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New mutualism for old: indirect disruption and direct facilitation of seed dispersal following Argentine ant invasion

  • Community Ecology - Original Paper
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Abstract

The indirect effects of biological invasions on native communities are poorly understood. Disruption of native ant communities following invasion by the Argentine ant (Linepithema humile) is widely reported to lead indirectly to the near complete collapse of seed dispersal services. In coastal scrub in southeastern Australia, we examined seed dispersal and handling of two native and two invasive alien plant species at Argentine ant-invaded or -uninvaded sites. The Argentine ant virtually eliminates the native keystone disperser Rhytidoponera victoriae, but seed dispersal did not collapse following invasion. Indeed, Argentine ants directly accounted for 92% of all ant-seed interactions and sustained overall seed dispersal rates. Nevertheless, dispersal quantity and quality among seed species differed between Argentine ant-invaded and -uninvaded sites. Argentine ants removed significantly fewer native Acacia retinodes seeds, but significantly more small seeds of invasive Polygala myrtifolia than did native ants at uninvaded sites. They also handled significantly more large seeds of A. sophorae, but rarely moved them >5 cm, instead recruiting en masse, consuming elaiosomes piecemeal and burying seeds in situ. In contrast, Argentine ants transported and interred P. myrtifolia seeds in their shallow nests. Experiments with artificial diaspores that varied in diaspore and elaiosome masses, but kept seed morphology and elaiosome quality constant, showed that removal by L. humile depended on the interaction of seed size and percentage elaiosome reward. Small diaspores were frequently taken, independent of high or low elaiosome reward, but large artificial diaspores with high reward instead elicited mass recruitment by Argentine ants and were rarely moved. Thus, Argentine ants appear to favour some diaspore types and reject others based largely on diaspore size and percentage reward. Such variability in response indirectly reduces native seed dispersal and can directly facilitate the spread of an invasive alien shrub.

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References

  • Abbott KL, Green PT (2007) Collapse of an ant-scale mutualism in a rainforest on Christmas Island. Oikos 116:1238–1246

    Article  Google Scholar 

  • Andersen AN (1982) Seed removal by ants in the mallee of northwestern Victoria. In: Buckley RC (ed) Ant–plant interactions in Australia. Dr W. Junk, The Hague, pp 31–43

    Google Scholar 

  • Beattie AJ (1985) The evolutionary ecology of ant–plant mutualisms. Cambridge University Press, Cambridge

    Google Scholar 

  • Beattie AJ Culver DC (1983) Inhumation: how ants and other invertebrates help seeds. Nature 297:627

    Google Scholar 

  • Berg RY (1975) Myrmecochorous plants in Australia and their dispersal by ants. Aust J Bot 23:475–508

    Article  Google Scholar 

  • Blancafort X, Gomez C (2005) Consequences of the Argentine ant, Linepithema humile (Mayr), invasion on pollination of Euphorbia characias (L.) (Euphorbiaceae). Acta Oecol Int J Ecol 28:49–55

    Article  Google Scholar 

  • Bond WJ (1995) Assessing the risk of plant extinction due to pollinator and disperser failure. In: Lawton JH, May RM (eds) Extinction rates. Oxford University Press, New York, pp 131–146

    Google Scholar 

  • 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 

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

    Article  Google Scholar 

  • Bronstein JL (1994) Our current understanding of mutualism. Q Rev Biol 69:31–51

    Article  Google Scholar 

  • Carney SE, Byerley MB, Holway DA (2003) Invasive Argentine ants (Linepithema humile) do not replace native ants as seed dispersers of Dendromecon rigida (Papaveraceae) in California, USA. Oecologia 135:576–582

    PubMed  Google Scholar 

  • Christian CE (2001) Consequences of a biological invasion reveal the importance of mutualism for plant communities. Nature 413:635–639

    Article  PubMed  CAS  Google Scholar 

  • Christian CE, Stanton ML (2004) Cryptic consequences of a dispersal mutualism: seed burial, elaiosome removal, and seed-bank dynamics. Ecology 85:1101–1110

    Article  Google Scholar 

  • Cordeiro NJ, Howe HF (2003) Forest fragmentation severs mutualism between seed dispersers and an endemic African tree. Proc Natl Acad Sci USA 100:14052–14056

    Article  PubMed  CAS  Google 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. Evol Ecol Res 9:1349–1362

    Google Scholar 

  • Foster JT, Robinson SK (2007) Introduced birds and the fate of Hawaiian rainforests. Conserv Biol 21:1248–1257

    Article  PubMed  Google Scholar 

  • Garrido JL, Rey PJ, Cerda X, Herrera CM (2002) Geographical variation in diaspore traits of an ant-dispersed plant (Helleborus foetidus): are ant community composition and diaspore traits correlated? J Ecol 90:446–455

    Article  Google Scholar 

  • Gomez C, Oliveras J (2003) Can the Argentine ant (Linepithema humile Mayr) replace native ants in myrmecochory? Acta Oecol 24:47–53

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Gunther RW, Lanza J (1989) Variation in attractiveness of Trillium diaspores to a seed-dispersing ant. Am Midl Nat 122:321–328

    Article  Google Scholar 

  • Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233

    Article  Google Scholar 

  • Howe HF, Miriti MN (2004) When seed dispersal matters. Bioscience 54:651–660

    Article  Google Scholar 

  • Hughes L, Westoby M (1990) Removal rates of seeds adapted for dispersal by ants. Ecology 71:138–148

    Article  Google Scholar 

  • Hughes L, Westoby M (1992a) Effect of diaspore characteristics on removal of seeds adapted for dispersal by ants. Ecology 73:1300–1312

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 

  • Human KG, Gordon DM (1997) Effects of Argentine ants on invertebrate biodiversity in northern California. Conserv Biol 11:1242–1248

    Article  Google Scholar 

  • Lach L (2007) A mutualism with a native membracid facilitates pollinator displacement by Argentine ants. Ecology 88:1994–2004

    Article  PubMed  Google Scholar 

  • Le Breton J, Chazeau J, Jourdan H (2003) Immediate impacts of invasion by Wasmannia auropunctata (Hymenoptera: Formicidae) on native litter ant fauna in a new caledonian rainforest. Aust Ecol 28:204–209

    Article  Google Scholar 

  • Ness JH, Bronstein JL (2004) The effects of invasive ants on prospective ant mutualists. Biol Invasions 6:445–461

    Article  Google Scholar 

  • Ness JH, Bronstein JL, Andersen AN, Holland JN (2004) Ant body size predicts dispersal distance of ant-adapted seeds: implications of small ant invasions. Ecology 85:1244–1250

    Article  Google Scholar 

  • O’Dowd DJ, Hay ME (1980) Mutualism between harvester ants and a desert ephemeral: seed escape from rodents. Ecology 60:531–540

    Article  Google Scholar 

  • O’Dowd DJ, Gill AM (1986) Seed dispersal syndromes in Australian Acacia. In: Murray DR (ed) Seed dispersal. Academic Press, Australia, pp 87–121

    Google Scholar 

  • O’Dowd DJ, Green PT, Lake PS (2003) Invasional ‘meltdown’ on an oceanic island. Ecol Lett 6:812–817

    Article  Google Scholar 

  • Pemberton RW (1988) Myrmecochory in the introduced range weed, leafy spurge (Euphorbia esula L.). Am Midl Nat 119:431–435

    Article  Google Scholar 

  • Pemberton RW, Irving DW (1990) Elaiosomes on weed seeds and the potential for myrmecochory in naturalized plants. Weed Sci 38:615–619

    Google Scholar 

  • Porter SD, Savignano DA (1990) Invasion of polygyne fire ants decimates native ants and disrupts arthropod community. Ecology 71:2095–2106

    Article  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Google Scholar 

  • Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmanek M (2000) Plant invasions—the role of mutualisms. Biol Rev 75:65–93

    Article  PubMed  CAS  Google Scholar 

  • Rico-Grey V, Oliveira PS (2007) The ecology and evolution of ant–plant interactions. University of Chicago Press, Chicago

    Google Scholar 

  • Rodgerson L (1998) Mechanical defense in seeds adapted for ant dispersal. Ecology 79:1669–1677

    Article  Google Scholar 

  • Rodriguez-Cabal MA, Aizen MA, Novaro AJ (2007) Habitat fragmentation disrupts a plant-disperser mutualism in the temperate forest of South America. Biol Conserv 139:195–202

    Article  Google Scholar 

  • Roulston TH, Silverman J (2002) The effect of food size and dispersion pattern on retrieval rate by the Argentine ant, Linepithema humile (Hymenoptera: Formicidae). J Insect Behav 15:633–648

    Article  Google Scholar 

  • Rowles AD, O’Dowd DJ (2007) Interference competition by Argentine ants displaces native ants: implications for biotic resistance to invasion. Biol Invasions 9:73–85

    Article  Google Scholar 

  • Rowles AD, O’Dowd DJ (in press) Impacts of the invasive Argentine ant on native ants and other invertebrates in coastal scrub in southeastern Australia. Aust Ecol

  • Silverman J, Roulston TH (2003) Retrieval of granular bait by the Argentine ant (Hymenoptera: Formicidae): effect of clumped versus scattered dispersion patterns. J Econ Ent 96:871–874

    Article  Google Scholar 

  • Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32

    Article  Google Scholar 

  • Simpson SR, Gross CL, Silberbauer LX (2005) Broom and honeybees in Australia: an alien liaison. Plant Biol 7:541–548

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Smith JMB (1989) An example of ant-assisted plant invasion. Aust J Ecol 14:247–250

    Article  Google Scholar 

  • Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21:208–216

    Article  PubMed  Google Scholar 

  • Traveset A, Riera N (2005) Disruption of a plant-lizard seed dispersal system and its ecological effects on a threatened endemic plant in the Balearic Islands. Conserv Biol 19:421–431

    Article  Google Scholar 

  • Walters AC (2006) Invasion of Argentine ants (Hymenoptera: Formicidae) in South Australia: impacts on community composition and abundance of invertebrates in urban parklands. Aust Ecol 31:567–576

    Article  Google Scholar 

  • Wilkinson L (2000) SYSTAT 10. SPSS, Chicago

    Google Scholar 

  • Witt ABR, Geertsema H, Giliomee J (2004) The impact of an invasive ant, Linepithema humile (Mayr) (Hymenoptera: Formicidae), on the dispersal of the elaiosome-bearing seeds of six plant species. Afr Entomol 12:223–230

    Google Scholar 

  • Zettler JA, Spira TP, Allen CR (2001) Ant-seed mutualisms: can red imported fire ants sour the relationship? Biol Conserv 101:249–253

    Article  Google Scholar 

Download references

Acknowledgments

J. Majer and J. Silverman commented on earlier drafts and comments by R.R. Dunn improved the manuscript. B. Rowles-van Rijswijk assisted in the field. A.N. Andersen identified the ant species. Parks Victoria provided access to Mornington Peninsula National Park under permit no. 10002268. This is contribution no. 147 from the Australian Centre for Biodiversity.

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  1. Alexei D. Rowles

    Present address: Department of Primary Industries, Rutherglen Centre, RMB 1145, Chiltern Valley Road, Rutherglen, VIC, 3685, Australia

Authors and Affiliations

  1. Australian Centre for Biodiversity, School of Biological Sciences, Monash University, Clayton, VIC, 3800, Australia

    Alexei D. Rowles & Dennis J. O’Dowd

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  1. Alexei D. Rowles
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  2. Dennis J. O’Dowd
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Correspondence to Alexei D. Rowles.

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Communicated by Jacqui Shykoff.

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Rowles, A.D., O’Dowd, D.J. New mutualism for old: indirect disruption and direct facilitation of seed dispersal following Argentine ant invasion. Oecologia 158, 709–716 (2009). https://doi.org/10.1007/s00442-008-1171-2

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