Skip to main content
SpringerLink
Log in

The critical role of ants in the extensive dispersal of Acacia seeds revealed by genetic parentage assignment

  • Plant-microbe-animal interactions - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Ants are prominent seed dispersal agents in many ecosystems, and dispersal distances are small in comparison with vertebrate dispersal agents. However, the distance and distribution of ant-mediated dispersal in arid/semi-arid environments remains poorly explored. We used microsatellite markers and parentage assignment to quantify the distance and distribution of dispersed seeds of Acacia karina, retrieved from the middens of Iridomyrmex agilis and Melophorus turneri perthensis. From parentage assignment, we could not distinguish the maternal from each parent pair assigned to each seed, so we applied two approaches to estimate dispersal distances, one conservative (CONS), where the parent closest to the ant midden was considered to be maternal, and the second where both parents were deemed equally likely (EL) to be maternal, and used both distances. Parentage was assigned to 124 seeds from eight middens. Maximum seed dispersal distances detected were 417 m (CONS) and 423 m (EL), more than double the estimated global maximum. Mean seed dispersal distances of 40 m (±5.8 SE) (CONS) and 79 m (±6.4 SE) (EL) exceeded the published global average of 2.24 m (±7.19 SD) by at least one order of magnitude. For both approaches and both ant species, seed dispersal was predominantly (44–84 % of all seeds) within 50 m from the maternal source, with fewer dispersal events at longer distances. Ants in this semi-arid environment have demonstrated a greater capacity to disperse seeds than estimated elsewhere, which highlights their important role in this system, and suggests significant novel ecological and evolutionary consequences for myrmecochorous species in arid/semi-arid Australia.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

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

    Article  Google Scholar 

  • Auld TD (1986) Population dynamics of the shrub Acacia suavelons (Sm.) Willd.: dispersal and the dynamics of the soil seed bank. Aust J Ecol 11:235–254

    Article  Google Scholar 

  • Auld TD (1997) Ecology of the Fabaceae in the Sydney region: fire, ants and the soil seedbank. Cunninghamia 4:531–551

    Google Scholar 

  • Beattie AJ, Culver DC (1983) The nest chemistry of two seed-dispersing ant species. Oecologia 56:99–103

    Article  Google Scholar 

  • Beaumont KP, Mackay DA, Whalen MA (2013) Multiphase myrmecochory: the roles of different ant species and effects of fire. Oecologia 172:791–803

    Article  PubMed  Google Scholar 

  • Bond WJ, Stock WD (1989) The costs of leaving home: ants disperse myrmecochorous seeds to low nutrient sites. Oecologia 81:412–417

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bronstein JL, Alarcon R, Geber M (2006) The evolution of plant–insect mutualisms. New Phytol 172:412–428

    Article  PubMed  Google Scholar 

  • Clobert J, Danchin E, Dhondt AA, Nichols JD (eds) (2001) Dispersal. Oxford University Press, Oxford

    Google Scholar 

  • 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 

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

    Article  Google Scholar 

  • Gibson MR, Richardson DM, Marchante E, Marchante H, Rodger JG, Stone GN, Byrne M, Fuentes-Ramírez A, George N, Harris C et al (2011) Reproductive biology of Australian acacias: important mediator of invasiveness? Divers Distrib 17:911–933

    Article  Google Scholar 

  • Giladi I (2006) Choosing benefits or partners: a review of the evidence for the evolution of myrmecochory. Oikos 112:481–492. doi:10.1111/j.0030-1299.2006.14258.x

    Article  Google Scholar 

  • Gómez C, Espadaler X (1998) Myrmecochorous dispersal distances: a world survey. J Biogeogr 25:573–580. doi:10.1046/j.1365-2699.1998.2530573.x

    Article  Google Scholar 

  • Gómez C, Espadaler X (2013) An update of the world survey of myrmecochorous dispersal distances. Ecography 36:1193–1201. doi:10.1111/j.1600-0587.2013.00289.x

    Article  Google Scholar 

  • Gove AD, Majer JD, Dunn RD (2007) A keystone ant species promotes seed dispersal in a diffuse mutualism. Oecologia 153:687–697

    Article  PubMed  Google Scholar 

  • Hamrick JL, Trapnell DW (2011) Using population genetic analyses to understand seed dispersal patterns. Acta Oecologia 37:641–649

    Article  Google Scholar 

  • Hanski I, Saccheri I (2006) Molecular-level variation affects population growth in a butterfly metapopulation. PLoS Biol 4:e129. doi:10.1371/journal.pbio.0040129

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Hardesty BD, Hubbell SP, Bermingham E (2006) Genetic evidence of frequent longdistance recruitment in a vertebrate dispersed tree. Ecol Lett 9:516–525

    Article  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDI: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620. doi:10.1046/j.1471-8286.2002.00305.x

    Article  Google Scholar 

  • He T, Krauss SL, Lamont BB, Miller BP, Enright NJ (2004) Long-distance seed dispersal in a metapopulation of Banksia hookeriana inferred from a population allocation analysis of amplified fragment length polymorphism data. Mol Ecol 13:1099–1109

    Article  CAS  PubMed  Google Scholar 

  • He TH, Lamont BB, Krauss SL, Enright NJ, Miller BP, Gove AD (2009) Ants cannot account for interpopulation dispersal of the arillate pea Daviesia triflora. New Phytol 181:725–733. doi:10.1111/j.1469-8137.2008.02686.x

    Article  PubMed  Google Scholar 

  • Heithaus ER (1981) Seed predation by rodents on 3 ant-dispersed plants. Ecology 62:136–145

    Article  Google Scholar 

  • Heterick BE (2009) A guide to the ants of south-western Australia. Records of the Western Australian Museum, Supplement 79, 205 pp

  • Heterick BE, Shattuck S (2011) Revision of the ant genus Iridomyrmex (Hymenoptera: Formicidae). Zootaxa 2845:1–174

    Google Scholar 

  • Hopper SD (2009) OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically-buffered, infertile landscapes. Plant Soil 322:49–86. doi:10.1007/s11104-009-0068-0

    Article  CAS  Google Scholar 

  • Jansen PA, Visser MD, Joseph Wright S, Rutten G, Muller-Landau HC (2014) Negative density dependence of seed dispersal and seedling recruitment in a Neotropical palm. Ecol Lett 17:1111–1120

    Article  PubMed  Google Scholar 

  • Jones AG, Small CM, Paczolt KA, Ratterman NL (2010) A practical guide to methods of parentage analysis. Mol Ecol Res 10:6–30. doi:10.1111/j.1755-0998.2009.02778.x

    Article  Google Scholar 

  • Kalisz S, Hanzawa FM, Tonsor SJ, Thiede DA, Voigt S (1999) Ant-mediated seed dispersal alters patterns of relatedness in a population of Trillium grandiflorum. Ecology 80:2620–2634. doi:10.1890/0012-9658(1999)080[2620:amsdap]2.0.co;2

    Article  Google Scholar 

  • Keith DA, Akçakaya HR, Thuiller W, Midgley GF, Pearson RG, Phillips SJ, Regan HM, Araújo MB, Rebelo TG (2008) Predicting extinction risks under climate change: coupling stochastic population models with dynamic bioclimatic habitat models. Biol Lett 4:560–563

    Article  PubMed Central  PubMed  Google Scholar 

  • Koelewijn HP (2004) Sibling competition, size variation and frequency-dependent outcrossing advantage in Plantago coronopus. Evol Ecol 18:51–74

    Article  Google Scholar 

  • Lamont BB, Downes S, Fox JED (1977) Importance-value curves and diversity indices applied to a species rich heath-land in Western Australia. Nature 265:438–441

    Article  Google Scholar 

  • Lengyel S, Gove AD, Latimer AM, Majer JD, Dunn RR (2009) Ants sow the seeds of global diversification in flowering plants. PLoS ONE 4:1–6. doi:10.1371/journal.pone.0005480

    Article  Google Scholar 

  • 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. Perspect Plant Ecol Evol Syst 12:43–55. doi:10.1016/j.ppees.2009.08.001

    Article  Google Scholar 

  • Majer JD (1980) The influence of ants on broadcast and naturally spread seed in rehabilitated bauxite mined areas. Reclam Rev 3:3–9

    Google Scholar 

  • Majer JD (1982) Ant–plant interactions in the Darling Botanical District of Western Australia. In: Buckley R (ed) Ant–plant Interactions in Australia. Springer, Dordrecht, pp 45–61

    Chapter  Google Scholar 

  • Majer JD (1984) The influence of ants on seeding operations in northern Australian mined areas. Reclam Reveg Rev 2:299–313

    Google Scholar 

  • Majer JD, Gove AD, Sochacki S, Searle P, Portlock C (2011) A comparison of the autecology of two seed-taking ant genera, Rhytidoponera and Melophorus. Insectes Soc 58:115–125

    Article  Google Scholar 

  • Marchante H, Freitas H, Hoffmann JH (2010) Seed ecology of an invasive alien species, Acacia longifolia (Fabaceae), in Portuguese dune ecosystems. Am J Bot 97:1780–1790. doi:10.3732/ajb.1000091

    Article  PubMed  Google Scholar 

  • Marshall TC, Slate J, Kruuk LER, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  CAS  PubMed  Google Scholar 

  • Maslin BR, Buscumb C (2007) Two new Acacia species (Leguminosae: Mimosoideae) from banded ironstone ranges in the Midwest region of south-west Western Australia. Nuytsia 17:263–272

    Google Scholar 

  • Millar MA, Byrne M, Nuberg I, Sedgley M (2008) High outcrossing and random pollen dispersal in a planted stand of Acacia saligna subsp. saligna revealed by paternity analysis using microsatellites. Tree Genet Genomes 4:367–377

    Article  Google Scholar 

  • Millar MA, Byrne M, Nuberg IK, Sedgley M (2012) High levels of genetic contamination in remnant populations of Acacia saligna from a genetically divergent planted stand. Restor Ecol 20:260–267

    Article  Google Scholar 

  • Millar MA, Coates DJ, Byrne M (2014) Extensive long-distance pollen dispersal and highly outcrossed mating in historically small and disjunct populations of Acacia woodmaniorum (Fabaceae), a rare banded iron formation endemic. Ann Bot 114:961–971

    Article  PubMed Central  PubMed  Google Scholar 

  • Mittermeier RA (2004) Hotspots revisited. University of Chicago Press, Chicago

    Google Scholar 

  • Montesinos D, Castro S, Rodríguez-Echeverría S (2012) Invasive acacias experience higher ant seed removal rates at the invasion edges. Web Ecol 12:33–37

    Article  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, Dafonesca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 40:853–858

    Article  Google Scholar 

  • Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol 15:278–285

    Article  PubMed  Google Scholar 

  • Nathan R, Klein EK, Robledo-Arnuncio JJ, Revilla E (2013) Dispersal kernels. In: Clobert J, Baguette M, Benton TG, Bullock JM (eds) Dispersal and spatial evolutionary ecology. Oxford University Press, Oxford, pp 496

  • Ness JH (2004) Forest edges and fire ants alter the seed shadow of an ant-dispersed plant. Oecologia 138:448–454

    Article  CAS  PubMed  Google Scholar 

  • Nevill PG, Anthony JM, Krauss SL (2010) Isolation and characterization of microsatellite markers for the banded ironstone endemic Acacia karina (Leguminosae: Mimosaceae) and cross-species amplification with A. stanleyi and A. jibberdingensis. Conserv Genet Resour 2:321–323. doi:10.1007/s12686-010-9219-0

    Article  Google Scholar 

  • Nevill PG, Wallace MJ, Miller JT, Krauss SL (2013) DNA barcoding for conservation, seed banking and ecological restoration of Acacia in the Midwest of Western Australia. Mol Ecol Resour 13:1033–1042. doi:10.1111/1755-0998.12060

    CAS  PubMed  Google Scholar 

  • O’Dowd DJ, Hay ME (1980) Multalism between harvester ants and a desert ephemeral: seed escape from rodents. Ecology 61:531–540

    Article  Google Scholar 

  • Pascov C (2013) Realised pollen and seed dispersal inferred from parentage analysis in Acacia karina. Honours thesis, The University of Western Australia, Perth

  • Passos L, Oliveira PS (2003) Interactions between ants, fruits, and seeds in restinga forests on south-eastern Brazil. J Trop Ecol 19:261–270

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539. doi:10.1093/bioinformatics/bts460

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pudlo RJ, Beattie AJ, Culver DC (1980) Population consequences of changes in an ant-seed mutualism in Sanguinaria canadensis. Oecologia 46:32–37

    Article  Google Scholar 

  • Schatral A, Kailis SG, Fox JED (1994) Seed dispersal by Hibbertia hypericoides (Dilleniaceae) by ants. J R Soc West Aust 77:81–85

    Google Scholar 

  • Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629. doi:10.1111/j.1461-0248.2006.00889.x

    Article  PubMed  Google Scholar 

  • Shattuck SO (1992) Generic revision of the ant subfamily Dolichoderinae (Hymenoptera: Formicide). Sociobiology 21:1–181

    Google Scholar 

  • Stone GN, Raine NE, Prescott M, Willmer PG (2003) Pollination ecology of acacias (Fabaceae, Mimosoideae). Aust Syst Bot 16:103–118

    Article  Google Scholar 

  • Trakhtenbrot A, Nathan R, Perry G, Richardson DM (2005) The importance of long-distance dispersal in biodiversity conservation. Divers Distrib 11:173–181. doi:10.1111/j.1366-9516.2005.00156.x

    Article  Google Scholar 

  • van der Pijl L (1982) Principles of dispersal in higher plants. Springer, Berlin

    Book  Google Scholar 

  • Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935

    Article  CAS  PubMed  Google Scholar 

  • Wandrag EM, Sheppard A, Duncan RP, Hulme PE (2013) Mutualism vs. antagonism in introduced and native ranges: can seed dispersal and predation determine Acacia invasion success? Perspect Plant Ecol Evol Syst 15:171–179

    Article  Google Scholar 

  • Whitney KD (2002) Dispersal for distance? Acacia ligulata seeds and meat ants Iridomyrmex viridiaeneus. Aust Ecol 27:589–595

    Article  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    CAS  PubMed Central  PubMed  Google Scholar 

  • Young JP (1981) Sib competition can favour sex in two ways. J Theor Biol 88:755–756

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Karara Mining Ltd for funding, Brian Heterick (Curtin University) for his assistance in identification of ant species collected from the field and comments on their biology and Melanie Britton for laboratory assistance. Phyllode and seed material was collected under permit number 63-1314 issued to SK under the Western Australian Wildlife Conservation Act 1950. The authors declare that they have no conflict of interest.

Author contribution statement

PGN originally formulated the idea. PGN, CMP, CPE, JDM, JA and SLK designed the study. PGN, CMP, CPE and JA collected the samples and/or data. CMP, CPE and SLK analysed the data. CMP, PGN CPE, JDM and SLK wrote the manuscript.

Author information

Authors and Affiliations

  1. Botanic Gardens and Parks Authority, Kings Park and Botanic Garden, West Perth, WA, 6005, Australia

    Caitlin M. Pascov, Paul G. Nevill, Carole P. Elliott, Janet M. Anthony & Siegfried L. Krauss

  2. School of Plant Biology, The University of Western Australia, Nedlands, WA, 6009, Australia

    Caitlin M. Pascov, Paul G. Nevill, Jonathan D. Majer, Janet M. Anthony & Siegfried L. Krauss

  3. Department of Environment and Agriculture, Curtin University, Bentley, WA, 6102, Australia

    Paul G. Nevill & Jonathan D. Majer

  4. School of Veterinary and Life Sciences, Environment and Conservation Sciences, Murdoch University, Perth, WA, 6150, Australia

    Carole P. Elliott

Authors
  1. Caitlin M. Pascov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paul G. Nevill
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carole P. Elliott
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jonathan D. Majer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Janet M. Anthony
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Siegfried L. Krauss
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Paul G. Nevill.

Additional information

Communicated by Carlos L. Ballare.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pascov, C.M., Nevill, P.G., Elliott, C.P. et al. The critical role of ants in the extensive dispersal of Acacia seeds revealed by genetic parentage assignment. Oecologia 179, 1123–1134 (2015). https://doi.org/10.1007/s00442-015-3400-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3400-9

Keywords

Search

Navigation