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Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Myrmecochory in Lepidosperma (Cyperaceae): perianth members provide a lipid-rich reward for ants

George T. Plunkett https://orcid.org/0000-0002-1413-665X A * , Nicolas J. Sadgrove B D , Boyd R. Wright A , Karen L. Wilson C and Jeremy J. Bruhl A
+ Author Affiliations
- Author Affiliations

A Botany, School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia.

B Pharmaceutical and Nutraceutical Group, School of Science and Technology, University of New England, Armidale, NSW 2351, Australia.

C National Herbarium of New South Wales, Royal Botanic Gardens and Domain Trust, Sydney, Mrs Macquaries Road, Sydney, NSW 2000, Australia.

D Present address: Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, UK.

* Correspondence to: george.t.plunkett@gmail.com

Handling Editor: Lynda Prior

Australian Journal of Botany 70(1) 1-12 https://doi.org/10.1071/BT21023
Submitted: 20 February 2021  Accepted: 24 August 2021   Published: 16 November 2021

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

The diaspores of Lepidosperma Labill. (Cyperaceae) have thickened perianth members persistent at the base of the fruit, which are generally assumed to form a unique type of elaiosome but this assumption has not been tested rigorously. We tested whether the perianth provides a lipid-rich food reward and improves diaspore removal by ants in three species of Lepidosperma. We measured (i) the lipid and fatty acid composition of the fruit and perianth of two species of Lepidosperma, and of the seed and aril of two species of Acacia (known myrmecochores), (ii) the relative attractiveness to ants of the perianth in three species of Lepidosperma, and (iii) the relative attractiveness to ants of the diaspores of the same species of Lepidosperma compared with the two species of Acacia. We found that (i) Lepidosperma diaspores show traits consistent with myrmecochory, particularly the high lipid content (∼12–60%) and fatty acid profile of perianth material, (ii) isolated perianth members were removed in greater numbers over all times than were diaspores only (i.e. with perianth removed) in two species of Lepidosperma (n = 100, P = 0.035 and 0.047), whereas the difference was equivocal in the third species (n = 100, P > 0.05), and (iii) Lepidosperma and Acacia diaspores were removed in similar numbers over time (n = 100, P > 0.5). Seven species of diaspore-removing ant were observed, with Rhytidoponera metallica accounting for ∼50% of observed removals. We conclude that the perianth members of Lepidosperma are an elaiosome that provides a lipid-rich food reward.

Keywords: elaiosome, fatty acids, GC-MS, lipids, Rhytidoponera.


References

Adams RP (2007) ‘Identification of essential oil components by gas chromatography/mass spectrometry. Vol. 456.’ (Allured Publishing Corporation: Carol Stream, IL, USA)

Andersen AN (1988) Dispersal distance as a benefit of myrmecochory. Oecologia 75, 507–511.
Dispersal distance as a benefit of myrmecochory.Crossref | GoogleScholarGoogle Scholar | 28312423PubMed |

Anjos DV, Andersen AN, Carvalho RL, Sousa RMF, Del-Claro K (2020) Switching roles from antagonist to mutualist: a harvester ant as a key seed disperser of a myrmecochorous plant. Ecological Entomology 45, 1063–1070.
Switching roles from antagonist to mutualist: a harvester ant as a key seed disperser of a myrmecochorous plant.Crossref | GoogleScholarGoogle Scholar |

Arnan X, Retana J, Rodrigo A, Cerdá X (2010) Foraging behaviour of harvesting ants determines seed removal and dispersal. Insectes Sociaux 57, 421–430.
Foraging behaviour of harvesting ants determines seed removal and dispersal.Crossref | GoogleScholarGoogle Scholar |

Bannon CD, Craske JD, Hai NT, Harper NL, O’Rourke KL (1982) Analysis of fatty acid methyl esters with high accuracy and reliability: II. Methylation of fats and oils with boron trifluoride-methanol. Journal of Chromatography A 247, 63–69.
Analysis of fatty acid methyl esters with high accuracy and reliability: II. Methylation of fats and oils with boron trifluoride-methanol.Crossref | GoogleScholarGoogle Scholar |

Barrett RL (2011) Systematic studies in Cyperaceae tribe Schoeneae: Lepidosperma and allied genera. PhD thesis, The University of Western Australia, Perth, WA, Australia.

Barrett RL (2013) Ecological importance of sedges: a survey of the Australasian Cyperaceae genus Lepidosperma. Annals of Botany 111, 499–529.
Ecological importance of sedges: a survey of the Australasian Cyperaceae genus Lepidosperma.Crossref | GoogleScholarGoogle Scholar | 23378523PubMed |

Barton K (1994) The perianth and dispersal in Cyperaceae. MLit thesis, The University of New England, Armidale, NSW, Australia.

Bas JM, Oliveras J, 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 |

Beattie AJ (1985) ‘The evolution of ant–plant mutualisms.’ (Cambridge University Press: New York, NY, USA)

Beattie AJ, Hughes L (2002) Ant–plant interactions. In ‘Plant–animal interactions: an evolutionary approach’. (Eds CM Herrera, O Pellmyr) pp. 211–235. (Blackwell: Oxford, UK)

Bebawi FF, Campbell SD (2004) Interactions between meat ants (Iridomyrmex spadius) and bellyache bush (Jatropha gossypiifolia. Australian Journal of Experimental Agriculture 44, 1157–1164.
Interactions between meat ants (Iridomyrmex spadius) and bellyache bush (Jatropha gossypiifolia.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 |

Bond WJ, Slingsby P (1983) Seed dispersal by ants in shrublands of the Cape Province and its evolutionary implication. South African Journal of Science 79, 231–233.
Seed dispersal by ants in shrublands of the Cape Province and its evolutionary implication.Crossref | GoogleScholarGoogle Scholar |

Bond WJ, Yeaton R, Stock WD (1991) Myrmecochory in Cape fynbos. In ‘Ant–plant interactions’. (Eds CR Huxley, DF Cutler) pp. 448–462. (Oxford University Press: New York, NY, USA)

Boulay R, Carro F, Soriguer RC, Cerda X (2007) Synchrony between fruit maturation and effective dispersers’ foraging activity increases seed protection against seed predators. Proceedings of the Royal Society – B. Biological Sciences 274, 2515–2322.
Synchrony between fruit maturation and effective dispersers’ foraging activity increases seed protection against seed predators.Crossref | GoogleScholarGoogle Scholar |

Brew CR, O’Dowd DJ, Rae ID (1989) Seed dispersal by ants: behaviour-releasing compounds in elaiosomes. Oecologia 80, 490–497.
Seed dispersal by ants: behaviour-releasing compounds in elaiosomes.Crossref | GoogleScholarGoogle Scholar | 28312833PubMed |

Bruhl JJ (1991) Comparative development of some taxonomically critical floral inflorescence features in Cyperaceae. Australian Journal of Botany 39, 119–127.
Comparative development of some taxonomically critical floral inflorescence features in Cyperaceae.Crossref | GoogleScholarGoogle Scholar |

Clark RE, King JR (2012) The ant, Aphaenogaster picea, benefits from plant elaiosomes when insect prey is scarce. Environmental Entomology 41, 1405–1408.
The ant, Aphaenogaster picea, benefits from plant elaiosomes when insect prey is scarce.Crossref | GoogleScholarGoogle Scholar | 23321086PubMed |

Davidson DW, Morton SR (1981) Myrmecochory in some plants (F. chenopodiaceae) of the Australian arid zone. Oecologia 50, 357–366.
Myrmecochory in some plants (F. chenopodiaceae) of the Australian arid zone.Crossref | GoogleScholarGoogle Scholar | 28309054PubMed |

Drake WE (1981) Ant-seed interaction in dry sclerophyll forest on North Stradbroke Island, Queensland. Australian Journal of Botany 29, 293–309.
Ant-seed interaction in dry sclerophyll forest on North Stradbroke Island, Queensland.Crossref | GoogleScholarGoogle Scholar |

Dunn RR, Gove AD, Barraclough TG, Givnish TJ, Majer JD (2007) Convergent evolution of an ant-plant mutualism across plant families, continents, and time. Evolutionary Ecology Research 9, 1349–1362.

Edwards W, Dunlop M, Rodgerson L (2006) The evolution of rewards: seed dispersal, seed size and elaiosome size. Journal of Ecology 94, 687–694.
The evolution of rewards: seed dispersal, seed size and elaiosome size.Crossref | GoogleScholarGoogle Scholar |

Fischer RC, Richter A, Hadacek F, 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 | 18095003PubMed |

Fournier DA, Skaug HJ, Ancheta J, Ianelli J, Magnusson A, Maunder M, Nielsen A, Sibert J (2012) AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optimization Methods and Software 27, 233–249.
AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models.Crossref | GoogleScholarGoogle Scholar |

Gaddy LL (1986) Twelve new ant-dispersed species from the southern Appalachians. Bulletin of the Torrey Botanical Club 113, 247–251.
Twelve new ant-dispersed species from the southern Appalachians.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 |

Gómez C, Espadaler X (2013) An update of the world survey of myrmecochorous dispersal distances. Ecography 36, 1193–1201.
An update of the world survey of myrmecochorous dispersal distances.Crossref | GoogleScholarGoogle Scholar |

Gómez C, Espadaler X, 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 | 16044350PubMed |

Gove AD, Majer JD, 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 | 17534665PubMed |

Handel SN (1976) Dispersal ecology of Carex pedunculata (Cyperaceae), a new North American myrmecochore. American Journal of Botany 63, 1071–1079.
Dispersal ecology of Carex pedunculata (Cyperaceae), a new North American myrmecochore.Crossref | GoogleScholarGoogle Scholar |

Hughes L, 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, Westoby M (1992a) 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 (1992b) Fate of seeds adapted for dispersal by ants in Australian sclerophyll vegetation. Ecology 73, 1285–1299.
Fate of seeds adapted for dispersal by ants in Australian sclerophyll vegetation.Crossref | GoogleScholarGoogle Scholar |

Hughes L, Westoby M, Jurado E (1994) Convergence of elaiosomes and insect prey: evidence from ant foraging behavior and fatty acid composition. Functional Ecology 8, 358–365.
Convergence of elaiosomes and insect prey: evidence from ant foraging behavior and fatty acid composition.Crossref | GoogleScholarGoogle Scholar |

Kjellsson G (1985) Seed fate in a population of Carex pilulifera L. I. Seed dispersal and ant-seed mutualism. Oecologia 67, 416–423.
Seed fate in a population of Carex pilulifera L. I. Seed dispersal and ant-seed mutualism.Crossref | GoogleScholarGoogle Scholar | 28311577PubMed |

Kjellsson G (1991) Seed fate in an ant-dispersed sedge, Carex pilulifera L.: recruitment and seedling survival in tests of models for spatial dispersion. Oecologia 88, 435–443.
Seed fate in an ant-dispersed sedge, Carex pilulifera L.: recruitment and seedling survival in tests of models for spatial dispersion.Crossref | GoogleScholarGoogle Scholar | 28313808PubMed |

Kodym A, Turner S, Delpratt J (2010) In situ seed development and in vitro regeneration of three difficult-to-propagate Lepidosperma species (Cyperaceae). Australian Journal of Botany 58, 107–114.
In situ seed development and in vitro regeneration of three difficult-to-propagate Lepidosperma species (Cyperaceae).Crossref | GoogleScholarGoogle Scholar |

Leal LC, Neto MCL, de Oliveira AFM, Andersen AN, Leal IR (2014) Myrmecochores can target high-quality disperser ants: variation in elaiosome traits and ant preferences for myrmecochorous Euphorbiaceae in Brazilian Caatinga. Oecologia 174, 493–500.
Myrmecochores can target high-quality disperser ants: variation in elaiosome traits and ant preferences for myrmecochorous Euphorbiaceae in Brazilian Caatinga.Crossref | GoogleScholarGoogle Scholar | 24085639PubMed |

Lengyel S, Gove AD, Latimer AM, Majer JD, Dunn RR (2009) Ants sow the seeds of global diversification in flowering plants. PLoS One 4, e5480
Ants sow the seeds of global diversification in flowering plants.Crossref | GoogleScholarGoogle Scholar | 19436714PubMed |

Lengyel S, Gove AD, Latimer AM, Majer JD, 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 |

Lenth RV (2016) Least-squares means: the R package lsmeans. Journal of Statistical Software 69, 1–33.
Least-squares means: the R package lsmeans.Crossref | GoogleScholarGoogle Scholar |

Lisci M, Bianchini M, Pacini E (1996) Structure and function of the elaiosome in some angiosperm species. Flora 191, 131–141.
Structure and function of the elaiosome in some angiosperm species.Crossref | GoogleScholarGoogle Scholar |

Mayer V, Olzant SM, Fischer RC (2005) Myrmecochorous seed dispersal in temperate regions. In ‘Seed fate: predation, dispersal, and seedling establishment’. (Eds PM Forget, JE Lambert, PE Hulme, SB Vander Wall) pp. 175–195. (CAB International Publishing: Wallingford, UK)

Milewski AV, Bond WJ (1982) Convergence of myrmecochory in mediteranean Australia and South Africa. In ‘Ant–plant interactions in Australia’. (Ed. RC Buckley) pp. 75–87. (Dr W. Junk Publishers: The Hague, Netherlands)

Mills KR, Bruhl JJ (2012) Myrmecochory is not all or nothing: comparative assessment of ant dispersal in a clonal sedge. In ‘Program and Abstracts: Australasian Systematic Botany Society Conference 2012: Local knowledge, global delivery’, 23–28 September 2012, Perth, WA, Australia. Abstract, p. 36. (University of New England: Armidale, NSW, Australia) Available at https://library.dbca.wa.gov.au/static/FullTextFiles/025673.pdf

O’Dowd DJ, Gill M (1986) Seed dispersal syndromes in Australian Acacia. In ‘Seed dispersal’. (Ed. DR Murray) pp. 87–121. (Academic Press: Sydney, NSW, Australia)

Ohkawara K, Higashi S (1994) Relative importance of ballistic and ant dispersal in two diplochorous Viola species (Violaceae). Oecologia 100, 135–140.
Relative importance of ballistic and ant dispersal in two diplochorous Viola species (Violaceae).Crossref | GoogleScholarGoogle Scholar | 28307037PubMed |

Pfeiffer M, Huttenlocher H, 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 |

Pierce SM, Cowling RM (1991) Dynamics of soil-stored seed banks of six shrubs in fire-prone dune fynbos. Journal of Ecology 79, 731–747.
Dynamics of soil-stored seed banks of six shrubs in fire-prone dune fynbos.Crossref | GoogleScholarGoogle Scholar |

Plunkett GT, Wilson KL, Bruhl JJ (2013) Sedges in the mist: a new species of Lepidosperma (Cyperaceae, Schoeneae) from the mountains of Tasmania. PhytoKeys 28, 19–59.
Sedges in the mist: a new species of Lepidosperma (Cyperaceae, Schoeneae) from the mountains of Tasmania.Crossref | GoogleScholarGoogle Scholar |

Prior KM, Saxena K, Frederickson ME (2014) Seed handling behaviours of native and invasive seed-dispersing ants differentially influence seedling emergence in an introduced plant. Ecological Entomology 39, 66–74.
Seed handling behaviours of native and invasive seed-dispersing ants differentially influence seedling emergence in an introduced plant.Crossref | GoogleScholarGoogle Scholar |

Reifenrath K, Becker C, 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 | 22903746PubMed |

Rice B, Westoby M (1981) Myrmecochory in sclerophyll vegetation of West Head, New South Wales. Australian Ecology 6, 291–298.
Myrmecochory in sclerophyll vegetation of West Head, New South Wales.Crossref | GoogleScholarGoogle Scholar |

Rico-Gray V, Oliveira PS (2007) ‘The ecology and evolution of ant-plant interactions.’ (University of Chicago Press: Chicago, IL, USA)

Rodgerson ML (1995) Seed fate and distribution of ant-dispersed plant species in Australia. PhD thesis, Macquarie University, Sydney, NSW, Australia.

Slingsby P, Bond W (1981) Ants – friends of the fynbos. Veld and Flora 67, 39–45.
Ants – friends of the fynbos.Crossref | GoogleScholarGoogle Scholar |

Stanton AO, Dias DA, O’Hanlon JC (2015) Egg dispersal in the Phasmatodea: convergence in chemical signalling strategies between plants and animals? Journal of Chemical Ecology 41, 689–695.
Egg dispersal in the Phasmatodea: convergence in chemical signalling strategies between plants and animals?Crossref | GoogleScholarGoogle Scholar | 26245262PubMed |

Tanaka K, Yamawo A, Yano O (2015) Seed dispersal by ants in Carex oxyandra var. oxyandra (Cyperaceae) from Japan. Journal of Japanese Botany 90, 129–133.

Taylor J (2010) The role of ants as seed dispersers in the Warkworth Sands Woodland, and their use as bioindicators of ecosystem restoration success. BSc(Hons) thesis. The University of New England, Armidale, NSW, Australia.

Thomas ML, Frameneau 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 |

Thomson FJ, Moles AT, Auld TD, Ramp D, Ren S, Kingsford RT (2010) Chasing the unknown: predicting seed dispersal mechanisms from plant traits. Journal of Ecology 98, 1310–1318.
Chasing the unknown: predicting seed dispersal mechanisms from plant traits.Crossref | GoogleScholarGoogle Scholar |

Turner SR (2013) Seed ecology of Lepidosperma scabrum (Cyperaceae), a dryland sedge from Western Australia with physiological seed dormancy. Australian Journal of Botany 61, 643–653.
Seed ecology of Lepidosperma scabrum (Cyperaceae), a dryland sedge from Western Australia with physiological seed dormancy.Crossref | GoogleScholarGoogle Scholar |

Warren RJ, Giladi I (2014) Ant-mediated seed dispersal: a few ant species (Hymenoptera: Formicidae) benefit many plants. Myrmecological News 20, 129–140.

Westoby M, Rice B, Shelley JM, Haig D, Kohen JL (1982) Plants’ use of ants for dispersal at West Head, New South Wales. In ‘Ant–plant interactions in Australia’. (Ed. RC Buckley) pp. 75–87. (Dr W. Junk Publishers: The Hague, Netherlands)

Wilson KL (1993) Cyperaceae. In ‘Flora of New South Wales. Vol. 4’. (Ed. G. Harden) pp. 293–396. (University of New South Wales Press: Sydney, NSW, Australia)

Wilson KL (1994a) Cyperaceae. In ‘Flora of Victoria. Vol. 2. Ferns and allied plants, conifers and monocotyledons’. (Eds NG Walsh, TJ Entwisle) pp. 238–356. (Inkata Press: Melbourne, Vic., Australia)

Wilson KL (1994) New taxa and combinations in the family Cyperaceae in eastern Australia. Telopea 5, 589–625.
New taxa and combinations in the family Cyperaceae in eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Wolff A, Debussche M (1999) Ants as seed dispersers in a Mediterranean old-field succession. Oikos 84, 443–452.
Ants as seed dispersers in a Mediterranean old-field succession.Crossref | GoogleScholarGoogle Scholar |

Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) ‘Mixed effects models and extensions in ecology with R.’ (Springer: New York, NY, USA)

Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1, 3–14.
A protocol for data exploration to avoid common statistical problems.Crossref | GoogleScholarGoogle Scholar |