Skip to main content

Advertisement

Log in

Regional-scale environmental resistance to non-native ant invasion

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

Abstract

A successful invasion of novel habitat requires that non-native organisms overcome native abiotic and biotic resistance. Non-native species can overcome abiotic resistance if they arrive with traits well-suited for the invaded habitat or if they can rapidly acclimate or adapt. Non-native species may co-exist with native species if they require novel, underused resources or if they can out-compete similar native species. We investigated abiotic and biotic resistance to the progression of a Brachyponera chinensis invasion in the southeastern U.S. relative to the dominant native woodland ant (Aphaenogaster). We used observational data from long-term plots along the elevation gradient of the Southern Appalachian Mountain escarpment to investigate the patterns of B. chinensis invasion, and we used physiological thermal tolerance, aggression assays and stable isotope analysis to determine whether abiotic or biotic factors explained B. chinensis invasion. We found that B. chinensis exhibited an inflexible and relatively poor ability to tolerate cold temperatures, which corresponded with limited success at higher elevations in the Southern Appalachian Mountains. Though we found native ant resistance to B. chinensis invasion, it paled in comparison to the invasive ant’s ability to form huge, cooperating supercolonies that eventually eliminated the native ant. Without biotic resistance, susceptible native species may only be protected if they can tolerate abiotic conditions that the invasive species cannot. For Aphaenogaster species, high elevations and northern latitudes beyond B. chinensis’ cold tolerance may be their only refuge.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data accessibility

The data generated and analyzed for the current study will be available in the SUNY Buffalo State Digital Commons (https://digitalcommons.buffalostate.edu/biology_data/7/) upon manuscript acceptance.

References

  • Allen HR (2017) Biology and behavior of the Asian needle ant, Brachyponera chinensis. Department of Entomology, Clemson University, Clemson, SC

    Google Scholar 

  • 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 Sociaux 58:459–467

    Article  Google Scholar 

  • 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 

  • Berryman A, Turchin P (2001) Identifying the density-dependent structure underlying ecological time series. Oikos 92:265–270

    Article  Google Scholar 

  • Bertelsmeier C, Blight O, Courchamp F (2016) Invasions of ants (Hymenoptera: Formicidae) in light of global climate change. Myrmecol News 22:25–42

    Google Scholar 

  • Bertelsmeier C, Ollier S, Liebhold A et al (2017) Recent human history governs global ant invasion dynamics. Nat Ecol Evol 1:84

    Article  Google Scholar 

  • Bishop TR, Robertson MP, Van Rensburg BJ et al (2016) Coping with the cold: minimum temperatures and thermal tolerances dominate the ecology of mountain ants. Ecol Entomol 42:105–114

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 

  • Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443

    Article  Google Scholar 

  • Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366

    Article  Google Scholar 

  • Clark JS, Soltoff BD, Powell AS et al (2012) Evidence from individual inference for high-dimensional coexistence: long-term experiments on recruitment response. PLoS ONE 7:e30050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crozier RH (1977) Genetic differentiation between populations of the ant Aphaenogaster ‘rudis’ in the southeastern United States. Genetica 47:17–36

    Article  Google Scholar 

  • del Toro I, Ribbons RR, Pelini SL (2012) The little things that run the world revisited: a review of ant-mediated ecosystem services and disservices (Hymenoptera: Formicidae). Myrmecol News 17:133–146

    Google Scholar 

  • Diamond SE, Chick L, Perez A et al (2017) Rapid evolution of ant thermal tolerance across an urban–rural temperature cline. Biol J Linn Soc 121:248–257

    Article  Google Scholar 

  • Dunn RR, Parker CR, Sanders NJ (2007) Temporal patterns of diversity: assessing the biotic and abiotic controls on ant assemblages. Biol J Linn Soc 91:191–201

    Article  Google Scholar 

  • Errard C, Delabie J, Jourdan H et al (2005) Intercontinental chemical variation in the invasive ant Wasmannia auropunctata (Roger) (Hymenoptera Formicidae): a key to the invasive success of a tramp species. Naturwissenschaften 92:319–323

    Article  CAS  PubMed  Google Scholar 

  • Eyer P-A, Matsuura K, Vargo EL et al (2018) Inbreeding tolerance as a pre-adapted trait for invasion success in the invasive ant Brachyponera chinensis. Mol Ecol 15:12. https://doi.org/10.1111/mec.14910

    Article  Google Scholar 

  • Fellers JH (1987) Interference and exploitations in a guild of woodland ants. Ecology 68:1466–1478

    Article  Google Scholar 

  • Folgarait PJ (1998) Ant biodiversity and its relationship to ecosystem functioning—a review. Biodivers Conserv 7:1221–1244

    Article  Google Scholar 

  • Fournier D, de Biseau J-C, De Laet S et al (2016) Social structure and genetic distance mediate nestmate recognition and aggressiveness in the facultative polygynous ant Pheidole pallidula. PLoS ONE 11:e0156440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furst MA, Durey M, Nash DR (2011) Testing the adjustable threshold model for intruder recognition on Myrmica ants in the context of a social parasite. Proc R Soc Lond Ser B Biol Sci 279:516–522

    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. University of Georgia, Athens, Georgia. http://coweeta.uga.edu/publications/2004_giladi_uga.pdf. Accessed 12 Nov 2019

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guenard B, Wetterer JK, MacGown JA (2018) Global and temporal spread of a taxonomically challenging invasive ant, Brachyponera chinensis (Hymenoptera: Formicidae). Fla Entomol 101:649–656

    Article  Google Scholar 

  • Hill MP, Chown SL, Hoffmann AA (2013) A predicted niche shift corresponds with increased thermal resistance in an invasive mite. Glob Ecol Biogeogr 22:942–951

    Article  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Belknap, Cambridge

    Book  Google Scholar 

  • Holway DA (1998) Factors governing rate of invasion: a natural experiment using Argentine ants. Oecologia 115:206–212

    Article  PubMed  Google Scholar 

  • Holway DA, Suarez AV, Case TJ (1998) Lose of intraspecific aggression in the success of a widespread invasive social insect. Science 282:949–952

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Huey RB, Stevenson R (1979) Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. Am Zool 19:357–366

    Article  Google Scholar 

  • Huszár DB, Larsen RS, Carlsen S et al (2014) Convergent development of ecological, genetic, and morphological traits in native supercolonies of the red ant Myrmica rubra. Behav Ecol Sociobiol 68:1859–1870

    Article  Google Scholar 

  • Ipser RM, Brinkman MA, Gardner WA et al (2004) A survey of ground-dwelling ants (Hymenoptera: Formicidae) in Georgia. Fla Entomol 87:253–260

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Korzukhin MD, Porter SD, Thompson LC et al (2001) Modeling temperature-dependent range limits for the fire ant Solenopsis invicta (Hymenoptera: Formicidae) in the United States. Ecol Entomol 30:645–655

    Article  Google Scholar 

  • Krushelnycky PD, Holway DA, LeBrun EG et al (2010) Invasion processes and causes of success. In: Lach L, Parr C, Abbott K (eds) Ant ecology. Oxford University Press, New York

    Google Scholar 

  • Lach L, Hooper-Bui LM (2009) Consequences of ant invasions. In: Lach L, Parr CL, Abbott KL (eds) Ant ecology. Oxford University Press, Oxford

    Chapter  Google Scholar 

  • Lafferty AJ (2018) Invasion and high-elevation acclimation of the red imported fire ant (Formicidae: Solenopsis invicta) in the Southern Blue Ridge escarpment region. Department of Biology, Western Carolina University, Cullowhee, NC

    Google Scholar 

  • Lee CE, Gelembiuk GW (2008) Evolutionary origins of invasive populations. Evol Appl 1:427–448

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Lubertazzi D (2012) The biology and natural history of Aphaenogaster rudis. Psyche 2012:752815

    Google Scholar 

  • Lucky A, Savage AM, Nichols LM et al (2014) Ecologists, educators, and writers collaborate with the public to assess backyard diversity in The School of Ants Project. Ecosphere 5:78

    Article  Google Scholar 

  • MacGown JA, Hill JG (2010) Annotated list of the ants of the Great Smoky Mountains National Park. Discover Life in America, Gatlinburg, TN

    Google Scholar 

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

    Article  Google Scholar 

  • Menzel TO (2012) Interactions between Aphaenogaster carolinensis (Hymenoptera: Formicidae) and four sympatric ant species. J Insect Behav 25:486–493

    Article  Google Scholar 

  • Moles AT, Flores-Moreno H, Bonser SP et al (2012) Invasions: the trail behind, the path ahead, and a test of a disturbing idea. J Ecol 100:116–127

    Article  Google Scholar 

  • Moran EV, Alexander JM (2014) Evolutionary responses to global change: lessons from invasive species. Ecol Lett 17:637–649

    Article  PubMed  Google Scholar 

  • Murata N, Tsuji K, Kikuchi T (2017) Social structure and nestmate discrimination in two species of Brachyponera ants distributed in Japan. Entomol Sci 20:86–95

    Article  Google Scholar 

  • 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 

  • 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 

  • Parr CL, Gibb H (2011) The discovery–dominance trade-off is the exception, rather than the rule. J Anim Ecol 81:233–241

    Article  PubMed  Google Scholar 

  • Paysen E (2007) Diversity and abundance of ants at forest edges in the Great Smoky Mountains National Park. Department of Entomology, Clemson University, Clemson, SC

    Google Scholar 

  • Pecarevic M, Danoff-Burg J, Dunn RR (2010) Biodiversity on Broadway—enigmatic diversity of the societies of ants (Formicidae) on the streets of New York City. PLoS ONE 5:e13222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Penick CA, Diamond SE, Sanders NJ, Dunn RR (2017) Beyond thermal limits: comprehensive metrics of performance identify key axes of thermal adaptation in ants. Funct Ecol 31:1091–1100

    Article  Google Scholar 

  • R Development Core Team Version 3.5.1 (2019) R: a language and environment for statistical computing, 3.5.0 edn. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • 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 

  • 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 

  • Roulston TH, Buczkowski G, Silverman J (2003) Nestmate discrimination in ants: effect of bioassay on aggressive behavior. Insectes Soc 50:151–159

    Article  Google Scholar 

  • Schlaepfer DR, Glattli M, Fischer M et al (2010) A multi-species experiment in their native range indicates pre-adaptation of invasive alien plant species. New Phytol 185:1087–1099

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Smith CR, Tillberg CV (2009) Stable isotope anlaysis and elemental analysis in ants. Cold Spring Harb Protoc 4:1–3

    Google Scholar 

  • Stachowicz JJ, Tilman D (2005) Species invasions and the relationships between species diversity, community saturation, and ecosystem functioning. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer, Sunderland, MA, pp 41–64

    Google Scholar 

  • Suarez AV, Holway DA, Case TJ (2001) Patterns of spread in biological invasions dominated by long-distance jump dispersal: insights from Argentine ants. Proc Natl Acad Sci USA 98:1095–1100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suarez AV, Holway DA, Ward PS (2005) The role of opportunity in the unintentional introduction of nonnative ants. Proc Natl Acad Sci USA 102:17032–17035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suarez AV, Holway DA, Tsutsui ND (2008) Genetics and behavior of a colonizing species: the invasive Argentine ant. Am Nat 172:S72–S84

    Article  PubMed  Google Scholar 

  • Suarez AV, McGlynn TP, Tsuitsui ND (2010) Biogeographic and taxonomic patterns of introduced ants. In: Lach L, Parr CL, Abbott KL (eds) Ant ecology. Oxford University Press, New York, pp 233–244

    Google Scholar 

  • Suehiro W, Hyodo F, Tanaka HO et al (2017) Radiocarbon analysis reveals expanded diet breadth associates with the invasion of a predatory ant. Sci Rep 7:15016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tillberg CV, Holway DA, LeBrun EG et al (2007) Trophic ecology of invasive Argentine ants in their native and introduced ranges. Proc Natl Acad Sci USA 104:20856–20861

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsutsui ND, Suarez AV, Holway DA et al (2000) Reduced genetic variation and the success of an invasive species. Proc Natl Acad Sci USA 97:5948–5953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warren II RJ (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. Accessed 12 Nov 2019

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

    Article  Google Scholar 

  • Warren RJ II, Chick L (2013) Upward ant distribution shift corresponds with minimum, not maximum, temperature tolerance. Glob Change Biol 19:2082–2088

    Article  Google Scholar 

  • 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 

  • Warren RJ II, Bahn V, Bradford MA (2011) Temperature cues phenological synchrony in ant-mediated seed dispersal. Glob Change Biol 17:2444–2454

    Article  Google Scholar 

  • Warren RJ II, Giladi I, Bradford MA (2012) Environmental heterogeneity and interspecific interactions influence occupancy be key seed-dispersing ants. Environ Entomol 41:463–468

    Article  PubMed  Google Scholar 

  • Warren RJ II, McMillan A, King JR et al (2015) Forest invader replaces predation but not dispersal services by a keystone species. Biol Invasions 23:3153–3162

    Article  Google Scholar 

  • Warren R II, Reed K, Mathew A et al (2018a) Release from intraspecific competition promotes dominance of a non-native invader. Biol Invasions 21:895–909

    Article  Google Scholar 

  • Warren II RJ, Mathew A, Reed K et al (2018b) Myrmica rubra microhabitat selection and putative ecological impact. Ecol Entomol (in press)

  • Wetterer JK (2015) Geographic origin and spread of cosmopolitan ants (Hymenoptera: Formicidae). Halteres 6:66–78

    Google Scholar 

  • Wilder SM, Holway DA, Suarez AV et al (2011) Intercontinental differences in resource use reveal the importance of mutualisms in fire ant invasions. Proc Natl Acad Sci USA 108:20639–20644

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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, Hungary

Download references

Acknowledgements

We would like to thank Ellie Sanders, Audrey Egler, Bethany Sharkey and David Reese from the Highlands Biological Station Climate Change Ecology course for field assistance. We also would like to thank Highlands Biological Station Director Jim Costa. We thank three anonymous reviewers for helpful comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. J. Warren II.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 46 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Warren, R.J., Candeias, M., Lafferty, A. et al. Regional-scale environmental resistance to non-native ant invasion. Biol Invasions 22, 813–825 (2020). https://doi.org/10.1007/s10530-019-02133-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-019-02133-3

Keywords

Navigation