Skip to main content
SpringerLink
Log in

Disruption of ant-seed dispersal mutualisms by the invasive Asian needle ant (Pachycondyla chinensis)

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

By disrupting the structure of native ant assemblages, invasive ants can have effects across trophic levels. Most studies to date, however, have focused on the impacts just two species (Linepithema humile and Solenopsis invicta). The impacts of many other invasive ant species on ecological processes in their introduced range are unknown. In this study we tested the hypothesis that the invasive ant Pachycondyla chinensis disrupts ant-seed dispersal mutualisms by displacing native ant species, especially the keystone mutualist Aphaenogaster rudis, while failing to disperse seeds itself. In a paired design we measured the impact of P. chinensis on the native ant-plant seed dispersal mutualism. The number of A. rudis workers was 96% lower in invaded than in intact plots, and the number of seeds removed was 70% lower in these plots. Finally, in invaded plots the abundance of Hexastylis arifolia, a locally abundant myrmecochorous plant, was 50% lower than in plots where P. chinensis was absent. A parsimonious interpretation of our results is that P. chinensis causes precipitous declines in the abundance of A. rudis within invaded communities, thereby disrupting the ant-plant seed dispersal mutualisms and reducing abundances of ant-dispersed plants. In sum, the magnitude of the effects of P. chinensis on seed dispersal is quantitatively similar to that documented for the intensively studied invasive Argentine ant. We suggest that more studies on the impacts of less-studied invasive ant species on seed dispersal mutualisms may increase our knowledge of the effects of these invaders on ecosystem function.

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

Similar content being viewed by others

References

  • Bascompte J, Jordano P, Melian CJ, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. Proc Nat Acad Sci USA 100:9383–9387

    Article  PubMed  CAS  Google Scholar 

  • Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433

    Article  PubMed  CAS  Google Scholar 

  • Bednar DM (2010) Pachycondyla (=Brachyponera) chinensis predation on Reticuletermes virginicus and competition with Aphaenogaster rudis. Master of science thesis, North Carolina State University, USA

  • Bestelmeyer BT, Agosti D, Alonso LE, Brandão CRF, Brown WL Jr, Delabie JHC, Silvestre R (2000) Field techniques for the study of ground-dwelling ants: an overview, description, and evaluation. In: Agosti D, Majer JD, Alonso LE, Schultz TR (eds) Ants: standard methods for measuring and monitoring biodiversity. Smithsonian Institution Press, Washigton, pp 122–144

    Google Scholar 

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

    Article  Google Scholar 

  • Cain ML, Damman H (1997) Clonal growth and ramet performance in the woodland herb, Asarum canadense. J Ecol 85:883–897

    Article  Google Scholar 

  • Canner JE (2010) The population ecology of ant-dispersed plants in space and time. Dissertation, North Carolina State University, USA

  • 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 412:635–639

    Article  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 

  • Culver DC, Beattie AJ (1980) The fate of Viola seeds dispersed by ants. J Bot 67:710–714

    Article  Google Scholar 

  • Damman H, Cain ML (1998) Population growth and viability analyses of the clonal woodland herb, Asarum canadense. J Ecol 86:13–26

    Article  Google Scholar 

  • D’Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass fire cycle, and global change. Annu Rev Ecol Syst 23:63–87

    Google Scholar 

  • Eguchi K (2004) A survey on seed predation by omnivorous ants in the warm-temperate zone of Japan (Insecta, Hymnoptera, Formicidae). New Entomol 53:7–18

    Google Scholar 

  • Ellison AM, Bank MS, Clinton BD, Colburn EA, Elliott K, Ford CR, Foster DR, Kloeppel BD, Knoepp JD, Lovett GM, Mohan J, Orwig DA, Rodenhouse NL, Sobczak WV, Stinson KA, Stone JK, Swan CM, Thompson J, von Holle B, Webster JR (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 9:479–486

    Article  Google Scholar 

  • Fellers JH (1989) Daily and seasonal activity in woodland ants. Oecologia 78:69–76

    Article  Google Scholar 

  • Giladi I (2004) The role of habitat-specific demography, habitat specific dispersal, and the evolution of dispersal distances in determining current and future distributions of the ant dispersed forest herb, Hexastylis arifolia. Dissertation, University of Georgia, USA

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

    Article  Google Scholar 

  • Gilbert LE (1980) Food web organization and the conservation of neotropical diversity. In: Soule ME, Wilcox BA (eds) Conservation biology: an evolutionary-ecological perspective. Sinauer, Sunderland, pp 11–33

    Google Scholar 

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

    Article  Google Scholar 

  • Gómez C, Pons P, Bas JM (2003) Effects of the Argentine ant Linepithema humile on seed dispersal and seedling emergence of Rhamunus alaternus. Ecography 26:532–538

    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 

  • Guénard B, Dunn RR (2010) A new (old), invasive ant in the hardwood forests of Eastern North America and its potentially widespread impacts. PLoS ONE 5(7):e11614. doi:10.1371/journal.pone.0011614

  • 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, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13:201–228

    Article  Google Scholar 

  • Jordano P, Schupp EW (2000) Determinants of seed disperser effectiveness: the quantity component and patterns of seed rain for Prunus mahaleb. Ecol Monogr 70:591–615

    Google Scholar 

  • Lessard JP, Fordyce JM, Gotelli NJ, Sanders NJ (2009) Invasive ants alter the phylogenetic structure of native communities. Ecology 90:2664–2669

    Article  PubMed  Google Scholar 

  • Levine JM, Vilà M, D’Antonio CM, Dukes JS, Grigulis K, Lavorel S (2003) Mechanism underlying the impacts of exotic plant invasions. Proc Royal Soc B 270:775–781

    Article  Google Scholar 

  • Manzaneda AJ, Rey PJ (2009) Assessing ecological specialization of an ant-seed dispersal mutualism through a wide geographic range. Ecology 90:3009–3022

    Article  PubMed  Google Scholar 

  • McCoy NL (2009) The geographical mosaic of myrmecochory in a global biodiversity hotspot and the fate of myrmecochorous seeds dispersed by a keystone seed disperser. Master of science thesis, North Carolina State University, USA

  • McGlynn T (1999) The worldwide transfer of ants: geographical distribution and ecological invasions. J Biogeogr 26:535–548

    Article  Google Scholar 

  • McGown JA (2009) The Asian Needle Ant, Pachycondyla chinensis (Emery)(Hymenoptera: Formicidae), reported from Alabama. Midsouth Entomol 2:88–89

    Google Scholar 

  • Mitchell CE, Turner MG, Pearson SM (2002) Effects of historical land use and forest patch size on myrmecochores and ant communities. Ecol Appl 12:1364–1377

    Article  Google Scholar 

  • Ness JH (2004) Forest edges and fire ants alter the seed shadow of an ant-dispersered plant. Oecologia 138:228–454

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ness JH, Morin DF, 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Rey PJ, Garrido JL, Alcántara JM, Ramírez JM, Aguilera A, García L, Manzaneda AJ, Fernández R (2002) Spatial variation in ant and rodent post-dispersal predation of vertebrate-dispersed seeds. Funct Ecol 16:773–781

    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 

  • Rodriguez-Cabal MA, Stuble KL, Nuñez MA, Sanders NJ (2009) Quantitative analysis of the effects of the exotic Argentine ant on seed-dispersal mutualisms. Biol Lett 5:499–502

    Article  PubMed  Google Scholar 

  • Rowles AD, O’Dowd DJ (2009) New mutualism for old: indirect disruption and direct facilitation of seed dispersal following Argentine ant invasion. Oecologia 158:709–716

    Article  PubMed  Google Scholar 

  • Sanders NJ, Suarez AV (2010) Elton’s insights into the ecology of ant invasions: lessons learned and lessons still to be learned. In: Richardson DM (ed) Fifty years of invasion ecology: the legacy of Charles Elton. Blackwell, New York, pp 239–251

    Google Scholar 

  • Schupp EW (1993) Quantity, quality and the effectiveness of seed dispersal by animals. Vetatio 107(108):15–29

    Google Scholar 

  • Schupp EW, Fuentes M (1995) Spatial patterns of seed dispersal and the unification of plant population ecology. Ecoscience 2:267–275

    Google Scholar 

  • Smith MR (1934) Ponerine ants of the genus Euponera in the United States. Ann Entomol Soc Am 27:558–564

    Google Scholar 

  • Stuble KL, Kirkman LK, Carroll CR (2010) Are red imported fire ants facilitators of native seed dispersal? Biol Invasions 12:1661–1669

    Article  Google Scholar 

  • Stuble KL, Kirkman LK, Carrol CR, Sanders NJ (2011) Relative effects of disturbance on red imported fire ants and native ant species in a longleaf pine ecosystem. Conserv Biol 25:618–622

    Article  PubMed  Google Scholar 

  • Styrsky JD, Eubanks MD (2010) A facultative mutualism between aphids and an invasive ant increases plant reproduction. Ecol Entomol 35:190–199

    Article  Google Scholar 

  • Suarez AV, Bolger DT, Case TJ (1998) Effects of fragmentation and invasion on native ant communities in coastal southern California. Ecology 79:2041–2056

    Article  Google Scholar 

  • Tardiff SE, Stanford JA (1998) Grizzly bear digging: effects on subalpine meadow plants in relation to mineral nitrogen availability. Ecology 79:2219–2228

    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 

  • Vazquez DP, Aizen MA (2004) Degree distribution in plant-animal mutualistic networks: forbidden links or random interactions. Oikos 108:421–426

    Article  Google Scholar 

  • Vazquez DP, Simberloff D (2004) Indirect effects of an introduced ungulate on pollination and plant reproduction. Ecol Monogr 74:281–308

    Article  Google Scholar 

  • Vazquez DP, Morris WF, Jordano P (2005) Interaction frequency as surrogate for the total effect of animal mutualists on plants. Ecol Lett 8:1088–1094

    Article  Google Scholar 

  • Vitousek PM (1990) Biological invasions and ecosystem processes—towards an integration of population biology and ecosystem studies. Oikos 57:7–13

    Article  Google Scholar 

  • Wenny DG, Levey DJ (1998) Directed seed dispersal by bellbirds in a tropical cloud forest. Proc Natl Acad Sci USA 95:6204–6207

    Article  PubMed  CAS  Google Scholar 

  • Yashiro T, Matsuura K, Guénard B, Terayama M, Dunn RR (2010) On the evolution of the species complex Pachycondyla chinensis (Hymenoptera: Formicidae: Ponerinae), including the origin of its invasive form and description of a new species. Zootaxa 2685:39–50

    Google Scholar 

  • Zelikova TJ, Dunn RR, Sanders NJ (2008) Variation in seed dispersal along an elevation gradient in Great Smoky Mountains National Park. Acta Oecol 34:155–162

    Article  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

We thank Historic Yates Mill County Park for permission to carry out field work and G. L. McCormick and J. E. Canner for assistance in the field. M. N. Barrios-Garcia, J. A. Schweitzer, J. K. Bailey and M. A. Nuñez provided advice that greatly improved this manuscript. This research was funded by the Department of Ecology and Evolutionary Biology at the University of Tennessee.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Tennessee, 569 Dabney Hall, Knoxville, TN, 37996, USA

    Mariano A. Rodriguez-Cabal, Katharine L. Stuble & Nathan J. Sanders

  2. Department of Biology, North Carolina State University, 120 David Clark Labs, Raleigh, NC, 27695, USA

    Benoit Guénard & Robert R. Dunn

Authors
  1. Mariano A. Rodriguez-Cabal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katharine L. Stuble
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Benoit Guénard
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Robert R. Dunn
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nathan J. Sanders
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mariano A. Rodriguez-Cabal.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rodriguez-Cabal, M.A., Stuble, K.L., Guénard, B. et al. Disruption of ant-seed dispersal mutualisms by the invasive Asian needle ant (Pachycondyla chinensis). Biol Invasions 14, 557–565 (2012). https://doi.org/10.1007/s10530-011-0097-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-011-0097-5

Keywords

Search

Navigation