Skip to main content
Log in

Harden up: metal acquisition in the weaponized ovipositors of aculeate hymenoptera

  • Original paper
  • Published:
Zoomorphology Aims and scope Submit manuscript

A Correction to this article was published on 16 June 2018

This article has been updated

Abstract

The use of metal ions to harden the tips and edges of ovipositors is known to occur in many hymenopteran species. However, species using the ovipositor for delivery of venom, which occurs in the aculeate hymenoptera (stinging wasps, ants, and bees) remains uninvestigated. In this study, scanning electron microscopy coupled with energy-dispersive X-ray analysis was used to investigate the morphology and metal compositional differences among aculeate aculei. We show that aculeate aculei have a wide diversity of morphological adaptations relating to their lifestyle. We also demonstrate that metals are present in the aculei of all families of aculeate studied. The presence of metals is non-uniform and concentrated in the distal region of the stinger, especially along the longitudinal edges. This study is the first comparative investigation to document metal accumulation in aculeate aculei.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14

Similar content being viewed by others

Change history

  • 16 June 2018

    The author would like to correct the errors in the publication of the original article. The corrected details are given below for your reading.

References

  • Arévalo E, Zhu Y, Carpenter JM, Strassmann JE, Queller DC, Flook P, Zhao S, Zacchi F, Queller DC, Strassmann JE (2004) The phylogeny of the social wasp subfamily Polistinae: evidence from microsatellite flanking sequences, mitochondrial COI sequence, and morphological characters. BMC Evolut Biol 4(1):8–8

    Article  Google Scholar 

  • Ascher JS, Danforth BN, Ji S (2001) Phylogenetic utility of the major opsin in Bees (Hymenoptera: Apoidea): a reassessment. Mol Phylogenet Evol 19(1):76–93

    Article  PubMed  CAS  Google Scholar 

  • Borowiec ML, Rabeling C, Brady SG, Fisher BL, Schultz TR, Ward PS (2017) Compositional heterogeneity and outgroup choice influence the internal phylogeny of the ants. Mol Phylogenet Evol (Sumbitted)

  • Brady SG, Schultz TR, Fisher BL, Ward PS (2006) Evaluating alternative hypotheses for the early evolution and diversification of ants. Proc Natl Acad Sci USA 103(48):18172–18177

    Article  PubMed  CAS  Google Scholar 

  • Branstetter MG, Danforth BN, Pitts JP, Faircloth BC, Ward PS, Buffington ML, Gates MW, Kula RR, Brady SG (2017) Phylogenomic insights into the evolution of stinging wasps and the origins of ants and bees. Curr Biol 27(7):1019–1025

    Article  PubMed  CAS  Google Scholar 

  • Cameron SA, Hines HM, Williams PH (2007) A comprehensive phylogeny of the bumble bees (Bombus). Biol J Lin Soc 91(1):161–188

    Article  Google Scholar 

  • Cardinal S, Danforth BN, Pitts JP, Gillespie JJ, Cameron SA (2011) The antiquity and evolutionary history of social behavior in bees. PLoS One 6(6):e21086–e21086

    Article  CAS  Google Scholar 

  • Cribb BW, Stewart A, Huang H, Truss R, Noller B, Rasch R, Zalucki MP (2008) Unique zinc mass in mandibles separates drywood termites from other groups of termites. Die Naturwissenschaften 95(5):433–441

    Article  PubMed  CAS  Google Scholar 

  • Cribb BW, Lin CL, Rintoul L, Rasch R, Hasenpusch J, Huang H (2010) Hardness in arthropod exoskeletons in the absence of transition metals. Acta Biomater 6(8):3152–3156

    Article  PubMed  CAS  Google Scholar 

  • Degtyar E, Harrington MJ, Politi Y, Fratzl P (2014) The mechanical role of metal ions in biogenic protein-based materials. Angew Chem Int Ed 53(45):12026–12044

    Article  CAS  Google Scholar 

  • Edwards A, Fawke JD, McClements JG, Smith SA, Wyeth P (1993) Correlation of zinc distribution and enhanced hardness in the mandibular cuticle of the leaf-cutting ant Atta sexdens rubropilosa. Cell Biol Int 17(7):697–698

    Article  Google Scholar 

  • Fisher RM (1993) How important is the sting in insect social evolution? Ethol Ecol Evol 5(2):157–168

    Article  Google Scholar 

  • Fontaine AR, Olsen N, Ring RA, Singla CL (1991) Cuticular metal hardening of mouthparts and claws of some forest insects of British Columbia. J Entomol Soc Br Columbia 88:45–55

    Google Scholar 

  • Goldstein JI, Newbury DE, Echlin P, Joy DC, Romig AD, Lyman CE, Fiori C, Lifshin E (1992) Scanning electron microscopy and X-ray microanalysis. A text for biologists, materials scientists, and geologists, 2nd ed. Plenum Press, New York

    Google Scholar 

  • Hasegawa E, Crozier RH (2006) Phylogenetic relationships among species groups of the ant genus Myrmecia. Mol Phylogenet Evol 38(3):575–582

    Article  PubMed  CAS  Google Scholar 

  • Hermann HR (1971) Sting autotomy, a defensive mechanism in certain social Hymenoptera. Insectes Soc 18(2):111–120

    Article  Google Scholar 

  • Hermann HR (1984). Defensive mechanisms in social insects. Praeger

  • Hillerton JE, Vincent JFV (1982) The specific location of zinc in insect mandibles. J Exp Biol 101:333–336

    CAS  Google Scholar 

  • Hillerton JE, Robertson B, Vincent JFV (1984) The presence of zinc or manganese as the predominant metal in the mandibles of adult, stored-product beetles. J Stored Prod Res 20(3):133–137

    Article  CAS  Google Scholar 

  • Kukuk PF, Eickwort GC, Raveret-Richter M, Alexander B, Gibson R, Morse RA, Ratnieks F (1989) Importance of the sting in the evolution of sociality in the hymenoptera. Ann Entomol Soc Am 82(1):1–5

    Article  Google Scholar 

  • Kundanati L, Gundiah N (2014) Biomechanics of substrate boring by fig wasps. J Exp Biol 217(11):1946–1954

    Article  PubMed  Google Scholar 

  • Lopez-Osorio F, Pickett KM, Carpenter JM, Ballif BA, Agnarsson I (2014) Phylogenetic relationships of yellowjackets inferred from nine loci (Hymenoptera: Vespidae, Vespinae, Vespula and Dolichovespula). Mol Phylogenet Evol 73:190–201

    Article  PubMed  CAS  Google Scholar 

  • Maschwitz UWJ, Kloft W (1981) Morphology and function of the venom apparatus of insects—bees, wasps, ants and caterpillars. Academic Press, Berlin; New York

    Google Scholar 

  • Morgan TD, Baker P, Kramer KJ, Basibuyuk HH, Quicke DLJ (2003) Metals in mandibles of stored product insects: do zinc and manganese enhance the ability of larvae to infest seeds? J Stored Prod Res 39(1):65–75

    Article  CAS  Google Scholar 

  • Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N, Pearse W (2015) caper: Comparative analyses of phylogenetics and evolution R. R package version 0.5.2

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20(2):289–290

    Article  PubMed  CAS  Google Scholar 

  • Perrard A, Pickett K, Villemant C, Kojima J-i, Carpenter J (2013) Phylogeny of hornets: a total evidence approach (Hymenoptera, Vespidae, Vespinae, Vespa). J Hymenoptera Res 32:1–15

    Article  Google Scholar 

  • Piek T (1986) Historical Introduction. In: Piek T (ed) Venoms of the hymenoptera: biochemical, pharmacological and behavioural aspects. Academic Press, Florida, pp 1–13

    Google Scholar 

  • Polidori C, García AJ, Nieves-Aldrey JL (2013) Breaking up the wall: metal-enrichment in Ovipositors, but not in mandibles, co-varies with substrate hardness in gall-wasps and their associates. PLoS ONE 8(7):70529–70529

    Article  CAS  Google Scholar 

  • Quicke D (1998) Manganese and zinc in the ovipositors and mandibles of hymenopterous insects. Zool J Linnean Soc 124(4):387–396

    Article  Google Scholar 

  • Quicke DLJ (2014) The braconid and ichneumonid parasitoid wasps biology, systematics, evolution and ecology. Wiley

  • Quicke DLJ, Leralec A, Vilhelmsen L (1999) Ovipositor structure and function in the parasitic Hymenoptera with an exploration of new hypotheses. Atti dell’Accademia Nazionale Italiana di Entomologia Rendiconti 47:197–239

    Google Scholar 

  • Ramya J, Rajagopal D (2008) Morphology of the sting and its associated glands in four different honey bee species. J Apic Res 47(1):46–52

    Article  Google Scholar 

  • Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3(2):217–223

    Article  Google Scholar 

  • Robertson PL (1968) A morphological and functional study of the venom apparatus in representatives of some major groups of Hymenoptera. Aust J Zool 16(1):133–133

    Article  Google Scholar 

  • Santos BF, Payne A, Pickett KM, Carpenter JM (2015) Phylogeny and historical biogeography of the paper wasp genus Polistes (Hymenoptera: Vespidae): implications for the overwintering hypothesis of social evolution. Cladistics 31(5):535–549

    Article  Google Scholar 

  • Schmidt C (2013) Molecular phylogenetics of ponerine ants (Hymenoptera: Formicidae: Ponerinae). Zootaxa 3647(2):201–250

    Article  PubMed  Google Scholar 

  • Schmidt JO (2016). The sting of the wild. Johns Hopkins University Press

  • Schmitz J, Moritz RFA (1998) Molecular phylogeny of Vespidae (Hymenoptera) and the evolution of sociality in wasps. Mol Phylogenet Evol 9(2):183–191

    Article  PubMed  CAS  Google Scholar 

  • Schofield RMS (2005) Metal-halogen biomaterials, vol 51, pp 45–47

  • Schofield RMS, Postlethwait JH, Lefevre HW (1997) MeV-ion microprobe analyses of whole Drosophila suggest that zinc and copper accumulation is regulated storage not deposit excretion. J Exp Biol 200(Pt 24):3235–3243

    PubMed  CAS  Google Scholar 

  • Schofield RMS, Nesson MH, Richardson KA (2002) Tooth hardness increases with zinc-content in mandibles of young adult leaf-cutter ants. Die Naturwissenschaften 89(12):579–583

    PubMed  CAS  Google Scholar 

  • Shorter JR, Rueppell O (2012) A review on self-destructive defense behaviors in social insects. Insectes Soc 59(1):1–10

    Article  Google Scholar 

  • Sledge MF, Dani FR, Fortunato A, Maschwitz U, Clarke SR, Francescato E, Hashim R, Morgan ED, Jones GR, Turillazzi S (1999) Venom induces alarm behaviour in the social wasp Polybioides raphigastra (Hymenoptera: Vespidae): an investigation of alarm behaviour, venom volatiles and sting autotomy. Physiological Entomology 24(3):234–239

    Article  CAS  Google Scholar 

  • Starr CK (1985) Enabling mechanisms in the origin of sociality in the hymenoptera—the sting’s the thing. Ann Entomol Soc Am 78(6):836–840

    Article  Google Scholar 

  • Starr CK (1989) In reply, is the sting the thing? Ann Entomol Soc Am 82(1):6–8

    Article  Google Scholar 

  • Symonds MRE, Blomberg SP (2014) A primer on phylogenetic generalised least squares. Springer, Berlin Heidelberg, Berlin, pp 105–130

    Google Scholar 

  • Willis LG, Winston ML, Honda BM (1992) Phylogenetic relationships in the honeybee (Genus Apis) as determined by the sequence of the cytochrome oxidase II region of mitochondrial DNA. Mol Phylogenet Evol 1(3):169–178

    Article  PubMed  CAS  Google Scholar 

  • Wilson JS, Williams KA, Forister ML, von Dohlen CD, Pitts JP (2012) Repeated evolution in overlapping mimicry rings among North American velvet ants. Nat Commun 3:1272–1272

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank UQ Centre for Microscopy for training in SEM techniques and MCI at the Smithsonian for use of microscopy facilities. KB received support from the Peter Buck predoctoral fellowship program (NMNH) and a UQ PhD scholarship. SGB received research support from U.S. National Science Foundation Grant DEB-1555905.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Seán G. Brady or Bryan G. Fry.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baumann, K., Vicenzi, E.P., Lam, T. et al. Harden up: metal acquisition in the weaponized ovipositors of aculeate hymenoptera. Zoomorphology 137, 389–406 (2018). https://doi.org/10.1007/s00435-018-0403-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-018-0403-1

Keywords

Navigation