Advertisement

Biological Invasions

, Volume 18, Issue 11, pp 3091–3101 | Cite as

Booms, busts and population collapses in invasive ants

Perpectives and paradigms

Abstract

The abundance of many invasive species can vary substantially over time, with dramatic population declines and local extinctions frequently observed in a wide range of taxa. We highlight population crashes of invasive ants, which are some of the most widespread and damaging invasive animals. Population collapse or substantial declines have been observed in nearly all of the major invasive ant species including the yellow crazy ant (Anoplolepis gracilipes), Argentine ants (Linepithema humile), big-headed or coastal brown ant (Pheidole megacephala), the tropical fire ant (Solenopsis geminata), red imported fire ants (Solenopsis invicta), and the little fire ant or electric ant (Wasmannia auropunctata). These declines frequently attract little attention, especially compared with their initial invasion phase. Suggested mechanisms for population collapse include pathogens or parasites, changes in the food availability, or even long-term effects of the reproductive biology of invasive ants. A critical component of the collapses may be a reduction in the densities of the invasive ant species, which are often competitively weak in low abundance. We propose that mechanisms causing a reduction in invasive ant abundance may initiate a local extinction vortex. Declines in abundance likely reduce the invasive ant’s competitive ability, resource acquisition and defense capability. These reductions could further reduce the abundance of an invasive ant species, and so on. Management of invasive ants through the use of pesticides is expensive, potentially ecologically harmful, and can be ineffective. We argue that pesticide use may even have the potential to forestall natural population declines and collapses. We propose that in order to better manage these invasive ants, we need to understand and capitalize on features of their population dynamics that promote population collapse.

Keywords

Boom and bust Population collapse Competition Pathogens and parasites Invasive ant Invasive species extinction vortex Management 

Notes

Acknowledgments

We thank two anonymous referees for providing valuable comments on this manuscript. P.J.L. was supported by a James Cook Fellowship from the Royal Society of New Zealand.

References

  1. Abbott KL (2005) Supercolonies of the invasive yellow crazy ant, Anoplolepis gracilipes, on an oceanic island: forager activity patterns, density and biomass. Insectes Sociaux 52:266–273. doi: 10.1007/s00040-005-0800-6 CrossRefGoogle Scholar
  2. Abbott KL, Abbott KL, Green PT, Green PT (2007) Collapse of an ant-scale mutualism in a rainforest on Christmas Island. Oikos 116:1238–1246. doi: 10.1111/j.2007.0030-1299.15629.x CrossRefGoogle Scholar
  3. Abbott KL, Abbott KL, Green PT et al (2014) Seasonal shifts in macronutrient preferences in supercolonies of the invasive Yellow Crazy Ant Anoplolepis gracilipes (Smith, 1857) (Hymenoptera: Formicidae) on Christmas Island, Indian Ocean. Austral Entomol 53:337–346. doi: 10.1111/aen.12081 CrossRefGoogle Scholar
  4. Adams ES, Tschinkel WR (2001) Mechanisms of population regulation in the fire ant Solenopsis invicta: an experimental study. J Anim Ecol 70:355–369. doi: 10.1046/j.1365-2656.2001.00501.x CrossRefGoogle Scholar
  5. Bouwma AM, Howard KJ, Jeanne RL (2005) Parasitism in a social wasp: effect of gregarines on foraging behavior, colony productivity, and adult mortality. Behav Ecol Sociobiol 59:222–233. doi: 10.2307/25063693 CrossRefGoogle Scholar
  6. Briano JA (2005) Long-term studies of the red imported fire ant, Solenopsis invicta, infected with the microsporidia Vairimorpha invictae and Thelohania solenopsae in Argentina. Environ Entomol 34:124–132. doi: 10.1603/0046-225X-34.1.124 CrossRefGoogle Scholar
  7. Callcott A-MA, Oi DH, Collins HL et al (2000) Seasonal studies of an isolated red imported fire ant (Hymenoptera: Formicidae) population in eastern Tennessee. Environ Entomol 29:788–794. doi: 10.1603/0046-225X-29.4.788 CrossRefGoogle Scholar
  8. Cerda X, Arnan X, Retana J (2013) Is competition a significant hallmark of ant (Hymenoptera: Formicidae) ecology? Myrmecol News 18:131–147Google Scholar
  9. Christian CE, Christian CE (2001) Consequences of a biological invasion reveal the importance of mutualism for plant communities. Nature 413:635–639. doi: 10.1038/35098093 CrossRefPubMedGoogle Scholar
  10. Cooling M, Hoffmann BD (2015) Here today, gone tomorrow: declines and local extinctions of invasive ant populations in the absence of intervention. Biol Invasions 17:3351–3357. doi: 10.1007/s10530-015-0963-7 CrossRefGoogle Scholar
  11. Cooling M, Hartley S, Sim DA, Lester PJ (2012) The widespread collapse of an invasive species: argentine ants (Linepithema humile) in New Zealand. Biol Lett 8:430–433. doi: 10.1098/rsbl.2011.1014 CrossRefPubMedGoogle Scholar
  12. Corin SE, Abbott KL, Ritchie PA, Lester PJ (2007) Large scale unicoloniality: the population and colony structure of the invasive Argentine ant (Linepithema humile) in New Zealand. Insectes Sociaux 54:275–282. doi: 10.1007/s00040-007-0942-9 CrossRefGoogle Scholar
  13. Cremer S, Ugelvig LV, Drijfhout FP et al (2008) The evolution of invasiveness in garden ants. Plos One 3:e3838. doi: 10.1371/journal.pone.0003838 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Crow JF (1994) Advantages of sexual reproduction. Dev Genet 15:205–213. doi: 10.1002/dvg.1020150303 CrossRefPubMedGoogle Scholar
  15. Drescher J, Bluthgen N, Schmitt T et al (2010) Societies drifting apart? Behavioural, genetic and chemical differentiation between supercolonies in the yellow crazy ant Anoplolepis gracilipes. Plos One 5:e13581–e13588. doi: 10.1371/journal.pone.0013581 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Feldhaar H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36:533–543. doi: 10.1111/j.1365-2311.2011.01318.x CrossRefGoogle Scholar
  17. Fluker SS, Beardsley JW (1970) Sympatric associations of three ants: Iridomyrmex humilis, Pheidole megacephala, and Anoplolepis longipes in Hawaii. Ann Entomol Soc Am 63:1290–1296CrossRefGoogle Scholar
  18. Foucaud J, Orivel J, Loiseau A et al (2010) Worldwide invasion by the little fire ant: routes of introduction and eco-evolutionary pathways. Evol Appl 3:363–374. doi: 10.1111/j.1752-4571.2010.00119.x CrossRefPubMedPubMedCentralGoogle Scholar
  19. Gilpin ME, Soulé ME (1986) Minimum viable populations: processes of species extinction. Sinauer, SunderlandGoogle Scholar
  20. Goldson SL, Bourdot GW, Brockerhoff EG et al (2015) New Zealand pest management: current and future challenges. J R Soc NZ 45:31–58. doi: 10.1080/03036758.2014.1000343 CrossRefGoogle Scholar
  21. Grangier J, Lester PJ (2011) A novel interference behaviour: invasive wasps remove ants from resources and drop them from a height. Biol Lett 7:664–667. doi: 10.1098/rsbl.2011.0165 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Grangier J, Lester PJ (2014) Carbohydrate scarcity increases foraging activities and aggressiveness in the ant Prolasius advenus (Hymenoptera: Formicidae). Ecol Entomol 39:684–692. doi: 10.1111/een.12146 CrossRefGoogle Scholar
  23. Grover CD, Kay AD, Monson JA et al (2007) Linking nutrition and behavioural dominance: carbohydrate scarcity limits aggression and activity in Argentine ants. Proc R Soc B 274:2951–2957. doi: 10.1098/rspb.2007.1065 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Gruber MAM, Hoffmann BD, Ritchie PA, Lester PJ (2012a) Genetic diversity is positively associated with fine-scale momentary abundance of an invasive ant. Ecol Evol 2:2091–2105. doi: 10.1002/ece3.313 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gruber MAM, Hoffmann BD, Ritchie PA, Lester PJ (2012b) The conundrum of the yellow crazy ant (Anoplolepis gracilipes) reproductive mode: no evidence for dependent lineage genetic caste determination. Insectes Sociaux 60:135–145. doi: 10.1007/s00040-012-0277-z CrossRefGoogle Scholar
  26. Gruber MAM, Burne AR, Abbott KL et al (2013) Population decline but increased distribution of an invasive ant genotype on a Pacific atoll. Biol Invasions 15:599–612. doi: 10.1007/s10530-012-0312-z CrossRefGoogle Scholar
  27. Haines IH, Haines JB (1978) Pest status of the crazy ant, Anoplolepis longipes (Jerdon) (Hymenoptera: Formicidae), in the Seychelles. Bull Entomol Res 68:627. doi: 10.1017/s0007485300009603 CrossRefGoogle Scholar
  28. Haines IH, Haines JB, Cherrett JM (1994) The impact and control of the crazy ant, Anoplolepis longipes (Jerd.), in the Seychelles. In: Williams DF (ed) Exotic ants: biology, impact, and control of introduced species. Westview Press, Boulder, pp 206–218Google Scholar
  29. Helanterä H, Strassmann JE, Carrillo J, Queller DC (2009) Unicolonial ants: where do they come from, what are they and where are they going? Trends Ecol Evol 24:341–349. doi: 10.1016/j.tree.2009.01.013 CrossRefPubMedGoogle Scholar
  30. Higes M, Meana A, Bartolomé C et al (2013) Nosema ceranae (Microsporidia), a controversial 21st century honey bee pathogen. Environ Microbiol Rep 5:17–29. doi: 10.1111/1758-2229.12024 CrossRefPubMedGoogle Scholar
  31. Holway DA (1999) Competitive mechanisms underlying the displacement of native ants by the invasive argentine ant. Ecology 80:238–251. doi: 10.1890/0012-9658 CrossRefGoogle Scholar
  32. Holway DA, Lach L, Suarez AV et al (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233. doi: 10.1146/annurev.ecolsys.33.010802.150444 CrossRefGoogle Scholar
  33. Human KG, Gordon DM (1996) Exploitation and interference competition between the invasive Argentine ant, Linepithema humile, and native ant species. Oecologia 105:405–412. doi: 10.2307/4221199 CrossRefGoogle Scholar
  34. Keller L (1995) Parasites, worker polymorphism, and queen number in social insects. Am Nat 145:842–847. doi: 10.1086/285772 CrossRefGoogle Scholar
  35. Keller L, Ross KG (1998) Selfish genes: a green beard in the red fire ant. Nature 394:573–575. doi: 10.1038/29064 CrossRefGoogle Scholar
  36. Lach L (2003) Invasive ants: unwanted partners in ant-plant interactions? Ann Missouri Bot Gard 90:91–108CrossRefGoogle Scholar
  37. Lach LL (2007) A mutualism with a native membracid facilitates pollinator displacement by Argentine ants. Ecology 88:1994–2004. doi: 10.1890/06-1767.1 CrossRefPubMedGoogle Scholar
  38. LeBrun E, Feener D (2002) Linked indirect effects in ant-phorid interactions: impacts on ant assemblage structure. Oecologia 133:599–607. doi: 10.1007/s00442-002-1068-4 CrossRefGoogle Scholar
  39. Lester PJ, Tavite A (2004) Long-legged ants, Anoplolepis gracilipes (Hymenoptera: Formicidae), have invaded Tokelau, changing composition and dynamics of ant and invertebrate communities. Pac Sci 58:391–401. doi: 10.1353/psc.2004.0031 CrossRefGoogle Scholar
  40. Lester PJ, Abbott KL, Sarty M, Burns KC (2009) Competitive assembly of South Pacific invasive ant communities. BMC Ecol 9:3. doi: 10.1186/1472-6785-9-3 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Lewis T, Cherrett JM, Haines I et al (1976) The crazy ant (Anoplolepis longipes (Jerd.) (Hymenoptera, Formicidae)) in Seychelles, and its chemical control. Bull Entomol Res 66:97. doi: 10.1017/s0007485300006520 CrossRefGoogle Scholar
  42. Mack RN, Simberloff D, Lonsdale WM et al (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710. doi: 10.1890/1051-0761(2000)010 CrossRefGoogle Scholar
  43. Macom TE, Porter SD (1996) Comparison of polygyne and monogyne red imported fire ant (Hymenoptera: Formicidae) population densities. Ann Entomol Soc Am 89:535–543. doi: 10.1093/aesa/89.4.535 CrossRefGoogle Scholar
  44. Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317:362–364. doi: 10.1126/science.1143046 CrossRefPubMedGoogle Scholar
  45. Mehdiabadi NJ, Kawazoe EA, Gilbert LE (2004) Phorid fly parasitoids of invasive fire ants indirectly improve the competitive ability of a native ant. Ecol Entomol 29:621–627. doi: 10.1111/j.0307-6946.2004.00636.x CrossRefGoogle Scholar
  46. Mikheyev AS, Mueller UG (2007) Genetic relationships between native and introduced populations of the little fire ant Wasmannia auropunctata. Divers Distrib 13:573–579. doi: 10.1111/j.1472-4642.2007.00370.x CrossRefGoogle Scholar
  47. Morrison LW (2000) Mechanisms of interspecific competition among an invasive and two native fire ants. Oikos 90:238–252. doi: 10.1034/j.1600-0706.2000.900204.x CrossRefGoogle Scholar
  48. Morrison LW (2002) Long-term impacts of an arthropod-community invasion by the imported fire ant, Solenopsis invicta. Ecology 83:2337–2345. doi: 10.1890/0012-9658 CrossRefGoogle Scholar
  49. O’Dowd DJ, Green PT, Lake PS (2003) Invasional “meltdown” on an oceanic island. Ecol Lett 6:812–817. doi: 10.1046/j.1461-0248.2003.00512.x CrossRefGoogle Scholar
  50. Pearcy M, Goodisman MAD, Keller L (2011) Sib mating without inbreeding in the longhorn crazy ant. Proc R Soc B 278:2677–2681. doi: 10.1098/rspb.2010.2562 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Plowes RM, Becnel JJ, Lebrun EG et al (2015) Myrmecomorba nylanderiae gen. et sp. nov., a microsporidian parasite of the tawny crazy ant Nylanderia fulva. J Invertebr Pathol 129:45–56. doi: 10.1016/j.jip.2015.05.012 CrossRefPubMedGoogle Scholar
  52. Porter SD, Savignano DA (1990) Invasion of polygyne fire ants decimates native ants and disrupts arthropod community. Ecology 71:2095–2106. doi: 10.2307/1938623 CrossRefGoogle Scholar
  53. Porter SD, Williams DF, Patterson RS, Fowler HG (1997) Intercontinental differences in the abundance of Solenopsis fire ants (Hymenoptera: Formicidae): escape from natural enemies? Environ Entomol 26:373–384. doi: 10.1093/ee/26.2.373 CrossRefGoogle Scholar
  54. Porter SD, Valles SM, Oi DH (2013) Host specificity and colony impacts of the fire ant pathogen, Solenopsis invicta virus 3. J Invertebr Pathol 114:1–6. doi: 10.1016/j.jip.2013.04.013 CrossRefPubMedGoogle Scholar
  55. Russell JA, Moreau CS, Goldman-Huertas B et al (2009) Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc Natl Acad Sci 106:21236–21241. doi: 10.1073/pnas.0907926106 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Sachs JL, Simms EL (2006) Pathways to mutualism breakdown. Trends Ecol Evol 21:585–592. doi: 10.1016/j.tree.2006.06.018 CrossRefPubMedGoogle Scholar
  57. Sagata K, Lester PJ (2009) Behavioural plasticity associated with propagule size, resources, and the invasion success of the Argentine ant Linepithema humile. J Appl Ecol 46:19–27. doi: 10.1111/j.1365-2664.2008.01523.x CrossRefGoogle Scholar
  58. Schroeder DC, Martin SJ (2012) Deformed wing virus: the main suspect in unexplained honeybee deaths worldwide. Virulence 3:589–591. doi: 10.4161/viru.22219 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Scott JG, Michel K, Bartholomay LC et al (2013) Towards the elements of successful insect RNAi. J Insect Physiol 59:1212–1221. doi: 10.1016/j.jinsphys.2013.08.014 CrossRefPubMedGoogle Scholar
  60. Sebastien A, Lester PJ, Hall RJ et al (2015) Invasive ants carry novel viruses in their new range and form reservoirs for a honeybee pathogen. Biol Lett 11:20150610. doi: 10.1098/rsbl.2015.0610 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Shykoff JA, Schmid-Hempel P (1991) Parasites and the advantage of genetic variability within social insect colonies. Proc R Soc B 243:55–58CrossRefGoogle Scholar
  62. Simberloff D, Gibbons L (2004) Now you see them, now you don’t—population crashes of established introduced species. Biol Invasions 6:161–172. doi: 10.1023/B:BINV.0000022133.49752.46 CrossRefGoogle Scholar
  63. Souza E, Follett PA, Price DK, Stacy EA (2008) Field suppression of the invasive ant Wasmannia auropunctata (Hymenoptera: Formicidae) in a tropical fruit orchard in Hawaii. J Econ Entomol 101:1068–1074. doi: 10.1093/jee/101.4.1068 CrossRefPubMedGoogle Scholar
  64. Strayer DL, Eviner VT, Jeschke JM, Pace ML (2006) Understanding the long-term effects of species invasions. Trends Ecol Evol 21:645–651. doi: 10.1016/j.tree.2006.07.007 CrossRefPubMedGoogle Scholar
  65. Tarpy DR (2003) Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc R Soc B 270:99–103. doi: 10.1098/rspb.2002.2199 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Tennant LE, Porter SD (1991) Comparison of diets of two fire ant species (Hymenoptera: Formicidae): solid and liquid components. J Entomol Sci 26:450–465Google Scholar
  67. Tillberg CVC, Holway DAD, Lebrun EGE, Suarez AVA (2007) Trophic ecology of invasive Argentine ants in their native and introduced ranges. Proc Natl Acad Sci USA 104:20856–20861. doi: 10.1073/pnas.0706903105 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Tindo M, Mbenoun Masse PS, Kenne M et al (2012) Current distribution and population dynamics of the little fire ant supercolony in cameroon. Insectes Sociaux 59:175–182. doi: 10.1007/s00040-011-0202-x CrossRefGoogle Scholar
  69. Torres JA, Snelling RR (1997) Biogeography of Puerto Rican ants: a non-equilibrium case? Biodivers Conserv 6:1103–1121. doi: 10.1023/A:1018332117719 CrossRefGoogle Scholar
  70. Towns DR, Atkinson IAE, Daugherty CH (2006) Have the harmful effects of introduced rats on islands been exaggerated? Biol Invasions 8:863–891. doi: 10.1007/s10530-005-0421-z CrossRefGoogle Scholar
  71. Tragust S, Feldhaar H, Espadaler X, Pedersen JS (2015) Rapid increase of the parasitic fungus Laboulbenia formicarum in supercolonies of the invasive garden ant Lasius neglectus. Biol Invasions 17:2795–2801. doi: 10.1007/s10530-015-0917-0 CrossRefGoogle Scholar
  72. Ugelvig LV, Kronauer DJC, Schrempf A et al (2010) Rapid anti-pathogen response in ant societies relies on high genetic diversity. Proc R Soc B 277:2821–2828. doi: 10.1098/rspb.2010.0644 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Valles SM, Oi DH, Yu F et al (2012) Metatranscriptomics and pyrosequencing facilitate discovery of potential viral natural enemies of the invasive Caribbean crazy ant, Nylanderia pubens. Plos One 7:e31828. doi: 10.1371/journal.pone.0031828 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Van Wilgenburg E, Torres CW, Tsutsui ND (2010) The global expansion of a single ant supercolony. Evol Appl 3:136–143. doi: 10.1111/j.1752-4571.2009.00114.x CrossRefPubMedPubMedCentralGoogle Scholar
  75. Ward DF, Stanley MC (2012) Site occupancy and detection probability of Argentine ant populations. J Appl Entomol 137:197–203. doi: 10.1111/j.1439-0418.2012.01722.x CrossRefGoogle Scholar
  76. Wetterer JK, Espadaler X, Wetterer AL et al (2006) Long-term impact of exotic ants on the native ants of Madeira. Ecol Entomol 31:358–368. doi: 10.1111/j.1365-2311.2006.00790.x CrossRefGoogle Scholar
  77. Wetterer JK, Davis O, Williamson JR (2014) Boom and bust of the tawny crazy ant, Nylanderia Fulva (Hymenoptera: Formicidae), on St. Croix, US Virgin Islands. Fla Entomol 97:1099–1103CrossRefGoogle Scholar
  78. Wilson EO (1976) The organization of colony defense in the ant Pheidole dentata Mayr (Hymenoptera: Formicidae). Behav Ecol Sociobiol 1:63–81CrossRefGoogle Scholar
  79. Wilson EO (2005) Environment: early ant plagues in the New World. Nature 433:32. doi: 10.1038/433032a CrossRefPubMedGoogle Scholar
  80. Wittman SE (2014) Impacts of invasive ants on native ant communities (Hymenoptera: Formicidae). Myrmecol News 19:111–123Google Scholar
  81. Yang C-C, Yu Y-C, Valles SM et al (2010) Loss of microbial (pathogen) infections associated with recent invasions of the red imported fire ant Solenopsis invicta. Biol Invasions 12:3307–3318. doi: 10.1007/s10530-010-9724-9 CrossRefGoogle Scholar
  82. Zhang H, Li H-C, Miao X-X (2012) Feasibility, limitation and possible solutions of RNAi-based technology for insect pest control. Insect Sci 20:15–30. doi: 10.1111/j.1744-7917.2012.01513.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.School of Biological SciencesVictoria University of WellingtonWellingtonNew Zealand
  2. 2.Pacific BiosecurityWellingtonNew Zealand

Personalised recommendations