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Functional Ultrastructure of Hymenopteran Stingers: Devastating Spear or Delicate Syringe

Part of: Micrographia Collection

Published online by Cambridge University Press:  26 May 2022

Jan Černý ,
František Weyda ,
Michal Perlík  and
Dalibor Kodrík Open the ORCID record for Dalibor Kodrík [Opens in a new window]
Jan Černý
Affiliation:
Institute of Entomology, Biology Centre, CAS, Branišovská 31, 370 05 České Budějovice, Czech Republic Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic
František Weyda
Affiliation:
Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic
Michal Perlík
Affiliation:
Institute of Entomology, Biology Centre, CAS, Branišovská 31, 370 05 České Budějovice, Czech Republic Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic
Dalibor Kodrík*
Affiliation:
Institute of Entomology, Biology Centre, CAS, Branišovská 31, 370 05 České Budějovice, Czech Republic Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic
*
*Corresponding author: Dalibor Kodrík, E-mail: [email protected]
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Abstract

In this study, we tested the hypothesis that a micro-serrated edge on the honey bee Apis mellifera stinger tip serves as a tool for more intensive crushing of cell membranes in the victim's tissues. This could have mechanical consequences as well as initiate metabolic pathways linked to cell membrane breakdown (e.g., production of biogenic amines). Accordingly, we found that hymenopteran species that use their stingers as an offensive or defensive weapon to do as much damage to the victim's body as possible had this cuticular microstructure. In parasitic hymenopterans, on the other hand, this structure was missing, as stingers are solely used to delicately transport venom to the victim's body in order to do little mechanical harm. We also demonstrated that the stinger lancets of the honey bee A. mellifera are living organs with sensilla innervated by sensory neurons and containing other essential tissues, rather than mere cuticular structures.

Keywords

beeHymenopteranerveSEMsensillastinger microstructureTEMultrastructure
Type
Micrographia
Information
Microscopy and Microanalysis , Volume 28 , Issue 5 , October 2022 , pp. 1808 - 1818
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of the Microscopy Society of America

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References

Banks, BEC & Shipolini, RA (1986). Chemistry and Pharmacology of Honey-Bee. London: Academic Press Inc. Ltd.Google Scholar
Beckage, NE & Gelman, DB (2004). Wasp parasitoid disruption of host development: Implications for new biologically based strategies for insect control. Annu Rev Entomol 49, 299–330.CrossRefGoogle ScholarPubMed
Bogdanov, S (2016). Bee Venom: Production, Composition, Quality. 1. The Bee Venom Book. Switzerland: Muehlethurnen.Google Scholar
Breed, MD, Robinson, GE & Page, RE (1990). Division of labor during honey bee colony defense. Behav Ecol Sociobiol 27, 395–401.CrossRefGoogle Scholar
Cerkvenik, U, Van de Straat, B, Gussekloo, SW & Van Leeuwen, JL (2017). Mechanisms of ovipositor insertion and steering of a parasitic wasp. Proc Natl Acad Sci USA 114, E7822–E7831.CrossRefGoogle ScholarPubMed
Chapman, RF (1998). The Insects, Structure and Function, 4th ed. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Csader, M, Mayer, K, Betz, O, Fischer, S & Eggs, B (2021). Ovipositor of the braconid wasp Habrobracon hebetor: Structural and functional aspects. J Hymenopt Res 83, 73–99.CrossRefGoogle Scholar
D'Adamo, P, Lozada, M & Corley, JC (2004). An attraction pheromone from heads of worker Vespula germanica wasps. J Insect Behav 17, 809–821.CrossRefGoogle Scholar
Dweck, HKM, Gadallah, NS & Darwish, E (2008). Structure and sensory equipment of the ovipositor of Habrobracon hebetor (Say) (Hymenoptera: Braconidae). Micron 39, 1255–1261.CrossRefGoogle Scholar
Evans, DL & Smidt, JO (1990). Insect Defenses. Adaptive Mechanisms and Strategies of Prey and Predators. New York: SUNY Press.Google Scholar
Fateryga, AV & Ivanov, S (2004). The nesting biology of Ancistrocerus nigricornis (Curtis, 1826) (Hymenoptera: Vespidae: Eumeninae) in Crimea. Izvestiya Kharkovskogo Entomologicheskogo Obshchestva 11, 154–163 (in Russian).Google Scholar
Feldberg, W (1940). The action of bee venom, cobra venom and lysolecithin on the adrenal medulla. J Physiol 99, 104–118.CrossRefGoogle ScholarPubMed
Free, JB (1958). The defence of bumblebee colonies. Behaviour 12, 233–242.CrossRefGoogle Scholar
Gal, R, Kaiser, M, Haspel, G & Libersat, F (2014). Sensory arsenal on the stinger of the parasitoid jewel wasp and its possible role in identifying cockroach brains. PLoS One 9, e89683.CrossRefGoogle ScholarPubMed
Gilley, D (2001). The behavior of honey bees (Apis mellifera ligustica) during queen duels. Ethology 107, 601–622.CrossRefGoogle Scholar
Horan, KL, Adamski, SW, Ayele, W, Langone, JJ & Grega, GJ (1986). Evidence that prolonged histamine suffusions produce transient increases in vascular permeability subsequent to the formation of venular macro-molecular leakage sites. Proof of the Majno-Palade hypothesis. Am J Pathol 123, 570–576.Google Scholar
Huang, ZY, Li, SY, Lu, W & Zheng, XL (2019). Structure and sense organs of ovipositors of an endoparasitoid Aprostocetus causalis and an ectoparasitoid Quadrastichus mendeli in Leptocybe spp. Microsc Microanal 25, 250–256.CrossRefGoogle Scholar
King, PE & Fordy, MR (1970). The external morphology of the pore structures on the tip of the ovipositor in Hymenoptera. Entomol Mon Mag 106, 65–66.Google Scholar
Koludarov, I, Jackson, TNW, den Brouw, BO, Dobson, J, Dashevsky, D, Arbuckle, K, Clemente, CJ, Stockdale, EJ, Cochran, C, Debono, J, Stephens, C, Panagides, N, Li, B, Manchadi, MLR, Violette, A, Fourmy, R, Hendrikx, I, Nouwens, A, Clements, J, Martelli, P, Kwok, HF & Fry, BG (2017). Enter the dragon: The dynamic and multifunctional evolution of anguimorpha lizard venoms. Toxins 9, 242.CrossRefGoogle ScholarPubMed
Krenn, HW & Pass, G (1993). Wing-hearts in mecoptera. Int J Insect Morphol Embryol 22, 63–76.CrossRefGoogle Scholar
Kryukova, NA, Dubovskiy, IM, Chertkova, EA, Vorontsova, YL, Slepneva, IA & Glupov, VV (2011). The effect of Habrobracon hebetor venom on the activity of the prophenoloxidase system, the generation of reactive oxygen species and encapsulation in the haemolymph of Galleria mellonella larvae. J Insect Physiol 57, 796–800.CrossRefGoogle ScholarPubMed
Kryukova, NA, Dubovskiy, IM, Gryzanova, EA, Naumkina, VV & Glupov, VV (2007). Cell immunity response of the Galleria mellonella (L.) (Lepidoptera, Piralidae) during parasitization of Habrobracon hebetor (Say) (Hymenoptera, Braconidae). Euroasian Entomol J 6, 361–364.Google Scholar
Lee, S, Baek, J & Yoon, K (2016). Differential properties of venom peptides and proteins in solitary vs. social hunting wasps. Toxins 8, 32.CrossRefGoogle ScholarPubMed
Le Lannic, J & Nénon, JP (1999). Functional morphology of the ovipositor in Megarhyssa atrata (Hymenoptera, Ichneumonidae) and its penetration into wood. Zoomorphology 119, 73–79.CrossRefGoogle Scholar
Ling, JT, Song, ZH, Wang, JR, Chen, KY, Li, JY, Xu, SJ, Ren, L, Chen, ZP, Jin, DW & Jiang, LL (2017). Effect of honeybee stinger and its microstructured barbs on insertion and pull force. J Mech Behav Biomed Mater 68, 173–179.CrossRefGoogle ScholarPubMed
Lubawy, J, Urbanski, A, Mrówczynska, L, Matuszewska, E, Swiatły-Błaszkiewicz, A, Matysiak, J & Rosinski, R (2019). The influence of bee venom melittin on the functioning of the immune system and the contractile activity of the insect heart – A preliminary study. Toxins 11, 494.CrossRefGoogle ScholarPubMed
Macek, J, Straka, J, Bogusch, P, Dvořák, L, Bezděčka, P & Tyrner, P (2010). Blanokřídlí České Republiky I. – žahadloví [in Czech]. Praha: Academia.Google Scholar
Michener, CD (2007). The Bees of the World, 2nd ed. Baltimore, Maryland: The John Hopkins University Press.Google Scholar
Moreno, M & Girald, E (2015). Three valuable peptides from bee and wasp venoms for therapeutic and biotechnological use: Melittin, apamin and mastoparan. Toxins 7, 1126–1150.CrossRefGoogle ScholarPubMed
Moritz, RFA, Pflugfelder, J & Crewe, RM (2003). Lethal fighting between honeybee queens and parasitic workers (Apis mellifera). Naturwissenschaften 90, 378–381.Google Scholar
Moritz, RFA & Southwick, EE (1992). Bees as Superorganisms: An Evolutionary Reality. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Ovruski, S, Aluja, M, Sivinski, J & Wharton, R (2000). Hymenopteran parasitoids on fruit-infesting Tephritidae (Diptera) in Latin America and the southern United States: Diversity, distribution, taxonomic status and their use in fruit fly biological control. J Integr Pest Manag 5, 81–107.CrossRefGoogle Scholar
Pennacchio, F, Caccia, S & Digilio, MC (2014). Host regulation and nutritional exploitation by parasitic wasps. Curr Opin Insect Sci 6, 74–79.CrossRefGoogle ScholarPubMed
Pollard, DG (1969). Directional control of the stylets in phytophagous Hemiptera. Proc R Entomol Soc Lond Ser A Gen Entomol 44, 173–185.Google Scholar
Prýmas, L, Danihlík, J, Dlouhá, Š, Dostálková, S, Kabát, M, Hroncová, Z & Petřivalský, M (2017). Včelařství, Vol. 2 (in Czech). Praha, Czech Republic: PSNV Praha.Google Scholar
Quicke, LJ (2015). The Braconid and Ichneumonid Parasitoid Wasps: Biology, Systematics, Evolution and Ecology. Oxford, UK: John Wiley & Sons.Google Scholar
Rasmont, P, Ghisbain, G & Terzo, M (2021). Bumblebees of Europe and Neighbouring Regions, 1st ed. Iver, UK: NAP Editions.Google Scholar
Santoro, D, Hartley, S, Suckling, DM & Lester, PJ (2015). The stinging response of the common wasp (Vespula vulgaris): Plasticity and variation in individual aggressiveness. Insectes Soc 62, 455–463.CrossRefGoogle Scholar
Shaik, HA, Mishra, A & Kodrík, D (2017). Beneficial effect of adipokinetic hormone on neuromuscular paralysis in insect body elicited by braconid wasp venom. Comp Biochem Physiol C 196, 11–18.Google ScholarPubMed
Shing, H & Erickson, EH (1982). Some ultrastructure of the honeybee (Apis mellifera L.) sting. Apidologie 13, 203–213.CrossRefGoogle Scholar
Sláma, K & Lukáš, J (2011). Myogenic nature of insect heartbeat and intestinal peristalsis, revealed by neuromuscular paralysis caused by the sting of a braconid wasp. J Insect Physiol 57, 251–259.CrossRefGoogle ScholarPubMed
Smith, EL (1970). Evolutionary morphology of the external insect genitalia. 2. Hymenoptera. Ann Entomol Soc Am 63, 1–27.CrossRefGoogle Scholar
Snodgrass, RE (1925). Anatomy and Physiology of the Honeybee, 1st ed. New York: McGraw-Hill Book Company.Google Scholar
Sumner, S, Law, G & Cini, A (2018). Why we love bees and hate wasps. Ecol Entomol 43, 836–845.CrossRefGoogle Scholar
Thompson, F (1932). About bee venom. Bee World 13, 37–40.CrossRefGoogle Scholar
Vincent, JF & King, MJ (1995). The mechanism of drilling by wood wasp ovipositors. Biomimetics 3, 187–201.Google Scholar
Weyda, F & Kodrík, D (2021). New functionally ultrastructural details of honey bee stinger tip: Serrated edge and pitted surface. J Apicult Res 60, 875–878.CrossRefGoogle Scholar
Wyatt, TD (2009). Pheromones and other chemical communication in animals. In Encyclopedia of Neuroscience, Squire, LR (Ed.), pp. 611–616. Oxford: Academic Press.CrossRefGoogle Scholar
Zablotny, JE (2009). Sociality. In Encyclopedia of Insects, Resh, VJ & Cardé, RT (Eds.), pp. 928–935. Amsterdam: Elsevier.CrossRefGoogle Scholar