Ant mediated dispersal of spiny stick insect (Extatosoma tiaratum) eggs and Acacia longifolia seeds is ant-species dependent
Hannah R. Smart A B * , Nigel R. Andrew A and James C. O’Hanlon A CA Insect Ecology Lab, School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia.
B Hawkesbury Institute for the Environment, Western Sydney University, Locked Bag 1797, Penrith, NSW 2751, Australia.
C School of Science and Technology, University of New England, Armidale, NSW 2351, Australia.
Australian Journal of Zoology 70(4) 105-114 https://doi.org/10.1071/ZO22036
Submitted: 8 September 2022 Accepted: 16 February 2023 Published: 27 April 2023
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Myrmecochory is a widespread mutualism between angiosperm plants and ants, where seed dispersal is facilitated by a nutrient-rich appendage known as the elaiosome. Some species of phasmids (Phasmatodea) have convergently evolved an appendage, the egg capitulum, that is analogous to the elaiosome. Research into ant-mediated dispersal of phasmid eggs is limited. It is unknown whether there are species-specific interactions between ants and phasmid eggs, nor if this variation in ant species behaviour towards eggs parallels behaviour towards seeds. We observed the behaviour of five Australian ant species towards Extatosoma tiaratum eggs and Acacia longifolia seeds. We found that ant species show significant variation in the likelihood of dispersing phasmid eggs and plant seeds. Iridomyrmex purpureus removed the largest quantities of eggs and seeds. Rhytidoponera metallica also removed large amounts of seeds but less eggs. Three species did not remove any eggs but removed small amounts of seeds. We found a species-specific component to dispersal of phasmid eggs and seeds by ants, indicating that this mutualism may depend on partner identity and abundance. Although seeds and eggs have convergently evolved to exploit ant behaviours, they elicit different behaviours in certain ant species, highlighting the complex nature of this interaction.
Keywords: animal vectors, ants, coevolution, dispersal, eggs, mutualism, myrmecochory, phasmids, seeds.
References
Andersen, AN (1988). Dispersal distance as a benefit of myrmecochory. Oecologia 75, 507–511.| Dispersal distance as a benefit of myrmecochory.Crossref | GoogleScholarGoogle Scholar |
Bas, JM, Oliveras, J, and Gómez, C (2009). Myrmecochory and short-term seed fate in Rhamnus alaternus: ant species and seed characteristics. Acta Oecologica 35, 380–384.
| Myrmecochory and short-term seed fate in Rhamnus alaternus: ant species and seed characteristics.Crossref | GoogleScholarGoogle Scholar |
Beaumont, KP, Mackay, DA, and Whalen, MA (2013). Multiphase myrmecochory: the roles of different ant species and effects of fire. Oecologia 172, 791–803.
| Multiphase myrmecochory: the roles of different ant species and effects of fire.Crossref | GoogleScholarGoogle Scholar |
Beaumont, KP, Mackay, DA, and Whalen, MA (2018). The role of Rhytidoponera metallica (Hymenoptera, Formicidae) in facilitating post-fire seed germination of three ant-dispersed legume species. Austral Ecology 43, 128–138.
| The role of Rhytidoponera metallica (Hymenoptera, Formicidae) in facilitating post-fire seed germination of three ant-dispersed legume species.Crossref | GoogleScholarGoogle Scholar |
Berg, RY (1975). Myrmecochorous plants in Australia and their dispersal by ants. Australian Journal of Botany 23, 475–508.
| Myrmecochorous plants in Australia and their dispersal by ants.Crossref | GoogleScholarGoogle Scholar |
Bologna, A, Toffin, E, Detrain, C, and Campo, A (2017). An automated method for large-scale monitoring of seed dispersal by ants. Scientific Reports 7, 40143.
| An automated method for large-scale monitoring of seed dispersal by ants.Crossref | GoogleScholarGoogle Scholar |
Boulay, R, Coll-Toledano, J, Manzaneda, AJ, and Cerdá, X (2006). Geographic variations in seed dispersal by ants: are plant and seed traits decisive? Naturwissenschaften 94, 242–246.
| Geographic variations in seed dispersal by ants: are plant and seed traits decisive?Crossref | GoogleScholarGoogle Scholar |
Bradler S, Buckley TR (2018) Biodiversity of Phasmatodea. In ‘Insect biodiversity: science and society’. (Eds PH Adler, RG Foottit) (pp. 281–313). (John Wiley & Sons, Ltd) Available at https://onlinelibrary.wiley.com/doi/abs/10.1002/9781118945582.ch11
Brock, PD (2001). Studies on the Australasian stick-insect genus Extatosoma Gray (Phasmida: Phasmatidae: Tropoderinae: Extatosomatini). Journal of Orthoptera Research 10, 303–313.
| Studies on the Australasian stick-insect genus Extatosoma Gray (Phasmida: Phasmatidae: Tropoderinae: Extatosomatini).Crossref | GoogleScholarGoogle Scholar |
Brock, PD (2016). Extatosoma and ants. The Phasmid Study Group Newsletter 136, .
Brock PD, Hasenpusch JW (2009) ‘The complete field guide to stick and leaf insects of Australia.’ (CSIRO Publishing) Available at https://www.publish.csiro.au/book/6012 [Retrieved 11 August 2021]
Brock PD, Büscher T, Baker E (2022) Phasmida species file online. Version 5.0/5.0. Available at http://Phasmida.SpeciesFile.org [Retrieved 12 December 2022]
Canner, J, Dunn, R, Giladi, I, and Gross, K (2012). Redispersal of seeds by keystone ant augments the spread of common wildflowers. Acta Oecologica 40, 31–39.
| Redispersal of seeds by keystone ant augments the spread of common wildflowers.Crossref | GoogleScholarGoogle Scholar |
Christianini, AV, Mayhé-Nunes, AJ, and Oliveira, PS (2007). The role of ants in the removal of non-myrmecochorous diaspores and seed germination in a neotropical savanna. Journal of Tropical Ecology 23, 343–351.
| The role of ants in the removal of non-myrmecochorous diaspores and seed germination in a neotropical savanna.Crossref | GoogleScholarGoogle Scholar |
Clark, JT (1976). The capitulum of phasmid eggs (Insecta: Phasmida). Zoological Journal of the Linnean Society 59, 365–375.
| The capitulum of phasmid eggs (Insecta: Phasmida).Crossref | GoogleScholarGoogle Scholar |
Compton, SG, and Ware, AB (1991). Ants disperse the elaiosome-bearing eggs of an African stick insect. Psyche: A Journal of Entomology 98, 207–213.
| Ants disperse the elaiosome-bearing eggs of an African stick insect.Crossref | GoogleScholarGoogle Scholar |
Fischer, RC, Richter, A, Hadacek, F, and Mayer, V (2008). Chemical differences between seeds and elaiosomes indicate an adaptation to nutritional needs of ants. Oecologia 155, 539–547.
| Chemical differences between seeds and elaiosomes indicate an adaptation to nutritional needs of ants.Crossref | GoogleScholarGoogle Scholar |
Giladi, I (2006). Choosing benefits or partners: a review of the evidence for the evolution of myrmecochory. Oikos 112, 481–492.
| Choosing benefits or partners: a review of the evidence for the evolution of myrmecochory.Crossref | GoogleScholarGoogle Scholar |
Goldberg, J, Bresseel, J, Constant, J, Kneubühler, B, Leubner, F, Michalik, P, and Bradler, S (2015). Extreme convergence in egg-laying strategy across insect orders. Scientific Reports 5, 7825.
| Extreme convergence in egg-laying strategy across insect orders.Crossref | GoogleScholarGoogle Scholar |
Gove, AD, Majer, JD, and Dunn, RR (2007). A keystone ant species promotes seed dispersal in a “diffuse” mutualism. Oecologia 153, 687–697.
| A keystone ant species promotes seed dispersal in a “diffuse” mutualism.Crossref | GoogleScholarGoogle Scholar |
Gutierrez Rapalino, BP, and Domínguez Haydar, YDC (2017). Contribution of Pheidole fallax and Ectatomma ruidum (Hymenoptera: Formicidae) to the dispersion and germination of seeds in rehabilitated areas of the Cerrejón coal mine, Colombia. Revista de Biología Tropical 65, 575–587.
| Contribution of Pheidole fallax and Ectatomma ruidum (Hymenoptera: Formicidae) to the dispersion and germination of seeds in rehabilitated areas of the Cerrejón coal mine, Colombia.Crossref | GoogleScholarGoogle Scholar |
Gómez, C, and Espadaler, X (1998). Seed dispersal curve of a Mediterranean myrmecochore: influence of ant size and the distance to nests. Ecological Research 13, 347–354.
| Seed dispersal curve of a Mediterranean myrmecochore: influence of ant size and the distance to nests.Crossref | GoogleScholarGoogle Scholar |
Gómez, C, Espadaler, X, and Bas, JM (2005). Ant behaviour and seed morphology: a missing link of myrmecochory. Oecologia 146, 244–246.
| Ant behaviour and seed morphology: a missing link of myrmecochory.Crossref | GoogleScholarGoogle Scholar |
Heterick, BE, and Shattuck, S (2011). Revision of the ant genus Iridomyrmex (Hymenoptera: Formicidae). Zootaxa 2845, 1–175.
| Revision of the ant genus Iridomyrmex (Hymenoptera: Formicidae).Crossref | GoogleScholarGoogle Scholar |
Hill, SJ, Silcocks, SC, and Andrew, NR (2020). Impacts of temperature on metabolic rates of adult Extatosoma tiaratum reared on different host plant species. Physiological Entomology 45, 7–15.
| Impacts of temperature on metabolic rates of adult Extatosoma tiaratum reared on different host plant species.Crossref | GoogleScholarGoogle Scholar |
Hughes, L, and Westoby, M (1990). Removal rates of seeds adapted for dispersal by ants. Ecology 71, 138–148.
| Removal rates of seeds adapted for dispersal by ants.Crossref | GoogleScholarGoogle Scholar |
Hughes, L, and Westoby, M (1992a). Capitula on stick insect eggs and elaiosomes on seeds: convergent adaptations for burial by ants. Functional Ecology 6, 642–648.
| Capitula on stick insect eggs and elaiosomes on seeds: convergent adaptations for burial by ants.Crossref | GoogleScholarGoogle Scholar |
Hughes, L, and Westoby, M (1992b). Effect of diaspore characteristics on removal of seeds adapted for dispersal by ants. Ecology 73, 1300–1312.
| Effect of diaspore characteristics on removal of seeds adapted for dispersal by ants.Crossref | GoogleScholarGoogle Scholar |
Hughes, L, Westoby, M, and Jurado, E (1994). Convergence of elaiosomes and insect prey: evidence from ant foraging behaviour and fatty acid composition. Functional Ecology 8, 358–365.
| Convergence of elaiosomes and insect prey: evidence from ant foraging behaviour and fatty acid composition.Crossref | GoogleScholarGoogle Scholar |
Kaspari, M (1996). Worker size and seed size selection by harvester ants in a neotropical forest. Oecologia 105, 397–404.
| Worker size and seed size selection by harvester ants in a neotropical forest.Crossref | GoogleScholarGoogle Scholar |
Key KHL (1991) Phasmatodea (stick-insects). In ‘The insects of Australia: a textbook for students and research workers, Vol. 1, Issue v. 2’. 2nd edn. (Ed. CSIRO) pp. 394–404. (Melbourne University Press). Available at https://books.google.com.au/books?id=xQyJnQAACAAJ
Kodela PG (2005) PlantNET – FloraOnline– Acacia longifolia. Available at https://plantnet.rbgsyd.nsw.gov.au/cgi-bin/NSWfl.pl?page=nswfl&lvl=sp&name=Acacia~longifolia
Leal, IR, Wirth, R, and Tabarelli, M (2007). Seed dispersal by ants in the semi-arid Caatinga of north-east Brazil. Annals of Botany 99, 885–894.
| Seed dispersal by ants in the semi-arid Caatinga of north-east Brazil.Crossref | GoogleScholarGoogle Scholar |
Leal, LC, Neto, MCL, de Oliveira, AFM, Andersen, AN, and Leal, IR (2014). Myrmecochores can target high-quality disperser ants: variation in elaiosome traits and ant preferences for myrmecochorous Euphorbiaceae n Brazilian Caatinga. Oecologia 174, 493–500.
| Myrmecochores can target high-quality disperser ants: variation in elaiosome traits and ant preferences for myrmecochorous Euphorbiaceae n Brazilian Caatinga.Crossref | GoogleScholarGoogle Scholar |
Lengyel, S, Gove, AD, Latimer, AM, Majer, JD, and Dunn, RR (2010). Convergent evolution of seed dispersal by ants, and phylogeny and biogeography in flowering plants: a global survey. Perspectives in Plant Ecology, Evolution and Systematics 12, 43–55.
| Convergent evolution of seed dispersal by ants, and phylogeny and biogeography in flowering plants: a global survey.Crossref | GoogleScholarGoogle Scholar |
Lubertazzi, D, Aliberti Lubertazzi, MA, McCoy, N, Gove, AD, Majer, JD, and Dunn, RR (2010). The ecology of a keystone seed disperser, the ant Rhytidoponera violacea. Journal of Insect Science 10, 158.
| The ecology of a keystone seed disperser, the ant Rhytidoponera violacea.Crossref | GoogleScholarGoogle Scholar |
McArthur AJ (2007) A key to Camponotus Mayr of Australia. In ‘Advances in ant systematics (Hymenoptera: Formicidae): homage to E. O. Wilson – 50 years of contributions’. (Eds RR Snelling, BL Fisher, PS Ward) pp. 290–351. (Memoirs of the American Entomological Institute 80)
Middleton, EJT, Reid, CR, Mann, RP, and Latty, T (2018). Social and private information influence the decision making of Australian meat ants (Iridomyrmex purpureus). Insectes Sociaux 65, 649–656.
| Social and private information influence the decision making of Australian meat ants (Iridomyrmex purpureus).Crossref | GoogleScholarGoogle Scholar |
Miller, CN, Whitehead, SR, and Kwit, C (2020). Effects of seed morphology and elaiosome chemical composition on attractiveness of five Trillium species to seed-dispersing ants. Ecology and Evolution 10, 2860–2873.
| Effects of seed morphology and elaiosome chemical composition on attractiveness of five Trillium species to seed-dispersing ants.Crossref | GoogleScholarGoogle Scholar |
Ness, JH, Bronstein, JL, Andersen, AN, and Holland, JN (2004). Ant body size predicts dispersal distance of ant-adapted seeds: implications of small-ant invasions. Ecology 85, 1244–1250.
| Ant body size predicts dispersal distance of ant-adapted seeds: implications of small-ant invasions.Crossref | GoogleScholarGoogle Scholar |
Ness, JH, Morin, DF, and Giladi, I (2009). Uncommon specialization in a mutualism between a temperate herbaceous plant guild and an ant: are Aphaenogaster ants keystone mutualists? Oikos 118, 1793–1804.
| Uncommon specialization in a mutualism between a temperate herbaceous plant guild and an ant: are Aphaenogaster ants keystone mutualists?Crossref | GoogleScholarGoogle Scholar |
O’Hanlon, JC, Hill, SJ, and Andrew, NR (2019). Using devitalised seeds in myrmecological research. Austral Entomology 58, 805–809.
| Using devitalised seeds in myrmecological research.Crossref | GoogleScholarGoogle Scholar |
O’Hanlon, JC, Jones, BR, and Bulbert, MW (2020). The dynamic eggs of the Phasmatodea and their apparent convergence with plants. The Science of Nature 107, 34.
| The dynamic eggs of the Phasmatodea and their apparent convergence with plants.Crossref | GoogleScholarGoogle Scholar |
Pettit, L, and Latty, T (2016). Greenhead ants Rhytidoponera metallica make trade-offs between food temperature and food concentration. Ecological Entomology 41, .
| Greenhead ants Rhytidoponera metallica make trade-offs between food temperature and food concentration.Crossref | GoogleScholarGoogle Scholar |
Pfeiffer, M, Huttenlocher, H, and Ayasse, M (2010). Myrmecochorous plants use chemical mimicry to cheat seed-dispersing ants. Functional Ecology 24, 545–555.
| Myrmecochorous plants use chemical mimicry to cheat seed-dispersing ants.Crossref | GoogleScholarGoogle Scholar |
Reifenrath, K, Becker, C, and Poethke, HJ (2012). Diaspore trait preferences of dispersing ants. Journal of Chemical Ecology 38, 1093–1104.
| Diaspore trait preferences of dispersing ants.Crossref | GoogleScholarGoogle Scholar |
Robertson, JA, Bradler, S, and Whiting, MF (2018). Evolution of oviposition techniques in stick and leaf insects (Phasmatodea). Frontiers in Ecology and Evolution 6, 216.
| Evolution of oviposition techniques in stick and leaf insects (Phasmatodea).Crossref | GoogleScholarGoogle Scholar |
Rocha, MLC, Cristaldo, PF, Cruz, JS, Sacramento, JJM, Ferreira, DV, and Araújo, APA (2018). Ants associated with Turnera subulata (Turneraceae): elaiosome attraction, seed dispersion and germination. Neotropical Entomology 47, 750–756.
| Ants associated with Turnera subulata (Turneraceae): elaiosome attraction, seed dispersion and germination.Crossref | GoogleScholarGoogle Scholar |
RStudio Team (2020) RStudio: Integrated Development for R. RStudio, PBC, Boston, MA. Available at http://www.rstudio.com/
Schneider, A, and Elgar, MA (2010). Facultative sex and reproductive strategies in response to male availability in the spiny stick insect, Extatosoma tiaratum. Australian Journal of Zoology 58, 228–233.
| Facultative sex and reproductive strategies in response to male availability in the spiny stick insect, Extatosoma tiaratum.Crossref | GoogleScholarGoogle Scholar |
Shattuck S (1999) ‘Australian ants.’ (CSIRO Publishing) Available at https://www.publish.csiro.au/book/503
Shelomi, M (2011). Phasmid eggs do not survive digestion by quails and chickens. Journal of Orthoptera Research 20, 159–162.
| Phasmid eggs do not survive digestion by quails and chickens.Crossref | GoogleScholarGoogle Scholar |
Stanton, AO, Dias, DA, and O’Hanlon, JC (2015). Egg dispersal in the Phasmatodea: convergence in chemical signaling strategies between plants and animals? Journal of Chemical Ecology 41, 689–695.
| Egg dispersal in the Phasmatodea: convergence in chemical signaling strategies between plants and animals?Crossref | GoogleScholarGoogle Scholar |
Tanaka, K, Ogata, K, Mukai, H, Yamawo, A, and Tokuda, M (2015). Adaptive advantage of myrmecochory in the ant-dispersed herb Lamium amplexicaule (Lamiaceae): predation avoidance through the deterrence of post-dispersal seed predators. PLoS ONE 10, e0133677.
| Adaptive advantage of myrmecochory in the ant-dispersed herb Lamium amplexicaule (Lamiaceae): predation avoidance through the deterrence of post-dispersal seed predators.Crossref | GoogleScholarGoogle Scholar |
Thomas, ML, and Framenau, VW (2005). Foraging decisions of individual workers vary with colony size in the greenhead ant Rhytidoponera metallica (Formicidae, Ectatomminae). Insectes Sociaux 52, 26–30.
| Foraging decisions of individual workers vary with colony size in the greenhead ant Rhytidoponera metallica (Formicidae, Ectatomminae).Crossref | GoogleScholarGoogle Scholar |
Turner, KM, and Frederickson, ME (2013). Signals can trump rewards in attracting seed-dispersing ants. PLOS ONE 8, e71871.
| Signals can trump rewards in attracting seed-dispersing ants.Crossref | GoogleScholarGoogle Scholar |
van Wilgenburg, EV, and Elgar, MA (2007). Colony structure and spatial distribution of food resources in the polydomous meat ant Iridomyrmex purpureus. Insectes Sociaux 54, 5–10.
| Colony structure and spatial distribution of food resources in the polydomous meat ant Iridomyrmex purpureus.Crossref | GoogleScholarGoogle Scholar |
Wickham H (2016) ‘Ggplot2.’ 2nd edn. (Springer)
Windsor, DM, Trapnell, DW, and Amat, G (1996). The egg capitulum of a neotropical walkingstick, Calynda bicuspis, induces aboveground egg dispersal by the ponerine ant, Ectatomma ruidum. Journal of Insect Behavior 9, 353–367.
| The egg capitulum of a neotropical walkingstick, Calynda bicuspis, induces aboveground egg dispersal by the ponerine ant, Ectatomma ruidum.Crossref | GoogleScholarGoogle Scholar |
Yamada, A, Bresseel, J, Chen, Z, Nguyen, AD, and Eguchi, K (2021). Deposition of phasmid eggs (Phasmatodea) in the nests of Acanthomyrmex glabfemoralis Zhou & Zheng, 1997 (Hymenoptera: Formicidae: Myrmicinae). Taiwania 66, 267–272.
| Deposition of phasmid eggs (Phasmatodea) in the nests of Acanthomyrmex glabfemoralis Zhou & Zheng, 1997 (Hymenoptera: Formicidae: Myrmicinae).Crossref | GoogleScholarGoogle Scholar |