL (2017) Honey bee hairs and pollenkitt are essential for pollen capture and removal. Bioinspiration & Biomimetics 12:026015. https://doi.org/10.1088/1748-3190/aa5c6e

Baumann G (2006) Untersuchungen zur Pollenportionierung bei einheimischen Salvia-Arten – Quantifizierung, Biomechanik und Pollenhaftung. Diploma thesis, Botanical Garden of the Albert-Ludwigs-Universität Freiburg, Germany.

Berger LA, Vaissière BE, Moffett JO, Merritt SJ (1988) Bombus spp. (Hymenoptera: Apidae) as pollinators of male-sterile upland cotton on the Texas high plains. Environmental Entomology 17:789-794. https://doi.org/10.1093/ee/17.5.789

Bhat PP, Appathurai S, Harris MT, Pasquali M, McKinley GH, Basaran OA (2010) Formation of beads-on-a-string structures during break-up of viscoelastic filaments. Nature Physics 6:625-631. http://dx.doi.org/10.1038/nphys1682

Brochu KK, van Dyke MT, Milano NJ, Petersen JD, McArt SH, Nault BA, Kessler A, Danforth BN (2020) Pollen defenses negatively impact foraging and fitness in a generalist bee (Bombus impatiens: Apidae). Scientific Reports 10:3112. https://doi.org/10.1038/s41598-020-58274-2

Buchmann SL, Shipman CW (1990) Pollen harvesting rates for Apis mellifera L. on Gossypium (Malvaceae) flowers. Journal of the Kansas Entomological Society 63:92-100. http://www.jstor.org/stable/25085151

Christensen PB (1986) Pollen morphological studies in the Malvaceae. Grana 25:95-117. https://doi.org/10.1080/00173138609428890

Dobson HE (1988) Survey of pollen and pollenkitt lipids - chemical cues to flower visitors? American Journal of Botany 75:170-182. https://doi.org/10.2307/2443884

Erni P, Varagnat M, Clasen C, Cresta J, McKinley GH (2011) Microrheometry of sub-nanolitre biopolymer samples: non-Newtonian flow phenomena of carnivorous plant mucilage. Soft Matter 7:10889-10898. https://doi.org/10.1039/C1SM05815K

Gorenflo A, Diekötter T, van Kleunen M, Wolters V, Jauker F (2017) Contrasting pollination efficiency and effectiveness among flower visitors of Malva sylvestris, Borago officinalis and Onobrychis viciifolia. Journal of Pollination Ecology 21:62-70. https://doi.org/10.26786/1920-7603(2017)421

Harano K, Nakamura J (2016) Nectar loads as fuel for collecting nectar and pollen in honeybees: adjustment by sugar concentration. Journal of Comparative Physiology A 202:435-443. https://doi.org/10.1007/s00359-016-1088-x

Hargreaves AL, Harder LD, Johnson SD (2009) Consumptive emasculation: the ecological and evolutionary consequences of pollen theft. Biological Reviews 84:259-276. https://doi.org/10.1111/j.1469-185X.2008.00074.x

Hasegawa TM, Makino TT, Sakai S (2021) Optimal pollen stickiness to pollinators for maximizing paternal fitness: Increased number of recipient flowers or increased pollen deposition on recipient flowers? Journal of Theoretical Biology 524:110731. https://doi.org/10.1016/j.jtbi.2021.110731

Hensel R, Neinhuis C, Werner C (2016) The springtail cuticle as a blueprint for omniphobic surfaces. Chemical Society Reviews 45:323-341. https://doi.org/10.1039/C5CS00438A

Hesse M (1980) Zur Frage der Anheftung des Pollens an blütenbesuchende Insekten mittels Pollenkitt und Viscinfäden. Plant Systematics and Evolution 133:135-148. https://doi.org/10.1007/BF00984377

Hesse M, Ulrich S (2012) Pollen: stunning diversity and amazing beauty. Biologie in unserer Zeit 42:34-41. https://doi.org/10.1002/biuz.201210468

Ito S, Gorb SN (2019a) Attachment-based mechanisms underlying capture and release of pollen grains. Journal of the Royal Society Interface 16:20190269. https://doi.org/10.1098/rsif.2019.0269

Ito S, Gorb SN (2019b) Fresh “pollen adhesive” weakens humidity-dependent pollen adhesion. Applied Materials & Interfaces 11:24691-24698. https://doi.org/10.1021/acsami.9b04817

Koch K, Bhushan B, Barthlott W (2008) Diversity of structure, morphology and wetting of plant surfaces. Soft Matter 4:1943-1963. https://doi.org/10.1039/B804854A

Konzmann S, Lunau K (2014) Divergent rules for pollen and nectar foraging bumblebees - a laboratory study with artificial flowers offering diluted nectar substitute and pollen surrogate. PLoS ONE 9:e91900. https://doi.org/10.1371/journal.pone.0091900

Konzmann S, Koethe S, Lunau K (2019) Pollen grain morphology is not exclusively responsible for pollen collectability in bumble bees. Scientific Reports 9:4705. https://doi.org/10.1038/s41598-019-41262-6

van der Kooi CJ, Vallejo-Marín M, Leonhardt SD (2021) Mutualisms and (a)symmetry in plant-pollinator interactions. Current Biology 31:R91-R99. https://doi.org/10.1016/j.cub.2020.11.020

Lin H, Gomez I, Meredith JC (2013) Pollenkitt wetting mechanism enables species-specific tunable pollen adhesion. Langmuir 29:3012-3023. https://doi.org/10.1021/la305144z

Lin H, Lizarraga L, Bottomley LA, Meredith JC (2015) Effect of water absorption on pollen adhesion. Journal of Colloid and Interface Science 442:133-139. https://doi.org/10.1016/j.jcis.2014.11.065

Lunau K, Papiorek S, Eltz T, Sazima M (2011) Avoidance of achromatic colours by bees provides a private niche for hummingbirds. Journal of Experimental Biology 214:1607-1612. https://doi.org/10.1242/jeb.052688

Lunau K, Piorek V, Krohn O, Pacini E (2015) Just spines - mechanical defense of malvaceous pollen against collection by corbiculate bees. Apidologie 46:144-149. https://doi.org/10.1007/s13592-014-0310-5

Lynn A, Piotter E, Harrison E, Galen C (2020) Sexual and natural selection on pollen morphology in Taraxacum. American Journal of Botany 107:364-374. https://doi.org/10.1002/ajb2.1428

Mayer G, Oliveira IS, Baer A, Hammel JU, Gallant J, Hochberg R (2015) Capture of prey, feeding, and functional anatomy of the jaws in velvet worms (Onychophora). Integrative and Comparative Biology 55:217-227. https://doi.org/10.1093/icb/icv004

Michener CD (2007) The Bees of the World. The Johns Hopkins University Press, Baltimore.

Michener CD, Winston ML, Jander R (1978) Pollen manipulation and related activities and structures in bees of the family Apidae. University of Kansas Science Bulletin 51:575-601. https://digitalcommons.usu.edu/bee_lab_mi/101

Nicolson SW (2011) Bee food: the chemistry and nutritional value of nectar, pollen and mixtures of the two. African Zoology 46:197-204. https://doi.org/10.3377/004.046.0201

Opell BD, Clouse ME, Andrews SF (2018) Elastic modulus and toughness of orb spider glycoprotein glue. PLoS ONE 13:e0196972. https://doi.org/10.1371/journal.pone.0196972

Pacini E, Hesse M (2005) Pollenkitt – its composition, forms and functions. Flora 200:399-415. https://doi.org/10.1016/j.flora.2005.02.006

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 Interactions 9:197-203. https://doi.org/10.1007/s11829-015-9358-z

Pokorny T, Lunau K, Eltz T (2014) Raising the sugar content - orchid bees overcome the constraints of suction feeding through manipulation of nectar and pollen provisions. PLoS ONE 9:e113823. https://doi.org/10.1371/journal.pone.0113823

Prisle NL, Lin JJ, Purdue S, Lin H, Meredith JC, Nenes A (2019) Cloud condensation nuclei activity of six pollenkitts and the influence of their surface activity. Atmospheric Chemistry and Physics 19:4741-4761. https://doi.org/10.5194/acp-19-4741-2019

R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

Schlindwein C, Pick RA, Martins CF (2009) Evaluation of oligolecty in the Brazilian bee Ptilothrix plumata (Hymenoptera, Apidae, Emphorini). Apidologie 40:106-116. https://doi.org/10.1051/apido/2008067

Shoemaker DN (1911) Notes on vicinism in cotton in 1908. Journal of Heredity 1:252-254. https://doi.org/10.1093/jhered/os-6.1.252

Tepedino VJ, Arneson LC, Durham SL (2016) Pollen removal and deposition by pollen- and nectar-collecting specialist and generalist bee visitors to Iliamna bakeri (Malvaceae). Journal of Pollination Ecology 19:50-56. https://doi.org/10.26786/1920-7603(2016)2

Thorp RW (1979) Structural, behavioral, and physiological adaptations of bees (Apoidea) for collecting pollen. Annals of the Missouri Botanical Garden 66:788-812. https://doi.org/10.2307/2398919

Thorp RW (2000) The collection of pollen by bees. Plant Systematics and Evolution 222:211-223. https://doi.org/10.1007/BF00984103

Vaissière BE, Vinson SB (1994) Pollen morphology and its effect on pollen collection by honey bees, Apis mellifera L. (Hymenoptera: Apidae), with special reference to upland cotton, Gossypium hirsutum L. (Malvaceae). Grana 33:128-138. https://doi.org/10.1080/00173139409428989

Vaknin Y, Gan-Mor S, Bechar A, Ronen B, Eisikowitch D (2000) The role of electrostatic forces in pollination. Plant Systematics and Evolution 222:133-142. https://doi.org/10.1007/BF00984099

Vanderplanck M, Gilles H, Nonclercq D, Duez P, Gerbaux P (2020) Asteraceae paradox: chemical and mechanical protection of Taraxacum pollen. Insects 11:304. https://doi.org/10.3390/insects11050304

Vansell GH (1944) Cotton nectar in relation to bee activity and honey production. Journal of Economic Entomology 37:528-530. https://doi.org/10.1093/jee/37.4.528

Voigt D, Gorb E, Gorb S (2009) Hierarchical organisation of the trap in the protocarnivorous plant Roridula gorgonias (Roridulaceae). Journal of Experimental Biology 212:3184-3191. https://doi.org/10.1242/jeb.034280

Voigt D, Roth-Nebelsick A, Miranda T, Ebner M, Gorb S (2012) Visualization of small water droplets on surfaces with different degree of wettability by using cryo-scanning electron microscopy. Journal of Advanced Microscopy Research 7:64-67. https://doi.org/10.1166/jamr.2012.1091

Wappler T, Labandeira CC, Engel MS, Zetter R, Grímsson F (2015) Specialized and generalized pollen-collection strategies in an ancient bee lineage. Current Biology 25:3092-3098. https://doi.org/10.1016/j.cub.2015.09.021

Bumble bee collecting pink pollen of Malope trifida on its hind legs (above); bumble bee densely covered with pale yellow pollen of Hibiscus syriacus, but unable to collect it (below)

Published

2023-05-23

How to Cite

Konzmann, S., Neunkirchen, M., Voigt, D., Neinhuis, C., & Lunau, K. (2023). Pollenkitt is associated with the collectability of Malvoideae pollen for corbiculate bees. Journal of Pollination Ecology, 33, 128–138. https://doi.org/10.26786/1920-7603(2023)754

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