Male flowers of Aconitum compensate for toxic pollen with increased floral signals and rewards for pollinators

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Pollinators; Alkaloids; Aconitum napellus; Toxic pollen

Abstract :

[en] Many plants require animal pollinators for successful reproduction; these plants provide pollinator resources in pollen and nectar (rewards) and attract pollinators by specific cues (signals). In a seeming contradiction, some plants produce toxins such as alkaloids in their pollen and nectar, protecting their resources from ineffective pollinators. We investigated signals and rewards in the toxic, protandrous bee-pollinated plant Aconitum napellus, hypothesizing that male-phase flower reproductive success is pollinator-limited, which should favour higher levels of signals (odours) and rewards (nectar and pollen) compared with female-phase flowers. Furthermore, we expected insect visitors to forage only for nectar, due to the toxicity of pollen. We demonstrated that male-phase flowers emitted more volatile molecules and produced higher volumes of nectar than female-phase flowers. Alkaloids in pollen functioned as chemical defences, and were more diverse and more concentrated compared to the alkaloids in nectar. Visitors actively collected little pollen for larval food but consumed more of the lesstoxic nectar. Toxic pollen remaining on the bee bodies promoted pollen transfer efficiency, facilitating pollination.

Disciplines :

Phytobiology (plant sciences, forestry, mycology...)
Chemistry

Author, co-author :

Jacquemart, Anne-Laure; Université Catholique de Louvain - UCL > Earth and Life Institute- Agronomy

Buyens, C.; Université Catholique de Louvain - UCL > Earth and Life Institute- Agronomy

Hérent, M.-F.; Université Catholique de Louvain - UCL > Louvain Drug Research Institute

Quetin-Leclercq, Joëlle ; Université Catholique de Louvain - UCL > Louvain Drug Research Institute

Lognay, Georges ; Université de Liège - ULiège - GxABT > Chimie Analytique

Hance, Thierry; Université Catholique de Louvain - UCL > Earth and Life Institute – Biodiversity

Quinet, M.; Université Catholique de Louvain - UCL > Earth and Life Institute- Agronomy

Language :

English

Title :

Male flowers of Aconitum compensate for toxic pollen with increased floral signals and rewards for pollinators

Publication date :

2019

Journal title :

Scientific Reports

eISSN :

2045-2322

Publisher :

Nature Publishing Group, London, United Kingdom

Volume :

Pages :

art. 16498

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://www.nature.com/articles/s41598-019-53355-3

Available on ORBi :

since 12 October 2020

Statistics

Number of views

71 (2 by ULiège)

Number of downloads

46 (2 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Bronstein, J. L. The exploitation of mutualisms. Ecol. Lett. 4, 277–287 (2001).
Barrett, S. C. H. & Harder, L. D. The ecology of mating and its evolutionary consequences in seed plants. Annu. Rev. Ecol. Evol. Syst. 48, 135–157 (2017).
Goulson, D. Bumblebees: Behaviour, Ecology and Conservation (Oxford University Press, 2009).
Gosselin, M. et al. Does Aconitum septentrionale chemically protect floral rewards to the advantage of specialist bumblebees? Ecol. Entomol. 38, 400–407 (2013).
Arnold, S. E. J., Idrovo, P., Lomas Arias, L. J., Belmain, S. R. & Stevenson, P. C. Herbivore defence compounds occur in pollen and reduce bumblebee colony fitness. J. Chem. Ecol. 40, 878–881 (2014).
Baracchi, D., Marples, A., Jenkins, A. J., Leitch, A. R. & Chittka, L. Nicotine in floral nectar pharmacologically influences bumblebee learning of floral features. Sci. Rep. 7, 1951 (2017).
Jacquemart, A.-L. et al. Tilia trees: toxic or valuable resources for pollinators? Apidologie 49, 538–550 (2018).
Barlow, S. E. et al. Distasteful nectar deters floral robbery. Curr. Biol. 27, 2552–2558 (2017).
Mayer, C. et al. Nectar robbing improves male reproductive success of the endangered Aconitum napellus ssp. lusitanicum. Evol. Ecol. 28, 669–685 (2014).
Whittall, J. B. & Hodges, S. A. Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447, 706–710 (2007).
Heinrich, B. Resource partitioning among some eusocial insects: bumblebees. Ecology 57, 874–889 (1976).
Bosch, M., Simon, J., Blanché, C. & Molero, J. Pollination ecology in tribe Delphineae (Ranunculaceae) in W Mediterranean area: floral visitors and pollinator behaviour. Lagascalia 19, 545–562 (1997).
Minnaar, C., Anderson, B., de Jager, M. L. & Karron, J. D. Plant–pollinator interactions along the pathway to paternity. Ann. Bot. 123, 225–245 (2019).
Zhao, Z. G., Lu, N. N. & Conner, J. K. Adaptive pattern of nectar volume within inflorescences: bumblebee foraging behavior and pollinator-mediated natural selection. Sci. Rep. 6, 34499 (2016).
Carlson, J. & Harms, K. The evolution of gender-biased nectar production in hermaphroditic plants. Bot. Rev. 72, 179–205 (2006).
Antoń, S. & Denisow, B. Nectar production and carbohydrate composition across floral sexual phases: contrasting patterns in two protandrous Aconitum species (Dephinieae, Ranunculaceae). Flora 209, 464–470 (2014).
Bell, G., Lefebvre, L., Giraldeau, L.-A. & Weary, D. Partial preference of insects for the male flowers of an annual herb. Oecologia 64, 287–294 (1984).
Ashman, T. L. Sniffing out patterns of sexual dimorphism in floral scent. Funct. Ecol. 23, 852–862 (2009).
Waelti, M. O., Page, P. A., Widmer, A. & Schiestl, F. How to be an attractive male: floral dimorphism and attractiveness to pollinators in a dioecious plant. BMC Evol. Biol. 9, 190 (2009).
Antoń, S., Denisow, B., Komoń-Janczara, E. & Targoński, Z. Nectary and gender-biased nectar production in dichogamous Chamaenerion angustifolium (L.) Scop. (Onagraceae). Plant Species Biol. 32, 380–391 (2017).
Ashman, T. L., Bradburn, M., Cole, D. H., Blaney, B. H. & Raguso, R. A. The scent of a male: the role of floral volatiles in pollination of a gender dimorphic plant. Ecology 86, 2099–2105 (2005).
Lu, N. N., Li, X. H., Li, L. & Zhao, Z. G. Variation of nectar production in relation to plant characteristics in protandrous Aconitum gymnandrum. J. Plant Ecol. 6, 122–129 (2015).
Zhao, Z.-G., Meng, J.-L., Fan, B.-L. & Du, G.-Z. Reproductive patterns within racemes in protandrous Aconitum gymnandrum (Ranunculaceae): potential mechanism and among-family variation. Plant Syst. Evol. 273, 247 (2008).
Liao, W.-J. et al. Female reproductive success decreases with display size in monkshood, Aconitum kusnezoffii (Ranunculaceae). Ann. Bot. 104, 1405–1412 (2009).
Sowig, P. Effects of flowering plant’s patch size on species composition of pollinator communities, foraging strategies, and resource partitioning in bumblebees (Hymenoptera: Apidae). Oecologia 78, 550–558 (1989).
Ameri, A. The effects of Aconitum alkaloids on the central nervous system. Prog. Neurobiol. 56, 211–235 (1998).
Kiss, T. et al. Identification of diterpene alkaloids from Aconitum napellus subsp. firmum & GIRK channel activities of some Aconitum alkaloids. Fitoterapia 90, 85–93 (2013).
Dobson, H. E. M., Danielson, E. M. & Wesep, I. D. V. Pollen odor chemicals as modulators of bumble bee foraging on Rosa rugosa Thunb. (Rosaceae). Plant Species Biol. 14, 153–166 (1999).
Byers, K. J. R. P., Bradshaw, H. D. & Riffell, J. A. Three floral volatiles contribute to differential pollinator attraction in monkeyflowers (Mimulus). J. Exp. Biol. 217, 614–623 (2014).
Muhlemann, J. K., Klempien, A. & Dudareva, N. Floral volatiles: from biosynthesis to function. Plant Cell Environ. 37, 1936–1949 (2014).
Wang, T. N. et al. Scent matters: differential contribution of scent to insect response in flowers with insect vs. wind pollination traits. Ann. Bot. 123, 289–301 (2019).
Knudsen, J. T., Eriksson, R., Gershenzon, J. & Ståhl, B. Diversity and distribution of floral scent. Bot. Rev. 72, 1–120 (2006).
Griffin, A. M. & Byers, D. L. Pollinator behavior differs between female and hermaphroditic plants of Lobelia spicata Lam. (Campanulaceae). J. Torrey Bot. Soc. 139, 131–136 (2012).
Massart, A. Les différences d’attraction entre les stades floraux chez Aconitum napellus subsp. lusitanicum. Master thesis dissertation. UCLouvain, 70 pp. (2019).
Nakamura, S. & Kudo, G. Foraging responses of bumble bees to rewardless floral patches: importance of within-plant variance in nectar presentation. AoB Plants 8, plw037 (2016).
Pyke, G. H. Optimal foraging movement patterns of bumblebees between inflorescences. Theor. Popul. Biol. 13, 72–98 (1978).
Cruden, R. W., Hermann, S. M. & Peterson, S. Patterns of nectar production and plant-pollinator coevolution. In The Biology of Nectaries, (eds Bentley, B. & Elias, T.), pp. 80–125 (1983).
Varga, S., Nuortila, C. & Kytöviita, M. M. Nectar sugar production across floral phases in the gynodioecious protandrous plant Geranium sylvaticum. Plos One 8, e62575 (2013).
Parachnowitsch, A. L., Manson, J. S. & Sletvold, N. Evolutionary ecology of nectar. Ann. Bot. 123, 247–261 (2019).
Harder, L. D. & Wilson, W. G. A clarification of pollen discounting and its joint effects with inbreeding depression on mating system evolution. Am. Nat. 152, 684–695 (1998).
Jordan, C. Y., Natta, M. & Harder, L. D. Flower orientation influences the consistency of bumblebee movement within inflorescences. Ann. Bot. 118, 523–527 (2016).
Wang, Z., Wen, J., Xing, J. & He, Y. Quantitative determination of diterpenoid alkaloids in four species of Aconitum by HPLC. J. Pharm. Biomed. Anal. 40, 1031–1034 (2006).
Irwin, R. E., Cook, D., Richardson, L. L., Manson, J. S. & Gardner, D. R. Secondary compounds in floral rewards of toxic rangeland plants: impacts on pollinators. J. Agric. Food Chem. 62, 7335–7344 (2014).
Detzel, A. & Wink, M. Attraction, deterrence or intoxication of bees (Apis mellifera) by plant allochemicals. Chemoecology 4, 8–18 (1993).
Ruedenauer, F. A., Spaethe, J. & Leonhardt, S. D. How to know which food is good for you: bumblebees use taste to discriminate between different concentrations of food differing in nutrient content. J. Exp. Biol. 218, 2233–2240 (2015).
Tiedeken, E. J., Stout, J. C., Stevenson, P. C. & Wright, G. A. Bumblebees are not deterred by ecologically relevant concentrations of nectar toxins. J. Exp. Biol. 217, 1620–1625 (2014).
Ruedenauer, F. A., Wöhrle, C., Spaethe, J. & Leonhardt, S. D. Do honeybees (Apis mellifera) differentiate between different pollen types? Plos One 13, e0205821 (2018).
Cook, D., Manson, J. S., Gardner, D. R., Welch, K. D. & Irwin, R. E. Norditerpene alkaloid concentrations in tissues and floral rewards of larkspurs and impacts on pollinators. Biochem. Syst. Ecol. 48, 123–131 (2013).
Nicholls, E. & Ibarra, N. H. Assessment of pollen rewards by foraging bees. Funct. Ecol. 31, 76–87 (2017).
Muth, F., Francis, J. S. & Leonard, A. S. Bees use the taste of pollen to determine which flowers to visit. Biol. Lett. 12, 20160356 (2016).
Praz, C., Müller, A. & Dorn, S. Specialized bees fail to develop on non-host pollen: do plants chemically protect their pollen? Ecology 89, 795–804 (2008).
Wang, X. Y., Tang, J., Wu, T., Wu, D. & Huang, S. Q. Bumblebee rejection of toxic pollen facilitates pollen transfer. Curr. Biol. 29, 1401–1406 (2019).
Moquet, L., Bruyère, L., Pirard, B. & Jacquemart, A.-L. Nectar foragers contribute to the pollination of buzz-pollinated plant species. Am. J. Bot. 104, 1451–1463 (2017).
Ma, C., Kessler, S., Simpson, A. & Wright, G. A novel behavioral assay to investigate gustatory responses of individual, freely-moving bumble bees (Bombus terrestris). J.Visual. Exp. 113, e54233 (2016).