Forest invader replaces predation but not dispersal services by a keystone species

Abstract

Invasive species generally occur and thrive in human-disturbed ecosystems, but Brachyponera chinensis (Asian needle ant, formerly ‘Pachycondyla chinensis’) also invades intact forests. The invasion into native habitats potentially puts B. chinensis in direct competition with the keystone seed-dispersing ants in the genus Aphaenogaster. We observed B. chinensis colonizing artificial nests placed in deciduous forest of the north Georgia Piedmont (US). Their presence appeared to displace existing Aphaenogaster rudis and Reticulitermes flavipes (subterranean termite) colonies. We subsequently mapped the B. chinensis invasion as well as co-existing A. rudis and R. flavipes colonies by examining coarse woody material (CWM) for nesting colonies. We tested whether the B. chinensis invasion changed with forest microclimates, covaried with A. rudis and/or R. flavipes occurrence, and whether it was associated with failed dispersal of a dominant understory herb. Our results and observations suggest that B. chinensis shares ecological niche requirements (temperature, moisture and CWM as nesting habitat) with A. rudis, severely diminishing the abundance of this native ant. In supplanting A. rudis, B. chinensis appears to play an equivalent role to A. rudis as a termite predator, but fails as a seed disperser. Essentially, the invader substitutes for the negative but not the positive species interactions, thereby apparently shifting ecological dynamics in the invaded system.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Abe T (1990) Evolution of worker caste in termites. In: Veeresh GK, Mallik B, Viraktamath CA (eds) Social insects and the environment. Oxford and IBH, New Delhi

    Google Scholar 

  2. Akaike H (1973) Information theory as an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Second international symposium on information theory. Akademiai Kiado, Budapest, pp 267–281

    Google Scholar 

  3. Bednar DM (2010) Pachycondyla (=Brachyponera) predation on Reticulitermes virginicus and competition with Aphaenogaster rudis. M.S. Thesis, North Carolina State. http://www.lib.ncsu.edu/resolver/1840.16/6363

  4. Bednar DM, Silverman J (2011) Use of termites, Reticulitermes virginicus, as a springboard in the invasive success of a predatory ant, Pachycondyla (=Brachyponera) chinensis. Insectes Soc 58:459–467

    Article  Google Scholar 

  5. Bednar DM, Shik JZ, Silverman J (2013) Prey handling perfomance facilitates competitive dominance of an invasive over native keystone ant. Behav Ecol 24:1312–1319

    Article  Google Scholar 

  6. Bolton B (2010) Identification guide to the ant genera of the world. Harvard University Press, Cambridge

    Google Scholar 

  7. Bradford MA, Warren RJ II, Baldrain P et al (2014) Climate fails to predict wood decomposition at regional scales. Nat Clim Change 4:625–630

    CAS  Article  Google Scholar 

  8. Buczkowski G, Bennett G (2007) Protein marking reveals predation on termites by the woodland ant, Aphaenogaster rudis. Insectes Soc 54:219–224

    Article  Google Scholar 

  9. Buczkowski G, Bennett G (2008) Behavioral interactions between Aphaenogaster rudis (Hymenoptera: Formicidae) and Reticulitermes flavipes (Isoptera: Rhinotermitidae): the importance of physical barriers. J Insect Behav 21:296–305

    Article  Google Scholar 

  10. Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches. University of Chicago, Chicago

    Book  Google Scholar 

  11. Creighton WS (1950) The ants of North America. The Cosmos Press Inc., Cambridge

    Google Scholar 

  12. Darwin C (1859) The origin of species by means of natural selection or the preservation of favoured races in the struggle for life. Murray, London

    Book  Google Scholar 

  13. Elton CS (1958) the ecology of invasions of animals and plants. Methuen, London

    Book  Google Scholar 

  14. Emerson AE (1936) Termite distribution in the United States. Science 83:410–411

    CAS  Article  PubMed  Google Scholar 

  15. Felker-Quinn E, Schweitzer JA, Bailey JK (2013) Meta-analysis reveals evolution in invasive plant species but little support for Evolution of Increased Competitive Ability (EICA). Ecol Evol 3:739–751

    PubMed Central  Article  PubMed  Google Scholar 

  16. 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. University of Georgia, Athens, Georgia. http://coweeta.uga.edu/publications/2004_giladi_uga.pdf, pp. 175

  17. Gotoh A, Ito F (2008) Seasonal cycle of colony structure in the Ponerine ant Pachycondyla chinensis in western Japan (Hymenoptera, Formicidae). Insectes Soc 55:98–104

    Article  Google Scholar 

  18. Guenard 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:e11614. doi:10.1371/journal.pone.0011614

    PubMed Central  Article  PubMed  Google Scholar 

  19. Guenard B, Silverman J (2011) Tandem carrying, a new foraging strategy in ants: description, function, and adaptive significance relative to other described foraging strategies. Naturwissenschaften 98:651–659

    CAS  Article  PubMed  Google Scholar 

  20. Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19:470–474

    Article  PubMed  Google Scholar 

  21. Hurlbert SH, Lombardi CM (2009) Final collapse of the Newman-Pearson decision theoretic framework and the rise of the neoFisherian. Ann Zool Fenn 46:311–349

    Article  Google Scholar 

  22. Kahle D, Wickham H (2013) ggmap: a package for spatial visualization with Google Maps and OpenStreetMap. http://CRAN.R-project.org/package=ggmap

  23. King JR, Tschinkel WR (2008) Experimental evidance that human impacts drive fire ant invasions and ecological change. Proc Natl Acad Sci 105:20339–20343

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  24. King JR, Tschinkel WR (2013) Experimental evidence for weak effects of fire ants in a naturally invaded pine-savanna ecosystem. Ecol Entomol 38:68–75

    Article  Google Scholar 

  25. King JR, Warren RJ II, Bradford MA (2013) Social insects dominate eastern US temperate hardwood forest macroinvertebrate communities in warmer regions. PLoS One 8:e75843

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  26. Korb J (2007) Termites. Curr Biol 17:995–999

    Article  Google Scholar 

  27. Lessard JP, Fordyce JA, Gotelli NJ et al (2009) Invasive ants alter the phylogenetic structure of ant communities. Ecology 90:2664–2669

    Article  PubMed  Google Scholar 

  28. Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545

    Article  Google Scholar 

  29. Lubertazzi D (2012) The biology and natural history of Aphaenogaster rudis. Psyche 2012:1–11

    Article  Google Scholar 

  30. Martin PH, Canham CD, Marks PL (2009) Why forests appear resistant to exotic plant invasions: intentional introductions, stand dynamics, and the role of shade tolerance. Front Ecol Environ 7:142–149

    Article  Google Scholar 

  31. Matsuura K (2002) Colony-level stabilization of soldier head width for head-plug defense in the termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Behav Ecol Sociobiol 51:172–179

    Article  Google Scholar 

  32. Menke SB, Holway DA (2006) Abiotic factors control invasion by Argentine ants at the community scale. J Anim Ecol 75:368–376

    Article  PubMed  Google Scholar 

  33. Nelder MP, Paysen ES, Zungoli PA et al (2006) Emergence of the introduced ant Pachycondyla chinensis (Formicidae: Ponerinae) as a public health threat in the southeastern United States. J Med Entomol 43:1094–1098

    Article  PubMed  Google Scholar 

  34. 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 12:1793–1804

    Article  Google Scholar 

  35. Ordonez A, Wright IJ, Olff H (2010) Functional differences between native and alien species: a global-scale comparison. Funct Ecol 24:1353–1361

    Article  Google Scholar 

  36. Pudlo RJ, Beattie AJ, Culver DC (1980) Population consequences of changes in ant-seed mutualism in Sanguinaria canadensis. Oecologia 146:32–37

    Article  Google Scholar 

  37. Rice ES, Silverman J (2013) Propagule pressure and climate contribute to the displacement of Linepithema humile by Pachycondyla chinensis. PLoS One 8:856281

    Google Scholar 

  38. Rodriguez-Cabal MA, Stuble KL, Guenard B et al (2012) Disruption of ant-seed dispersal mutualisms by the invasive Asian needle ant (Pachycondyla chinensis). Biol Invasions 14:557–565

    Article  Google Scholar 

  39. Roura-Pascual N, Bas JM, Hui C (2010) The spread of the Argentine ant: environmental determinants and impacts on native ant communities. Biol Invasions 12:2399–2412

    Article  Google Scholar 

  40. Sanders NJ, Saurez AV (2011) 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. Blackwell Publishing, Hoboken

    Google Scholar 

  41. Smallwood J (1982) Nest relocation in ants. Insectes Soc 29:138–147

    Article  Google Scholar 

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

    Google Scholar 

  43. Smith DR (1979) Catalog of Hymenoptera in America North of Mexico. Smithsonian Institution Press, Washington, DC

    Google Scholar 

  44. Talbot M (1951) Populations and hibernating conditions of the ant Aphaenogaster (Attomyrma) rudis Emery (Hymenoptera: Formicidae). Ann Entomol Soc Am 44:302–307

    Article  Google Scholar 

  45. Thorne BL, Traniello JFA, Adams ES et al (1999) Reproductive dynamics and colony structure of subterranean termites of the genus Reticulitermes (Isoptera: Rhinotermitidae): a review of the evidence from behavioral, ecological, and genetic studies. Ethol Ecol Evol 11:149–169

    Article  Google Scholar 

  46. Umphrey GJ (1996) Morphometric discrimination among sibling species in the fulva - rudis - texana complex of the ant genus Aphaenogaster (Hymenoptera: Formicidae). Can J Zool 74:528–559

    Article  Google Scholar 

  47. Vargo EL, Leniaud I, Swoboda LE et al (2013) Clinal variation in colony breeding structure and level of inbreeding in the subterranean termites Reticulitermes flavipes and R. grassei. Mol Ecol 22:1447–1462

    Article  PubMed  Google Scholar 

  48. Vila M, Espinar JL, Hejda M et al (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708

    Article  PubMed  Google Scholar 

  49. Warren RJ II, Bradford MA (2011) The shape of things to come: woodland herb niche contraction begins during recruitment in mesic forest microhabitat. Proc R Soc B Biol. Sci. 278:1390–1398

    Article  Google Scholar 

  50. Warren RJ II, Bradford MA (2012) Ant colonization and coarse woody debris decomposition in temperate forests. Insectes Soc 59:215–221

    Article  Google Scholar 

  51. Warren RJ II, Bradford MA (2013) Mutualism fails when climate response differs between interacting species. Glob Change Biol 20:466–474

    Article  Google Scholar 

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

    Google Scholar 

  53. Warren RJ II (2007) Linking understory evergreen herbaceous distributions and niche differentiation using habitat-specific demography and experimental common gardens. University of Georgia, Athens, GA. http://coweeta.uga.edu/publications/10315.pdf

  54. Warren RJ II, Giladi I, Bradford MA (2010) Ant-mediated seed dispersal does not facilitate niche expansion. J Ecol 98:1178–1185

    Article  Google Scholar 

  55. Warren RJ II, Giladi I, Bradford MA (2014) Competition as a mechanism structuring mutualisms. J Ecol 102:486–495

    Article  Google Scholar 

  56. Yashiro T, Matsuura K, Guenard B et al (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 

  57. Zalasiewicz J, Williams M, Smith A et al (2008) Are we now living in the Anthropocene? GSA Today 18:4–8

    Google Scholar 

  58. Zelikova TJ, Sanders D, Dunn RR (2011) The mixed effects of experimental ant removal on seedling distribution, belowground invertebrates, and soil nutrients. Ecosphere 2:1–14

    Article  Google Scholar 

  59. Zungoli PA, Benson EP (2008) Seasonal occurrence of swarming activity and worker abundance of Pachycondyla chinensis (Hymenoptera: Formicidae). In: Robinson WH, Bajomi D (eds) Proceedings of the Sixth International Conference on Urban Pests. OOK-Press Kft, Veszprem

    Google Scholar 

Download references

Acknowledgments

We thank Holly Emmert, Lauren Evans, Katie Mackoul, Mallory Nickel, Chris Dodge, Charlene Gray and Sara Miller from the Highlands Biological Station Climate Change Ecology course for field assistance. We also thank Phil Lester for helpful manuscript comments. This is the Termite Ecology and Myrmecology (TEAM) working group publication number 4.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Robert J. Warren II.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Warren, R.J., McMillan, A., King, J.R. et al. Forest invader replaces predation but not dispersal services by a keystone species. Biol Invasions 17, 3153–3162 (2015). https://doi.org/10.1007/s10530-015-0942-z

Download citation

Keywords

  • Aphaenogaster rudis
  • Asian needle ant
  • Brachyponera chinensis
  • Coarse woody material
  • Pachycondyla chinensis
  • Reticulitermes flavipes
  • Termite