×

Erection mechanism of glossal hairs during honeybee feeding. (English) Zbl 1343.92060

Summary: Many animals use their mouthparts or tongue to feed themselves rapidly and efficiently. Honeybees have evolved specialized tongues to collect nectar from flowers. Nectar-intake movements consist of rapid protraction and retraction of glossa from a tube formed by the maxillae and labial palps. We establish a physical model to reveal the driving mechanism of hair erection. Results indicate that the glossa of honeybees is similar to a compression spring. Experimental results show that hair erection is generated by the tension of hyaline rod and the elasticity of segmental sheath. The retractor muscle of hyaline rod is contracted at first, which compresses the sheath of pigmented rings and flattens the hairs. While the retractor muscle of hyaline rod relaxes, the elastic energy storage in the compressed glossal sheath will release to change the equivalent stiffness of glossal sheath and erect glossal hairs. These results explain the erection mechanism of glossal hairs during honeybee feeding.

MSC:

92C10 Biomechanics
Full Text: DOI

References:

[1] Arruda, E. M.; Boyce, M. C., A three-dimensional constitutive model for the large stretch behaviour of rubber elastic materials, J. Mech. Phys. Solids, 41, 389-412 (1993) · Zbl 1355.74020
[2] Borrell, B. J., Mechanics of nectar feeding in the orchid bee Euglossa imperialis: pressure, viscosity and flow, J. Exp. Biol., 209, 4901-4907 (2006)
[3] Briant, T. J., On the anatomy and functions of the tongue of the honey‐bee (worker), J. Linn. Soc. Lond., Zool., 17, 408-417 (1884)
[4] Crompton, A. W.; Musinsky, C., How dogs lap: ingestion and intraoral transport in Canis familiaris, Biol. Lett., 7, 882-884 (2011)
[5] Falibene, A.; Gontijo, A. F.; Josens, R., Sucking pump activity in feeding behaviour regulation in carpenter ants, J. Insect Physiol., 55, 518-524 (2009)
[6] Harper, C. J.; Swartz, S. M.; Brainer, E. L., Specialized bat tongue is a hemodynamic nectar mop, Proc. Natl. Acad. Sci. U. S. A., 110, 8852-8857 (2013)
[7] Higginson, A. D.; Gilbert, F., Paying for nectar with wingbeats: a new model of honeybee foraging, Proc. R. Soc. B: Biol. Sci., 271, 2595-2603 (2004)
[8] Kim, S.; Laschi, C.; Trimmer, B., Soft robotics: a bioinspired evolution in robotics, Trends Biotechnol., 31, 287-294 (2013)
[9] Kim, W.; Gilet, T.; JWM, Bush, Optimal concentrations in nectar feeding, Proc. Natl. Acad. Sci. U. S. A., 108, 16618-16621 (2011)
[10] Kim, W.; Peaudecerf, F.; Baldwin, M. W.; JWM, Bush, The hummingbird’s tongue: a self-assembling capillary syphon, Proc. R. Soc. B: Biol. Sci., 279, 4990-4996 (2012)
[11] Krenn, H. W.; Plant, J. D.; Szucsich, N. U., Mouthparts of flower-visiting insects, Arthropod Struct. Dev., 34, 1-40 (2005)
[12] Lee, S. J.; Lee, S. C.; Kim, B. H., Liquid-intake flow around the tip of butterfly proboscis, J. Theor. Biol., 348, 113-121 (2014) · Zbl 1412.92058
[13] Li, C.; Wu, J.; Yang, Y.; Zhu, R.; Yan, S., Drag reduction in the mouthpart of a honeybee facilitated by galea ridges for nectar-dipping strategy, J. Bion. Eng., 12, 70-78 (2015)
[14] Ohno, S.; Hiroki, C.; Yu, W., Design and manipulation of a suction-based micro robot for moving in the abdominal cavity, Adv. Robot., 24, 1741-1761 (2010)
[15] Prakash, M.; Quéré, D.; JWM, Bush, Surface tension transport of prey by feeding shorebirds: the capillary ratchet, Science, 320, 931-934 (2008)
[16] Reis, P. M.; Jung, S.; Aristoff, J. M.; Stocker, R., How cats lap: water uptake by Felis catus, Science, 330, 1231-1234 (2010)
[17] Ren, D.; Labandeira, C. C.; Santiago-Blay, J. A.; Rasnitsyn, A.; Shih, C.; Bashkuev, A.; Logan, M. A.V.; Hotton, C.; Dilcher, D., A probable pollination mode before angiosperms: Eurasian, long-proboscid scorpionflies, Science, 326, 840-847 (2009)
[18] Rico-Guevara, A.; Rubega, M. A., The hummingbird tongue is a fluid trap, not a capillary tube, Proc. Natl. Acad. Sci. U. S. A., 108, 9356-9360 (2010)
[19] Shimizu, A.; Dohzono, I.; Nakaji, M.; Roff, D. A.; Miller, D. G.; Osato, S.; Yajima, T.; Niitsu, S.; Utsugi, N.; Sugawara, T.; Yoshimura, J., Fine-tuned bee-flower coevolutionary state hidden within multiple pollination interactions, Sci. Rep., 4, 3988 (2014)
[20] Simpson, J.; Riedel, I., Discharge and manipulation of labial gland secretion by workers of Apis mellifera (L.)(Hymenoptera: Apidae), Proc. R. Entomol. Soc. Lond. Ser. A, Gen. Entomol., 39, 76-82 (1964)
[21] Snodgrass, R. E., Anatomy of the Honey Bee (1984), Cornell University Press: Cornell University Press London, UK
[22] Tan, K.; Latty, T.; Hu, Z.; Wang, Z.; Yang, S.; Chen, W.; Oldroyd, B. P., Preferences and tradeoffs in nectar temperature and nectar concentration in the Asian hive bee Apis cerana, Behav. Ecol. Sociobiol., 68, 13-20 (2014)
[23] Wright, G. A.; Baker, D. D.; Palmer, M. J.; Stabler, D.; Mustard, J. A.; Power, E. F.; Borland, A. M.; Stevenson, P. C., Caffeine in floral nectar enhances a pollinator׳s memory of reward, Science, 339, 1202-1204 (2013)
[24] Wu, J.; Zhu, R.; Yan, S.; Yang, Y., Erection pattern and section-wise wettability of a honeybee׳s glossal hairs in nectar feeding, J. Exp. Biol., 111013 (2015)
[25] Yang, H.; Wu, J.; Yan, S., Effects of erectable glossal hairs on a honeybee׳s nectar-drinking strategy, Appl. Phys. Lett., 104, 263701 (2014)
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.