[en] The feeding mechanisms of animals constrain the spectrum of resources that they can exploit profitably. For floral nectar eaters, both corolla depth and nectar properties have marked influence on foraging choices. We report the multiple strategies used by honey bees to efficiently extract nectar at the range of sugar concentrations and corolla depths they face in nature. Honey bees can collect nectar by dipping their hairy tongues or capillary loading when lapping it, or they can attach the tongue to the wall of long corollas and directly suck the nectar along the tongue sides. The honey bee feeding apparatus is unveiled as a multifunctional tool that can switch between lapping and sucking nectar according to the instantaneous ingesting efficiency, which is determined by the interplay of nectar-mouth distance and sugar concentration. These versatile feeding mechanisms allow honey bees to extract nectar efficiently from a wider range of floral resources than previously appreciated and endow them with remarkable adaptability to diverse foraging environments.
Disciplines :
Physics Zoology
Author, co-author :
Wei, Jiangkun; School of Aeronautics and Astronautics, Sun Yat-Sen University, Shenzhen 518107, People's Republic of China
Rico-Guevara, Alejandro ; Department of Biology, University of Washington, Seattle, WA 98195 ; Burke Museum of Natural History and Culture, University of Washington, Seattle, WA 98105
Nicolson, Susan W; Department of Zoology and Entomology, University of Pretoria, Hatfield 0028, South Africa
Brau, Fabian ; Université libre de Bruxelles, Nonlinear Physical Chemistry Unit, CP231, Brussels 1050, Belgium
DAMMAN, Pascal ; Université de Mons - UMONS > Faculté des Science > Service du Laboratoire Interfaces et Fluides Complexes
Gorb, Stanislav N ; Functional Morphology and Biomechanics, Department of Zoology, Kiel University, Kiel 24118, Germany
Wu, Zhigang; School of Aeronautics and Astronautics, Sun Yat-Sen University, Shenzhen 518107, People's Republic of China
Wu, Jianing ; School of Aeronautics and Astronautics, Sun Yat-Sen University, Shenzhen 518107, People's Republic of China ; School of Advanced Manufacturing, Sun Yat-Sen University, Shenzhen 518107, People's Republic of China
Language :
English
Title :
Honey bees switch mechanisms to drink deep nectar efficiently.
Publication date :
25 July 2023
Journal title :
Proceedings of the National Academy of Sciences of the United States of America
S885 - Laboratoire Interfaces et Fluides complexes
Research institute :
R150 - Institut de Recherche sur les Systèmes Complexes
Funders :
MOST | National Natural Science Foundation of China shenzhen science and technology program Walt Halperin Endowed Professorship The Washington Research Foundation as Distinguished Investigator The F.R.S.-FNRS research grant
Funding text :
ACKNOWLEDGMENTS. We appreciate the staff at the Shanghai Synchrotron Radiation Facility for helping us recording the honey bee feeding process by synchrotron X-ray video. This work was supported by the National Natural Science Foundation of China (grant no. 51905556 and grant no. 52275298), the Shenzhen Science and Technology Program (grant no.GXWD2021B03 and grant no. 20220817165030002), the Walt Halperin Endowed Professorship (to A.R.-G.), the Washington Research Foundation as Distinguished Investigator (to A.R.-G.), and The F.R.S.-FNRS research grant (PDR “ElastoCap”) no T.0025.19.
H. W. Krenn, Insect Mouthparts: Form, Function, Development andPerformance (Springer Nature, 2019).
C. Darwin, The Various Contrivances by which Orchids are Fertilised by Insects (John Murray, 1877).
K. G. Kornev, P. H. Adler, “Physical determinants of fluid-feeding in insects” in Insect Mouthparts, (Springer, 2019), pp. 263–314.
L. A. Nilsson, The evolution of flowers with deep corolla tubes. Nature 334, 147–149 (1988).
W. Kim, T. Gilet, J. W. M. Bush, Optimal concentrations in nectar feeding. Proc. Natl. Acad. Sci. U.S.A. 108, 16618–16621 (2011).
M. S. Lehnert et al., Mouthpart conduit sizes of fluid-feeding insects determine the ability to feed from pores. Proc. Biol. Sci. 284, 20162026 (2017).
C. Zhang, P. H. Adler, K. G. Kornev, Insect solutions for open self-cleaning microfluidics. Adv. Mater. Interfaces 6, 1–8 (2019).
C. J. van der Kooi, J. Ollerton, The origins of flowering plants and pollinators. Science 368, 1306–1308 (2020).
A. Rico-Guevara, K. J. Hurme, R. Elting, A. L. Russell, Bene“fit” assessment in pollination coevolution: Mechanistic perspectives on hummingbird bill-flower matching. Integr. Comp. Biol. 61, 681–695 (2021).
S. G. T. Klumpers, M. Stang, P. G. L. Klinkhamer, Foraging efficiency and size matching in a plant–pollinator community: The importance of sugar content and tongue length. Ecol. Lett. 22, 469–479 (2019).
L. D. Harder, Flower handling efficiency of bumble bees: Morphological aspects of probing time. Oecologia 57, 274–280 (1983).
L. D. Harder, Effects of nectar concentration and flower depth on flower handling efficiency of bumble bees. Oecologia 69, 309–315 (1986).
M. Tschapka, T. P. Gonzalez-Terrazas, M. Knörnschild, Nectar uptake in bats using a pumping-tongue mechanism. Sci. Adv. 1, e1500525 (2015).
A. Rico-Guevara, M. A. Rubega, The hummingbird tongue is a fluid trap, not a capillary tube. Proc. Natl. Acad. Sci. U.S.A. 108, 9356–9360 (2011).
A. Rico-Guevara, T. H. Fan, M. A. Rubega, Hummingbird tongues are elastic micropumps. Proc. Biol. Sci. 282, 20151014 (2015).
D. Cuban, A. E. Hewes, A. J. Sargent, D. J. Groom, A. Rico-Guevara, On the feeding biomechanics of nectarivorous birds. J. Exp. Biol. 225, jeb243096 (2022).
S. W. Nicolson, “Nectar Consumers” in Nectaries and Nectar (Springer, 2007), pp. 289–342.
R. Snodgrass, Anatomy of the Honey Bee (Cornell University Press, 1956).
L. Goodman, Form and Function in the Honey Bee (International Bee Research Association, 2003).
L. D. Harder, Measurement and estimation of functional proboscis length in bumblebees (Hymenoptera: Apidae). Canadian J. Zool. 60, 1073–1079 (1982).
H. Yang, J. Wu, S. Yan, Effects of erectable glossal hairs on a honeybee’s nectar-drinking strategy. Appl. Phys. Lett. 104, 1–5 (2014).
J. Wu, R. Zhu, S. Yan, Y. Yang, Erection pattern and section-wise wettability of honeybee glossal hairs in nectar feeding. J. Exp. Biol. 218, 664–667 (2015).
J. Zhao, J. Wu, S. Yan, Erection mechanism of glossal hairs during honeybee feeding. J. Theoret. Biol. 386, 62–68 (2015).
J. Wei et al., Sucking or lapping: Facultative feeding mechanisms in honey bees (Apis mellifera). Biol. Lett. 16, 1–5 (2020).
J. Wu, G. Shi, Y. Zhao, S. Yan, How to dip nectar: Optimal time apportionment in natural viscous fluid transport. J. Phys. D Appl. Phys. 51, 245401 (2018).
A. Lechantre et al., Essential role of papillae flexibility in nectar capture by bees. Proc. Natl. Acad. Sci. U.S.A. 118, 1–7 (2021).
T. Petanidou, E. Smets, The potential of marginal lands for bees and apiculture–Nectar secretion in Mediterranean shrublands. Apidologie 26, 39–52 (1995).
S. A. Corbet, E. S. Delfosse, Honeybees and the nectar of Echium plantagineum L. in southeastern Australia. Aust. J. Ecol. 9, 125–139 (1984).
H. W. Krenn, J. D. Plant, N. U. Szucsich, Mouthparts of flower-visiting insects. Arthropod Struct. Dev. 34, 1–40 (2005).
J. Wei et al., Trade-off mechanism of honey bee sucking and lapping. Soft Matter. 18, 5568–5574 (2022).
G. H. Pyke, N. M. Waser, The production of dilute nectars by hummingbird and honeyeater flowers. Biotropica 13, 260–270 (1981).
P. Green, M. McHenry, A. Rico-Guevara, Mechanoethology: The physical mechanisms of behavior. Integr. Comp. Biol. 61, 613–623 (2021).
K. G. Kornev, A. A. Salamatin, P. H. Adler, C. E. Beard, Structural and physical determinants of the proboscis-sucking pump complex in the evolution of fluid-feeding insects. Sci. Rep. 7, 1–18 (2017).
D. Langbein, The shape and stability of liquid menisci at solid edges. J. Fluid Mech. 213, 251–265 (1990).
W. Kim, J. W. M. Bush, Natural drinking strategies. J. Fluid Mech. 705, 7–25 (2012).
J. Paul, F. Roces, Fluid intake rates in ants correlate with their feeding habits. J. Insect Physiol. 49, 347–357 (2003).
L. Shi, J. Wu, H. W. Krenn, Y. Yang, S. Yan, Temporal model of fluid-feeding mechanisms in a long proboscid orchid bee compared to the short proboscid honey bee. J. Theor. Biol. 484, 110017 (2020).
K. A. Pivnick, J. N. McNeil, Effects of nectar concentration on butterfly feeding: Measured feeding rates for Thymelicus lineola (Lepidoptera: Hesperiidae) and a general feeding model for adult Lepidoptera. Oecologia 66, 226–237 (1985).
J. Wei et al., Enhanced flexibility of the segmented honey bee tongue with hydrophobic tongue hairs. ACS Appl. Mater. Interfaces 14, 12911–12919 (2022).
J. Wei et al., Hydrophilic and opened canals in honey bee tongue rods endow elastic structures with multiple functions. Acta Biomaterialia 137, 162–171 (2022).
S. W. Nicolson, Sweet solutions: Nectar chemistry and quality. Philos. Trans. R Soc. B 377, 20210163 (2022).
P. K. Visscher, T. D. Seeley, Foraging strategy of honeybee colonies in a temperate deciduous forest. Ecology 63, 1790–1801 (1982).
M. Beekman, F. L. W. Ratnieks, Long-range foraging by the honey-bee Apis mellifera L. Funct. Ecol. 14, 490–496 (2000).
C. R. Ribbands, The foraging method of individual honey-bees. J. Anim. Ecol. 18, 47–66 (1949).
K. Lunau et al., Nectar mimicry: A new phenomenon. Sci. Rep. 10, 1–11 (2020).
Y. Sun et al., Specialized morphology and material properties make a honey bee tongue both extendible and structurally stable. Acta Biomaterialia 136, 412–419 (2021).
H. G. Baker, Sugar concentrations in nectars from hummingbird flowers. Biotropica 7, 37 (1975).
B. J. Borrell, Suction feeding in orchid bees (Apidae: Euglossini). Proc. R Soc. B Biol. Sci. 271 (suppl. 4), S164–S166 (2004).
J. V. Düster, M. H. Gruber, F. Karolyi, J. D. Plant, H. W. Krenn, Drinking with a very long proboscis: Functional morphology of orchid bee mouthparts (Euglossini, Apidae, Hymenoptera). Arthropod Struct. Dev. 47, 25–35 (2018).
S. J. Lee, B. H. Kim, J. Y. Lee, Experimental study on the fluid mechanics of blood sucking in the proboscis of a female mosquito. J. Biomechanics 42, 857–864 (2009).
