Abstract
Floral nectar often contains chemicals that are deterrent to pollinators, presenting potential challenges to outcrossing plant species. Plants may be able to co-opt pollinator chemical signals to mitigate the negative effects of nectar deterrent compounds on pollination services. We found that buckwheat (Fagopyrum esculentum) and Mexican sunflower (Tithonia diversifolia) produce nectar with abundant phenolics, including three components of the Apis honeybee queen mandibular pheromone (QMP). In addition, these nectars contain a non-pheromonal phenolic, chlorogenic acid (CA), which was toxic to honeybees, and T. diversifolia nectar also contained isochlorogenic acid (IA). Fresh nectar or solutions containing nectar phenolics reduced Apis individual feeding compared to sucrose solutions. However, freely foraging bees preferred solutions with QMP components to control solutions, and QMP components over-rode or reversed avoidance of CA and IA. Furthermore, prior exposure to the presence or just the odor of QMP components removed the deterrent effects of CA and IA. By mimicking the honey bee pheromone blend, nectar may maintain pollinator attraction in spite of deterrent nectar compounds.




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References
Adler LS (2000) The ecological significance of toxic nectar. Oikos 91:409–420
Adler LS, Irwin RE (2005) Ecological costs and benefits of defenses in nectar. Ecology 86:2968–2978
Adler LS, Seifert MG, Wink M, Morse GE (2012) Reliance on pollinators predicts defensive chemistry across tobacco species. Ecol Lett 15:1140–1148
Beggs KT, Glendining KA, Marechal NM, Vergoz V, Nakamura I, Slessor KN, Mercer AR (2007) Queen pheromone modulates brain dopamine function in worker honey bees. Proc Natl Acad Sci U S A 104:2460–2464
Björkman T (1995) The effectiveness of heterostyly in preventing illegitimate pollination in dish-shaped flowers. Sex Plant Reprod 8:143–146
Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510
Cawoy V, Kinet J-M, Jacquemart A-L (2008) Morphology of nectaries and biology of nectar production in the distylous species Fagopyrum esculentum. Ann Bot 102:675–684
Chaffiol A, Dupuy F, Barrozo RB, Kropf J, Renou M, Rospars J-P, Anton S (2014) Pheromone modulates plant odor responses in the antennal lobe of a moth. Chem Senses 39:451–463
Dötterl S, Vereecken NJ (2010) The chemical ecology and evolution of bee-flower interactions: a review and perspectives. Can J Zool 88:668–697
Elliott SE, Irwin RE, Adler LS, Williams NM (2008) The nectar alkaloid, gelsemine, does not affect offspring performance of a native solitary bee, Osmia lignaria (Megachilidae). Ecol Entomol 33:298–304
Galen C, Kaczorowski R, Todd SL, Geib J, Raguso RA (2011) Dosage-dependent impacts of a floral volatile compound on pollinators, larcenists, and the potential for floral evolution in the alpine skypilot Polemonium viscosum. Am Nat 177:258–272
Hartmann T, Theuring C, Bernays E (2003) Are insect-synthesized retronecine esters (creatonotines) the precursors of the male courtship pheromone in the arctiid moth Estigmene acrea? J Chem Ecol 29:2603–2608
Heil M (2011) Nectar: generation, regulation and ecological functions. Trends Plant Sci 16:191–200
Heil M, Barajas‐Barron A, Orona‐Tamayo D, Wielsch N, Svatos A (2014) Partner manipulation stabilises a horizontally transmitted mutualism. Ecol Lett 17:185–192
Hojo MK, Pierce NE, Tsuji K (2015) Lycaenid caterpillar secretions manipulate attendant ant behavior. Curr Biol 25:2260–2264
Kayode J, Oyeyemi SD (2014) Pollen analysis of Apis mellifera honey collected from Nigeria. Am J Agric Forest 2:226–231
Keeling CI, Otis GW, Hadisoesilo S, Slessor KN (2001) Mandibular gland component analysis in the head extracts of Apis cerana and Apis nigrocincta. Apidologie 32:243–252
Kessler D, Baldwin IT (2007) Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. Plant J 49:840–854
Kessler D, Gase K, Baldwin IT (2008) Field experiments with transformed plants reveal the sense of floral scents. Science 321:1200–1202
Leiss KA, Maltese F, Choi YH, Verpoorte R, Klinkhamer PG (2009) Identification of chlorogenic acid as a resistance factor for thrips in chrysanthemum. Plant Physiol 150:1567–1575
Liang Y, Cao W, Chen W-J, Xiao X-H, Zheng J-B (2009) Simultaneous determination of four phenolic components in citrus honey by high performance liquid chromatography using electrochemical detection. Food Chem 114:1537–1541
Liu F, He J, Fu W (2005) Highly controlled nest homeostasis of honey bees helps deactivate phenolics in nectar. Naturwissenschaften 92:297–299
Mao W, Schuler MA, Berenbaum MR (2015) A dietary phytochemical alters caste-associated gene expression in honey bees. Sci Adv 1:e1500795
Matsuo T, Sugaya S, Yasukawa J, Aigaki T, Fuyama Y (2007) Odorant-binding proteins OBP57d and OBP57e affect taste perception and host-plant preference in Drosophila sechellia. PLoS Biol 5:e118
McArt SH, Koch H, Irwin RE, Adler LS (2014) Arranging the bouquet of disease: floral traits and the transmission of plant and animal pathogens. Ecol Lett 17:624–636
Mukhopadhyay SK, Gupta S, Das AP, Bera S (2007) The beekeeping potential of Sub-Himalayan West Bengal, India: a palynological assessment of honey. J Apic Res 46:165
Ohnishi O (1991) Discovery of the wild ancestor of common buckwheat. Fagopyrum 11:5–10
Plettner E, Otis GW, Wimalaratne PDC, Winston ML, Slessor KN, Pankiw T, Punchihewa PWK (1997) Species-and caste-determined mandibular gland signals in honeybees (Apis). J Chem Ecol 23:363–377
Reddy GV, Guerrero A (2004) Interactions of insect pheromones and plant semiochemicals. Trends Plant Sci 9:253–261
Ruttner F (1988) Biogeography and taxonomy of honeybees. Springer, Berlin
Schiestl FP (2010) The evolution of floral scent and insect chemical communication. Ecol Lett 13:643–656
Schiestl FP, Johnson SD, Raguso RA (2010) Floral evolution as a figment of the imagination of pollinators. Trends Ecol Evol 25:382–383
Schulz S (1998) Insect-plant interactions − metabolism of plant compounds to pheromones and allomones by Lepidoptera and leaf beetles. Eur J Org Chem 1998:13–20
Sharrock R, Sinclair FL, Gliddon C, Rao IM, Barrios E, Mustonen P, Smithson P, Jones D, Godbold D (2004) A global assessment using PCR techniques of mycorrhizal fungal populations colonising Tithonia diversifolia. Mycorrhiza 14:103–109
Sugahara M, Izutsu K, Nishimura Y, Sakamoto F (2013) Oriental orchid (Cymbidium floribundum) attracts the Japanese honeybee (Apis cerana japonica) with a mixture of 3-hydroxyoctanoic acid and 10-hydroxy-(E)-2-decenoic acid. Zool Sci 30:99–104
Thomson JD, Draguleasa MA, Tan MG (2015) Flowers with caffeinated nectar receive more pollination. Arthropod Plant Interact 9:1–7
Tiedeken EJ, Stout JC, Stevenson PC, Wright GA (2014) Bumblebees are not deterred by ecologically relevant concentrations of nectar toxins. J Exp Biol 217:1620–1625
Vereecken NJ, Schiestl FP (2008) The evolution of imperfect floral mimicry. Proc Natl Acad Sci U S A 105:7484–7488
Wright G, Baker D, Palmer M, Stabler D, Mustard J, Power E, Borland A, Stevenson P (2013) Caffeine in floral nectar enhances a pollinator’s memory of reward. Science 339:1202–1204
Zhao G, Li J, Di N, Liu F (2014) Nectar phenolics drive cross visits between dimorphic flowers by honey bees. J Apic Res 53:489–492
Acknowledgments
We thank Mr. Yong Xiong and Yonghe Miao for assistance in nectar sampling, and many research assistants including Guangyin Zhao, Jianjun Li, Mingyue Ji, and Liyun Luo. We also thank Dr. Wei Cao of Northwest University, Xi’an City, China, for conducting nectar chemistry analysis, and members of the Adler lab, Prof. David Denlinger, Dr. Martin Heil, and one anonymous reviewer for feedback on the manuscript. This work was supported by National Basic Research Program of China (2007CB411603) and National Natural Science Foundation of China (30870445 and 31270525).
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Liu, F., Gao, J., Di, N. et al. Nectar Attracts Foraging Honey Bees with Components of Their Queen Pheromones. J Chem Ecol 41, 1028–1036 (2015). https://doi.org/10.1007/s10886-015-0642-2
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DOI: https://doi.org/10.1007/s10886-015-0642-2


