Egg Dispersal in the Phasmatodea: Convergence in Chemical Signaling Strategies Between Plants and Animals?

Abstract

Numerous tree species’ seeds contain an ‘elaiosome’ that acts as a food reward for ants and thus induces dispersal of the seeds. Many stick and leaf insect species appear to have evolved a convergent adaptation for dispersal whereby the egg ‘capitulum’ serves to induce ants to pick up and carry their eggs. Here, we investigated whether the capitulum facilitates egg dispersal by ants in the Australian stick insect Eurycnema goliath. The total fatty acid composition of E. goliath egg capsules and egg capitula were characterized to identify potential signaling compounds. Removing capitula from E. goliath eggs significantly reduced the likelihood of eggs being carried into the nests of Rhytidoponera metallica ants. Furthermore, attaching capitula to inert objects (polystyrene balls) resulted in these objects being carried into nests by R. metallica. Several fatty acids were present on the egg capsule surface in only trace amounts, whereas they made up over 10 % of the dry weight of egg capitula. The fatty acid composition of egg capitula consisted mostly of palmitic acid (C16:0), linoleic acid (C18: 2n6c), oleic acid (C18:1n9c), linolenic acid (C18:3n3), and stearic acid (C18:0). Previously reported research has found that a diglyceride lipid species of oleic acid induces carrying behavior in R. metallica when added to inert artificial stimuli. Therefore, we propose that the dispersal mechanism of E. goliath eggs has converged upon the same chemical signaling pathway used by plants to exploit ant behavior.

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

Fig. 1
Fig. 2

References

  1. Andersen AN (1988) Dispersal distance as a benefit of myrmecochory. Oecologia 75:507–511

    Article  Google Scholar 

  2. Beattie AJ (1983) Dispersal and distribution: an international symposium. Dispersal and distribution: an international symposium. P. Parey, Hamburg

    Google Scholar 

  3. Beattie AJ (1985) The evolutionary ecology of ant-plant mutualisms. Cambridge, U.K

  4. Bedford G (1978) Biology and ecology of the phasmatodea. Annu Rev Entomol 23:125–149

    Article  Google Scholar 

  5. Bond W, Slingsby P (1984) Collapse of an ant-plant mutualism: the Argentine ant (Iridomyrmex humilis) and myrmecochorous Proteaceae. Ecology 65:1031–1037

    Article  Google Scholar 

  6. Boyd RS (2001) Ecological benefits of myrmecochory for the endangered chaparral shrub Fremontodendron decumbens (Sterculiaceae). Am J Bot 88:234–241

    CAS  Article  PubMed  Google Scholar 

  7. Brew CR, O’Dowd J, Rae ID (1989) Seed dispersal by ants: behaviour-releasing compounds in elaiosomes. Oecologia 80:490–497

    Article  Google Scholar 

  8. Brock P (1998) Studies on the stick-insect genus Eurycnema Audinet-Serville (Phasmida: Phasmatisae) with particular reference to Australian species. J Orthop Res 7:61–70

    Article  Google Scholar 

  9. Brock PD, Hasenpusch JW (2009) The complete field guide to Australian stick and leaf insects. CSIRO Publishing, Collingwood

    Google Scholar 

  10. Ciccarelli D, Andreucci AC, Pagni AM, Gabari F (2005) Structure and development of the elaiosomes in Myrtus communis L. (Myrtaceae) seeds. Flora 200:326–331

    Article  Google Scholar 

  11. Clark JT (1976a) The capitulum of phasmid egg (Insecta: Phasmida). Zool J Linnean Soc 59:365–375

    Article  Google Scholar 

  12. Clark JT (1976b) The eggs of stick insects (Phasmida): a review with descriptions of the eggs of eleven species. Syst Entomol 1:95–105

    Article  Google Scholar 

  13. Compton SG, Ware AB (1991) Ants disperse the elaiosome-bearing eggs of an african stick insect. Psyche (Stuttg) 98:207–214

    Article  Google Scholar 

  14. Culver DC, Beattie AJ (1978) Myrmecochory in Viola: dynamics of seed-ant interactions in some West Virginia species. J Ecol 66:53–72

    Article  Google Scholar 

  15. Davidson DW, Morton SR (1981) Myrmecochory in some plants (F. chenopodiaceae) of the Australian arid zone. Oecologia 50:357–366

    Article  Google Scholar 

  16. Development Core Team R (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  17. Dunn RR, Gove AD, Barraclough TG et al (2007) Convergent evoution of ant-plant mutualism across plant families, continents, and time. Evol Ecol Res 9:1349–1362

    Google Scholar 

  18. Fischer RC, Richter F, Hadacek F, Mayer V (2008) Chemical differences between seeds and elaiosomes indicate an adaptation to nutritional needs of ants. Oecologia 155:539–547

    Article  PubMed  Google Scholar 

  19. Giladi I (2006) Choosing benefits or partners: a review of the evidence for the evolution of myrmecochory. Oikos 112:481–492

    Article  Google Scholar 

  20. Hadley NF (1981) Cuticular lipids of terrestrial plants and arthropods: a comparison of their structure composition and waterproofing function. Biol Rev 56:23–47

    CAS  Article  Google Scholar 

  21. Hanzawa FM, Beattie AJ, Culver DC (1988) Directed dispersal: demographic analysis of an ant-seed mutualism. Am Nat 131:1–13

    Article  Google Scholar 

  22. Heithaus ER (1981) Seed predation by rodents on three ant-dispersed plants. Ecology 62:136–145

    Article  Google Scholar 

  23. Higashi S, Tsuyuzaki S, Ohara M, Ito F (1989) Adaptive advantages of ant-dispersed seeds in the myrmecochorous plant Trillium tschonoskii (Liliaceae). Oikos 54:389–394

    Article  Google Scholar 

  24. Hughes L, Westoby M (1992a) Capitula on stick insect eggs and elaiosomes on seeds: convergent adaptations for burial by ants. Funct Ecol 6:642–648

    Article  Google Scholar 

  25. Hughes L, Westoby M (1992b) Fate of seeds adapted for dispersal by ants in Australian sclerophyll vegetation. Ecology 73:1285–1299

    Article  Google Scholar 

  26. Hughes L, Westoby M, Jurado E (1994) Convergence of elaiosomes and insect prey: evidence from ant foraging behaviour and fatty acid composition. Funct Ecol 8:358–365

    Article  Google Scholar 

  27. Lengyel S, Gove AD, Latimer AM et al (2009) Ants sow the seeds of global diversification in flowering plants. PLoS ONE 4:e5480

    PubMed Central  Article  PubMed  Google Scholar 

  28. Lengyel S, Gove AD, Latimer AM et al (2010) Convergent evolution of seed dispersal by ants, and phylogeny and biogeography in flowering plants. Perspect Plant Ecol Evol Syst 12:43–55

    Article  Google Scholar 

  29. Marshall DL, Beattie AJ, Bollenbacher WE (1979) Evidence for diglycerides as attractants in an ant-seed interaction. J Chem Ecol 5:335–344

    CAS  Article  Google Scholar 

  30. Müller C, Riederer M (2005) Plant surface properties in chemical ecology. J Chem Ecol 31:2621–2651

    Article  PubMed  Google Scholar 

  31. Olmstead ILD, Hill DRA, Dias DA et al (2013) A quantitative analysis of microalgal lipids for optimisation of biodiesel and omega-3 production. Biotechnol Bioeng 110:2096–2104

    CAS  Article  PubMed  Google Scholar 

  32. Rollo CD, Czyzewska E, Borden JH (1994) Fatty acid necromones for cockroaches. Naturwissenschaften 81:409–410

    CAS  Article  Google Scholar 

  33. Sheridan SL, Iversen KA, Itagaki H (1996) The role of chemical senses in seed-carrying behaviour by ants: a behavioural, physiological and morphological study. J Insect Physiol 42:149–159

    CAS  Article  Google Scholar 

  34. Skidmore BA, Heithaus ER (1988) Lipid cues for seed carrying by ants in Hepatica americana. J Chem Ecol 14:2185–2196

    CAS  Article  PubMed  Google Scholar 

  35. Thomas ML, Framenau VW (2005) Foraging decisions of individual workers vary with colony size in the greenhead ant Rhytidoponera metallica (Formicidae, Ectatomminae). Insect Soc 52:26–30

    Article  Google Scholar 

  36. Thompson SN (1973) A review and comparative characterization of the fatty acid composition of seven insect orders. Comp Biochem Physiol 42:467–782

    Google Scholar 

  37. Windsor DM, Trapnell DW, Amat G (1996) The egg capitulum of a neotropical walkingstick, Calynda bicuspis, induces aboveground egg dispersal by the ponerine ant, Ectatomma ruidum. J Insect Behav 9:353–367

    Article  Google Scholar 

Download references

Acknowledgments

We are indebted to Lucy-Marie Kempson, Lucy O’Farrell, Amy Smart, Erin Lynch, and Daniel Kitanov for assistance with data collection and animal husbandry. Macquarie University, the Linnean Society of New South Wales, and the Orthopterists’ Society provided funding to JC O’Hanlon. The authors are grateful to the Victorian Node of Metabolomics Australia, which is funded through Bioplatforms Australia Pty. Ltd., a National Collaborative Research Infrastructure Strategy (NCRIS), 5.1 Biomolecular platforms and informatics investment, and co-investment from the Victorian State Government and The University of Melbourne.

Author information

Affiliations

Authors

Corresponding author

Correspondence to James C. O’Hanlon.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Stanton, A.O., Dias, D.A. & O’Hanlon, J.C. Egg Dispersal in the Phasmatodea: Convergence in Chemical Signaling Strategies Between Plants and Animals?. J Chem Ecol 41, 689–695 (2015). https://doi.org/10.1007/s10886-015-0604-8

Download citation

Keywords

  • Myrmecochory
  • Eurycnema goliath
  • Rhytidoponera metallica
  • Elaiosome
  • Capitula