Floral nectar and insect flower handling time change over the flowering season: Results from an exploratory study

Amino acids; Biogenic amines; Echium vulgare; Neuroactive nectar; Octopamine; Pollinators; Ecology, Evolution, Behavior and Systematics; Nature and Landscape Conservation

Abstract :

[en] In recent decades, hundreds of secondary metabolites have been found in floral nectar and many studies have demonstrated that they can play various roles in modulating the behaviour of floral visitors. However, temporal variations in nectar chemistry over extended flowering seasons have never been substantiated. Moreover, the effects of nectar chemicals on insect behaviour are often studied under laboratory conditions, focusing on few insect species under artificial conditions which may influence insect responses. The aim of this exploratory study was to compare nectar chemistry and the durations of pollinator visits in the early and late summer periods of the long-flowering species Echium vulgare L. in natural populations. Nectar samples were collected in the early and late summer periods and insects were observed for a total of 480 min. The biogenic amine octopamine, sugars and the protein to non-protein amino acid ratio increased as the season proceeded. It remains to clarify whether these changes are determined by biotic and abiotic factors or whether the plant expresses some chemical constraint, however it seems likely that changes in nectar chemistry may be the cause of the longer visits by bumblebees to single flowers at the end of the flowering season. Though not conclusive, these results set a baseline for future research and highlight an interesting question. Since long-flowering plants see changing contexts during their bloom period, do they express chemical constraints to regulate their attractiveness?

Disciplines :

Environmental sciences & ecology

Author, co-author :

Barberis, M. ; Dipartimento di Scienze Biologiche, Geologiche e Ambientali, Università di Bologna, Bologna, Italy

Bogo, G. ; Grupo de Ecología de la Polinización, INIBIOMA, Universidad Nacional del Comahue-CONICET, Bariloche, Argentina ; Consiglio per la ricerca in agricoltura e l'analisi dell'economia agraria, Centro di ricerca agricoltura e ambiente (CREA-AA), Bologna, Italy

Bortolotti, L. ; Consiglio per la ricerca in agricoltura e l'analisi dell'economia agraria, Centro di ricerca agricoltura e ambiente (CREA-AA), Bologna, Italy

Flaminio, Simone ; Université de Mons - UMONS > Faculté des Sciences > Service de Zoologie ; Consiglio per la ricerca in agricoltura e l'analisi dell'economia agraria, Centro di ricerca agricoltura e ambiente (CREA-AA), Bologna, Italy

Giordano, E. ; Dipartimento di Scienze della Vita, Università di Siena, Siena, Italy

Nepi, M. ; Dipartimento di Scienze della Vita, Università di Siena, Siena, Italy ; National Biodiversity Future Center (NBFC), Italy

Galloni, M. ; Dipartimento di Scienze Biologiche, Geologiche e Ambientali, Università di Bologna, Bologna, Italy

Language :

English

Title :

Floral nectar and insect flower handling time change over the flowering season: Results from an exploratory study

Publication date :

October 2023

Journal title :

Acta Oecologica

ISSN :

1146-609X

eISSN :

1873-6238

Publisher :

Elsevier B.V.

Volume :

120

Pages :

103937

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://api.elsevier.com/content/article/PII:S1146609X23000498?httpAccept=text/xml

Research unit :

S869 - Zoologie

Research institute :

R100 - Institut des Biosciences

Funders :

Università di Bologna

Funding text :

We thank the anonymous reviewers for their useful suggestions, Fedele Greco, Nicolò Brunelli, Massimo Guarnieri and Michela Boi for their precious help. We are grateful to Lucia Conte for her support during late flowering season field surveys. Marta Barberis was supported by a PhD grant from the University of Bologna .

Available on ORBi UMONS :

since 20 September 2023

Statistics

Number of views

7 (0 by UMONS)

Number of downloads

13 (0 by UMONS)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Adler, L.S., Irwin, R.E., McArt, S.H., Vannette, R.L., Floral traits affecting the transmission of beneficial and pathogenic pollinator-associated microbes. Curr. Opin. Insect Sci. 4 (2021), 1–7, 10.1016/j.cois.2020.08.006.
Arnold, E.J.S., Dudenhoffer, J.-H., Fountain, M.T., James, K.L., Hall, D.R., Farman, D.I., Wackers, F.L., Stevenson, P.C., Bumble bees show an induced preference for flowers when primed with caffeinated nectar and a target floral odor. Curr. Biol. 31:18 (2021), 4127–4131, 10.1016/j.cub.2021.06.068.
Ayestaran, A., Giurfa, M., de Brito Sanchez, M.G., Toxic but drank: gustatory aversive compounds induce post-ingestional malaise in harnessed honeybees. Chapouthier, G., (eds.) PLoS ONE, vol. 5, 2010, e15000, 10.1371/journal.pone.0015000.
Baker, H.G., Baker, I., A brief historical review of the chemistry of floral nectar. Bentley, B., Elias, T., (eds.) The Biology of Nectarines, 1983, Columbia University Press, New York, 126–152.
Baker, H.G., Baker, I., The occurrence and significance of amino acids in floral nectars. Plant Systemat. Evol. 151 (1986), 175–186, 10.1007/BF02430273.
Barberis, M., Bogo, G., Bortolotti, L., Alessandrini, M., Conte, L., Nepi, M., Galloni, M., Gender-biased nectar targets different behavioural traits of flower visitors. Plant Ecol. 222 (2021), 233–246, 10.1007/s11258-020-01101-5.
Barberis, M., Bogo, G., Bortolotti, L., Guarnieri, M., Nepi, M., Felicioli, A., Galloni, M., Nectar tyramine decreases the duration of bumblebee visits on flowers. Arthropod Plant Interact, 2023, 10.1007/s11829-023-09976-7.
Barron, A.B., Maleszka, R., Vander Meer, R.K., Robinson, G.E., Octopamine modulates honey bee dance behavior. Proc. Natl. Acad. Sci. USA 104:5 (2007), 1703–1707, 10.1073/pnas.0610506104.
Bates, D., Machler, M., Fitting linear mixed-effects models using lme4. J. Stat. Software 67:1 (2015), 1–48, 10.18637/jss.v067.i01.
Blenau, W., Baumann, A., Molecular and pharmacological properties of insect biogenic amine receptors: lessons from Drosophila melanogaster and Apis mellifera. Arch. Insect Biochem. Physiol. 48 (2001), 13–38.
Boege, K., Marquis, R.J., Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol. Evol. 20:8 (2005), 441–448, 10.1016/j.tree.2005.05.001.
Bogo, G., Bortolotti, L., Sagona, S., Felicioli, A., Galloni, M., Barberis, M., Nepi, M., Effects of non protein amino acids in nectar on bee survival and behaviour. J. Chem. Ecol. 45 (2019), 278–285, 10.1007/s10886-018-01044-2.
Bogo, G., Fisogni, A., Rabassa-Juvanteny, J., Bortolotti, L., Nepi, M., Guarnieri, M., Conte, L., Galloni, M., Nectar chemistry is not only a plant's affair: floral visitors affect nectar sugar and amino acid composition. Oikos 00 (2021), 1–13, 10.1111/oik.08176.
Borrell, B.J., Effects of nectar concentration and flower depth on flower handling efficiency of bumble bees. Oecologia 69 (1986), 309–315, 10.1007/BF00377639.
Carlesso, D., Smargiassi, S., Pasquini, E., Bertelle, G., Baracchi, D., Nectar non-protein amino acids do not change nectar palatability but enhance learning and memory in honey bees. Sci. Rep., 11, 2021, 11721, 10.1038/s41598-021-90895-z.
Carlson, J., Harms, K.E., The evolution of gender-biased nectar production in hermaphrodite plants. Bot. Rev. 72 (2006), 179–205, 10.1663/0006-8101(2006)72[179:TEOGNP]2.0.CO;2.
Cohen, S.A., Micheaud, D.P., Synthesis of a fluorescent derivatizing reagent, 6-aminoquinolyl-N-hydroxysuccinimidyl carbamate, and its application for the analysis of hydrolysate amino acids via High Performance Liquid Chromatography. Anal. Biochem. 211 (1993), 279–287, 10.1006/abio.1993.1270.
Corbet, S.A., Bee visits and the nectar of Echium vulgare L. and Sinapis alba L. Ecol. Entomol. 3 (1978), 25–37, 10.1111/j.1365-2311.1978.tb00900.x.
Danforth, B.N., Minckley, R.L., Neff, J.L., Fawcett, F., The Solitary Bees: Biology, Evolution, Conservation. 2019, Princeton University Press, Princeton, Oxford, 10.2307/j.ctvd1c929.
Faegri, K., van der Pijl, L., The Principles of Pollination Ecology. 1979, Pergamon Press, Oxford, England.
Farooqui, T., Review of octopamine in insect nervous systems. Open Access Insect Physiol. 4 (2012), 1–17, 10.2147/OAIP.S20911.
Felicioli, A., Sagona, S., Galloni, M., Bortolotti, L., Bogo, G., Guarnieri, M., Nepi, M., Effects of non-protein amino acids on survival and locomotion of Osmia bicornis. Insect Mol. Biol., 2018, 10.1111/imb.12496.
Finetti, L., Roeder, T., Calò, G., Bernacchia, G., The insect type 1 receptors: from structure to behavior. Insects, 12, 2021, 315, 10.3390/insects12040315.
Fisogni, A., Rossi, M., Sgolastra, F., Bortolotti, L., Bogo, G., de Manincor, N., Quaranta, M., Galloni, M., Seasonal and annual variations in the pollination efficiency of a pollinator community of Dictamnus albus L. Plant Biol. 18 (2016), 445–454, 10.1111/plb.12417.
Galetto, L., Araujo, F.P., Grilli, G., Amarilla, L.D., Torres, C., Sazima, M., Flower trade-offs derived from nectar investment in female reproduction of two Nicotiana species. Solanaceae) 32:3 (2018), 473–478, 10.1590/0102-33062018abb0121.
Good, A.P., Gauthier, M.-P.L., Vannette, R.L., Fukami, T., Honey bees avoid nectar colonized by three bacterial species, but not by a yeast species, isolated from the bee gut. PLoS One, 9, 2014, e86494, 10.1371/journal.pone.0086494.
Harder, D.H., Effects of nectar concentration and flower depth on flower handling efficiency of bumble bees. Oecologia 69 (1986), 309–315, 10.1007/BF00377639.
Harris, R.C., Tallon, M.J., Dunnett, M., Boobis, L., Coakley, J., Kim, H.J., Fallowfield, J.L., Hill, C.A., Sale, C., Wise, J.A., The absorption of orally supplied beta-alanine and its effect on muscle carnosine synthesis in human vastus lateralis. Amino Acids 30 (2006), 279–289, 10.1007/s00726-006-0299-9.
Klinkhamer, P.G.L., de Jong, T.J., Effects of plant size, plant density and sex differential nectar reward on pollinator visitation in the protandrous Echium vulgare. Oikos 57 (1990), 399–405, 10.2307/3565970.
Lanza, J., Smith, G.C., Sack, S., Cash, A., Variation in nectar volume and composition of Impatiens capensis at the individual, plant, and population levels. Oecologia 102 (1995), 113–119, 10.1007/BF00333318.
Lucchetti, M.A., Pyrrolizidine Alkaloids: Occurrence in Bee Products and Impact on Honeybees (Apis mellifera L.)., 2017, Faculty of Science, Institute of Biology, University of Neuchâtel PhD Dissertation.
Lucchetti, M.A., Glauser, G., Kilchenmann, V., Dübecke, A., Beckh, G., Praz, C., Kast, C., Pyrrolizidine alkaloids from Echium vulgare in honey originate primarily from floral nectar. J. Agric. Food Chem. 64 (2016), 5267–5273, 10.1021/acs.jafc.6b02320.
Melser, C., Rademaker, M., Klinkhamer, P.G.L., Selection on pollen donors by Echium vulgare (Boraginaceae). Sex. Plant Reprod. 10 (1997), 305–312, 10.1007/s004970050103.
Mujagic, S., Erber, J., Sucrose acceptance, discrimination and proboscis responses of honey bees (Apis mellifera L.) in the field and the laboratory. J. Comp. Physiol. 195 (2009), 325–339, 10.1007/s00359-008-0409-0.
Mustard, J.A., Neuroactive nectar: compounds in nectar that interact with neurons. Arthropod-Plant Interact. 14 (2020), 151–159, 10.1007/s11829-020-09743-y.
Muth, F., Cooper, T.R., Bonilla, R.F., Leonard, A.S., A novel protocol for studying bee cognition in the wild. Methods Ecol. Evol. 9 (2020), 78–87, 10.1111/2041-210X.12852.
Muth, F., Philbin, C.S., Jeffrey, C.S., Leonard, A.S., Discovery of octopamine and tyramine in nectar and their effects on bumblebee behaviour. iScience, 2022, 10.1016/j.isci.2022.104765.
Nepi, M., Beyond nectar sweetness: the hidden ecological role of nonprotein amino acids in nectar. J. Ecol. 102 (2014), 108–115, 10.1111/1365-2745.12170.
Nepi, M., New perspectives in nectar evolution and ecology: simple alimentary reward or a complex multiorganism interaction?. Acta Agrobot., 70(1), 2017, 1704, 10.5586/aa.1704.
Nepi, M., Soligo, C., Nocentini, D., Abate, M., Guarnieri, M., Cai, G., Bini, L., Puglia, M., Bianch, L., Pacini, E., Amino acids and protein profile in floral nectar: much more than a simple reward. Flora 207 (2012), 475–481, 10.1016/j.flora.2012.06.002.
Nepi, M., Grasso, D.A., Mancuso, S., Nectar in plant–insect mutualistic relationships: from food reward to partner manipulation. Front. Plant Sci., 9, 2018, 1063, 10.3389/fpls.2018.01063.
Nicholls, M.S., Spatial pattern of ovule maturation in the inflorescence of Echium vulgare: demography, resource allocation and the constraints of architecture. Biol. J. Linn. Soc. 31 (1987), 247–256, 10.1111/j.1095-8312.1987.tb01991.x.
Nocentini, D., Pacini, E., Guarnieri, M., Nepi, M., Flower morphology, nectar traits and pollinators of Cerinthe major (Boraginaceae- Lithospermeae). Flora 207 (2012), 186–196, 10.1016/j.flora.2012.01.004.
Obeso, J.R., The costs of reproduction in plants. New Phytol. 155 (2002), 321–348, 10.1046/j.1469-8137.2002.00477.x.
Ohashi, K., Yahara, T., Behavioural responses of pollinators to variation in floral display size and their influences on the evolution of floral traits. Chittka, L., Thomson, J., (eds.) Cognitive Ecology of Pollination: Animal Behaviour and Floral Evolution, 2001, Cambridge University Press, Cambridge, 274–296.
Ornelas, J.F., Lara, C., Nectar replenishment and pollen receipt interact in their effects on seed production of Penstemon roseus. Oecologia 160 (2009), 675–685, 10.1007/s00442-009-1337-6.
Pappers, S.M., de Jong, T.J., Klinkhamer, P.G.L., Meelis, E., Effects of nectar content on the number of bumblebee approaches and the length of visitation sequences in Echium vulgare (Boraginaceae). Oikos 87 (1999), 580–586, 10.2307/3546822.
Pattrick, J.G., Symington, H.A., Federle, W., Glover, B.J., The mechanics of nectar offloading in the bumblebee Bombus terrestris and implications for optimal concentrations during nectar foraging. J. R. Soc., Interface, 17(162), 2020, 31964267, 10.1098/rsif.2019.0632.
Peng, T., Schroeder, M., Grüter, C., Octopamine increases individual and collective foraging in a neotropical stingless bee. Biol. Lett., 16, 2020, 20200238, 10.1098/rsbl.2020.0238.
Petanidou, T., Van Laere, A.J., Smets, E., Change in floral nectar components from fresh to senescent flowers of Capparis spinosa (Capparidaceae), a nocturnally flowering Mediterranean shrub. Plant Sist. Evol. 199 (1996), 79–92, 10.1007/BF00985919.
Petanidou, T., Van Laere, A., Ellis, W.N., Smets, E., What shapes amino acid and sugar composition in Mediterranean floral nectars?. Oikos 115 (2006), 155–169, 10.1111/j.2006.0030-1299.14487.x.
Pyke, G.H., What does it cost a plant to produce floral nectar?. Nature 350:6313 (1991), 58–59, 10.1038/350058a0.
Pyke, G.H., Floral nectar: pollinator attraction or manipulation? Trends Ecol. Evolution 31:5 (2016), 339–341, 10.1016/j.tree.2016.02.013.
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., R Core Team. Linear and Non-linear Mixed Effects Models. 2020 https://CRAN.R-project.org/package=nlme.
Pozo, M.I., Lievens, B., Jacquemym, H., Impact of microorganisms on nectar chemistry, pollinator attraction and plant fitness. Peck, R.L., (eds.) Nectar: Production, Chemical Composition and Benefits to Animals and Plants, 2014, Nova Science Publishers, New York, USA, 1–40.
Rademaker, M.C.J., De Jong, T.J., Van der Meijden, E., Selfing rates in natural populations of Echium vulgare: a combined empirical and model approach. Funct. Ecol. 13 (1999), 828–837, 10.1046/j.1365-2435.1999.00384.x.
Roeder, T., Octopamine in invertebrates. Prog. Neurobiol. 59 (1999), 533–561, 10.1016/S0301-0082(99)00016-7.
Roeder, T., Tyramine and octopamine: ruling behavior and metabolism. Annu. Rev. Entomol. 50 (2005), 447–477, 10.1146/annurev.ento.50.071803.130404.
Schoonhoven, L.M., van Loon, J.J.A., Dicke, M., Insect-plant Biology. 2005, Oxford University Press, Oxford.
Seo, H.J., Song, J., Yoon, H.J., Lee, K.Y., Effects of nectar contents on the foraging activity of honeybee (Apis mellifera) on Asian pear (Pyrus pyrifolia Nakai). Sci. Hortic. 245 (2019), 185–192, 10.1016/j.scienta.2018.10.009.
Simcock, N.K., Gray, H.E., Wright, G.A., Single amino acids in sucrose rewards modulate feeding and associative learning in the honeybee. J. Insect Physiol. 69 (2014), 41–48, 10.1016/j.jinsphys.2014.05.004.
Tiedge, K., Lohaus, G., Nectar sugars and amino acids in day- and night-flowering Nicotiana species are strongly shaped by pollinators' preferences than organic acids and inorganic ions. PLoS One 12 (2017), 1–25, 10.1371/journal.pone.0176865.
Torres, C., Galetto, L., Patterns and implications of floral nectar secretion, chemical composition, removal effects and standing crops in Mandevilla pentlandiana (Apocynaceae). Bot. J. Linn. Soc. 127 (1998), 207–223, 10.1111/j.1095-8339.1998.tb02098.x.
Vannette, R.L., Gauthier, M.P.L., Fukami, T., Nectar bacteria, but not yeast, weaken a plant–pollinator mutualism. Proc. Royal Soc. B., 280, 2013, e20122601, 10.1098/rspb.2012.2601.
Vannette, R.L., Fukami, T., Contrasting effects of yeasts and bacteria on floral nectar traits. Ann. Bot. 121 (2018), 1343–1349, 10.1093/aob/mcy032.
de Vega, C., Herrera, C.M., Relationships among nectar-dwelling yeasts, flowers and ants: patterns and incidence on nectar traits. Oikos 121 (2012), 1878–1888, 10.1111/j.1600-0706.2012.20295.x.
Venables, W.N., Ripley, B.D., Modern Applied Statistics with S. forth ed., 2002, Springer.
Whitton, P.S., Strang, R.H.C., Nicholson, R.A., The distribution of taurine in the tissues of some species of insects. Insect Biochem. 17 (1987), 573–577, 10.1016/0020-1790(87)90056-4.