Biological Invasions

, Volume 12, Issue 7, pp 2051–2057 | Cite as

Invasive Argentine ants reduce fitness of red maple via a mutualism with an endemic coccid

Original Paper

Abstract

Many invasive ant species form mutualisms with honeydew-producing Hemiptera and their aggressive presence deters the natural enemies of the Hemiptera. Invasive ant species like the Argentine ant have often been associated with hemipteran outbreaks in urban, agricultural and natural ecosystems. We investigated the effects of a mutualism between the invasive Argentine ant and the endemic terrapin scale on coccid density and the fitness of the host of this mutualism, the endemic red maple, situated in a commercial park. The terrapin scale has numerous natural enemies and we predicted that the high terrapin scale numbers associated with tending Argentine ants would collapse once Argentine ants were excluded from the host tree canopy. We predicted that excluding the Argentine ant from the tree canopy would result in an indirect net fitness benefit to the host. Terrapin scale numbers collapsed when Argentine ants were excluded from the host tree canopy. Red maples with Argentine ants excluded from their canopy had higher seed mass and larger early leaves indicating that this invasive ant-endemic scale mutualism imposed a net fitness cost to the host tree. The Argentine ant has yet to invade closed-canopy forest within its introduced range. The red maple is common in adjacent closed-canopy forest fragments and recent work has shown that invasion of these forest fragments by the Argentine ant is limited by a steady carbohydrate resource. We discuss the implications to forest invasion posed by a mutualism involving the Argentine ant and an endemic coccid.

Keywords

Coccidae Host fitness Invasion Linepithema humile Mesolecanium nigrofasciatum Mutualism 

References

  1. Abbott KL, Green PT (2007) Collapse of an ant-scale mutualism in a rainforest on Christmas Island. Oikos 116:1238–1246CrossRefGoogle Scholar
  2. Abou-Zaid MM, Helson BV, Nozzolillo C, Arnason JT (2001) Ethyl m-digallate from red maple, Acer rubrum L., as the major resistance factor to forest tent caterpillar, Malacosoma disstra Hbn. J Chem Ecol 27:2517–2527CrossRefPubMedGoogle Scholar
  3. Altfield L, Stiling P (2006) Argentine ants strongly affect some but not all common insects in Baccharis halimifolia. Environ Entomol 35:31–36CrossRefGoogle Scholar
  4. Altfield L, Stiling P (2009) Effects of aphid-tending Argentine ants, nitrogen enrichment and early-season herbivory on insects hosted by a coastal shrub. Biol Invasions 11:183–191CrossRefGoogle Scholar
  5. Bartlett BR (1961) The influence of ants upon parasites, predators, and scale insects. Ann Entomol Soc Am 54:543–551Google Scholar
  6. Blancafort X, Gomez C (2005) Consequences of the Argentine ant, Linepithema humile (Mayr), invasion on pollination of Euphorbia characias (L.) (Euphorbiaceae). Acta Oecol 28:49–55CrossRefGoogle Scholar
  7. Bolger DT, Suarez AV, Crooks KR, Morrison SA, Case TJ (2000) Arthropods in urban habitat fragments in southern California: area, age, and edge effects. Ecol Appl 10:1230–1248CrossRefGoogle Scholar
  8. Bond W, Slingsby P (1984) Collapse of an ant-plant mutualism: the Argentine ant (Iridomyrmex humilis) and myrmecochorous Proteaceae. Ecology 65:1031–1037CrossRefGoogle Scholar
  9. Brightwell RJ, Silverman J (2009) Effects of honeydew-producing hemipteran denial on local Argentine ant distribution and boric acid bait performance. J Econ Entomol 102:1170–1174CrossRefPubMedGoogle Scholar
  10. Bronstein JL (1994) Our current understanding of mutualism. Q Rev Biol 69:31–51CrossRefGoogle Scholar
  11. Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecology. Trends Ecol Evol 18:119–125CrossRefGoogle Scholar
  12. Buckley RC (1987) Interactions involving plants, homoptera, and ants. Annu Rev Ecol Syst 18:111–135CrossRefGoogle Scholar
  13. Buczkowski G, Vargo EL, Silverman J (2004) The diminutive supercolony: the Argentine ants of the southeastern United States. Mol Ecol 13:2235–2242CrossRefPubMedGoogle Scholar
  14. Cole FR, Medeiros AC, Loope LL, Zuehlke WW (1992) Effects of the Argentine ant on arthropod fauna of Hawaiian high-elevation shrubland. Ecology 73:1313–1322CrossRefGoogle Scholar
  15. Coppler LB, Murphy JF, Eubanks MD (2007) Red imported fire ants (Hymenoptera: Formicidae) increase the abundance of aphids in tomato. Fla Entomol 90:419–425CrossRefGoogle Scholar
  16. Critchfield WB (1971) Shoot growth and heterophylly in Acer. J Arnold Abor 52:240–266Google Scholar
  17. Daane KM, Sime KR, Fallon J, Cooper ML (2007) Impacts of Argentine ants on mealybugs and their natural enemies in California coastal vineyards. Ecol Entomol 32:583–596CrossRefGoogle Scholar
  18. Devorshak C (1994) The biology of natural enemies of terrapin scale on blueberries in North Carolina. Masters thesis. North Carolina State University. p 66Google Scholar
  19. Espadaler X, Gomez C (2003) The Argentine ant, Linepithema humile, in the Iberian Peninsula. Sociobiology 42:187–192Google Scholar
  20. Eubanks MD, Strysky JD (2006) Ant-Hemipteran mutualisms: keystone interactions that alter food web dynamics and influence plant fitness. In: Brodeur J, Boivin G (eds) Trophic and guild interactions in biological control, progress in biological control series. Springer, New York, pp 171–190CrossRefGoogle Scholar
  21. Gottshalk KW (1994) Shade, leaf growth, and crown development of Quercus rubra, Quercus velutina, Prunus serotina and Acer rubrum seedlings. Tree Physiol 14:735–749Google Scholar
  22. Hill M, Holm K, Vel T, Shah NJ, Matyot P (2003) Impact of the introduced yellow crazy ant Anoplolepis gracilipes on Bird Island, Seychelles. Biodivers Conserv 12:1969–1984CrossRefGoogle Scholar
  23. Holway DA (1998) Effect of Argentine ant invasions on ground-dwelling arthropods in northern California riparian woodlands. Oecologia 116:252–258CrossRefGoogle Scholar
  24. Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233CrossRefGoogle Scholar
  25. Human KG, Gordon DM (1997) Effects of Argentine ants on invertebrate biodiversity in northern California. Conserv Biol 11:1242–1248CrossRefGoogle Scholar
  26. Kaplan I, Eubanks MD (2005) Aphids alter the community-wide impact of fire ants. Ecology 86:1640–1649CrossRefGoogle Scholar
  27. Kikuzawa K (1983) Leaf survival of woody plants in deciduous broad leaved forests. Can J Bot 61:2133–2139Google Scholar
  28. Lach L (2003) Invasive ants: unwanted partners in ant-plant interactions? Ann Mo Bot Gard 90:91–108CrossRefGoogle Scholar
  29. Lach L (2007) A mutualism with a native membracid facilitates pollinator displacement by Argentine ants. Ecology 88:1994–2004CrossRefPubMedGoogle Scholar
  30. Loughrin JH, Potter DA, Hamilton-Kemp TR, Byers ME (1997) Response of Japanese beetles (Coleoptera: Scarabaeidae) to leaf volatiles of susceptible and resistant maple species. Environ Entomol 26:334–342Google Scholar
  31. Menke SB, Holway DA (2006) Abiotic factors control invasion by ants at the community scale. J Anim Ecol 75:368–376CrossRefPubMedGoogle Scholar
  32. Meyer JR, Nalepa CA, Devorshak C (2001) A new species of Anicetus (Hymenoptera: Encyrtidae) parasitizing terrapin scale, Mesolecanium nigrofasciatum (Hemiptera: Coccidae). Fla Entomol 84:686–690CrossRefGoogle Scholar
  33. Müller-Schwarze D, Schulte BA, Sun L, Müller-Schwarze C, Müller-Schwarze A (1994) Red maple (Acer rubrum) inhibits feeding by beaver (Castor canadiensis). J Chem Ecol 20:2021–2034CrossRefGoogle Scholar
  34. Ness JH, Bronstein JL (2004) The effects of invasive ants on prospective ant mutualists. Biol Invasions 6:445–461CrossRefGoogle Scholar
  35. O’Dowd DJ, Green PT, Lake PS (2003) Invasional ‘meltdown’ on an oceanic island. Ecol Lett 6:812–817CrossRefGoogle Scholar
  36. Oliveras J, Bas JM, Casellas D, Gomez C (2005) Numerical dominance of the Argentine ant vs. native ants and consequences on soil resource searching in Mediterranean cork-oak forests (Hymenoptera: Formicidae). Sociobiology 45:643–658Google Scholar
  37. Rowles AD, O’Dowd DJ (2007) Interference competition by Argentine ants displaces native ants: implications for biotic resistance to invasion. Biol Invasions 9:73–85CrossRefGoogle Scholar
  38. Rowles AD, O’Dowd DJ (2009a) Impacts of the invasive Argentine ant on native ants and other invertebrates in coastal scrub in south-eastern Australia. Aust Ecol 34:239–248CrossRefGoogle Scholar
  39. Rowles AD, O’Dowd DJ (2009b) New mutualism for old: indirect disruption and direct facilitation of seed dispersal following Argentine ant invasion. Oecologia 158:709–716CrossRefPubMedGoogle Scholar
  40. Rowles AD, Silverman J (2009) Carbohydrate supply limits invasion of natural communities by Argentine ants. Oecologia 161:161–171CrossRefPubMedGoogle Scholar
  41. Sanders NJ, Gotelli NJ, Heller NE, Gordon DM (2003) Community disassembly by an invasive species. Proc Natl Acad Sci USA 100:2474–2477CrossRefPubMedGoogle Scholar
  42. SAS (2002) Institute Inc., SAS 9.1.3 Help and Documentation, Cary, NC: SAS Institute Inc. 2000–2004Google Scholar
  43. Seastedt TR, Crossley DA, Hargrove WW (1983) The effects of low-level consumption by canopy arthropods on the growth and nutrient dynamics of black locust and red maple trees in the southern Appalachians. Ecology 64:1040–1048CrossRefGoogle Scholar
  44. Simanton FL (1916) The terrapin scale: an important insect enemy of peach orchards. USDA Tech Bull No. 351. pp 96Google Scholar
  45. Strysky JD, Eubanks MD (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proc R Soc B 274:151–164CrossRefGoogle Scholar
  46. Suarez AV, Holway DA, Case TJ (2001) Patterns of spread in biological invasions dominated by long-distance dispersal: insights from Argentine ants. Proc Natl Acad Sci USA 98:1095–1100CrossRefPubMedGoogle Scholar
  47. Trumble JT, Kolodny-Hirsh DM, Ting IP (1993) Plant compensation for arthropod herbivory. Annu Rev Entomol 38:93–119CrossRefGoogle Scholar
  48. Tsialtas JT, Maslaris N (2005) Leaf area estimation in a sugar beet cultivar by linear models. Photosynthetica 43:477–479CrossRefGoogle Scholar
  49. Walters AC (2006) Invasion of Argentine ants (Hymenoptera: Formicidae) in South Australia: impacts on community composition and abundance of invertebrates in urban parklands. Austral Ecol 31:567–576CrossRefGoogle Scholar
  50. Walters RS, Yawney HW (1990) Red Maple. In: Burns RM, Honkala BH (eds) Silvics of North America, vol 2. Hardwoods. USDA Forest Service, Washington, http://www.na.fs.fed.us/pubs/silvics_manual/Volume_2/acer/rubrum.htm
  51. Ward PS (1987) Distribution of the introduced Argentine ant (Iridomyrmex humilis) in natural habitats of the lower Sacramento Valley and its effects on the indigenous ant fauna. Hilgardia 55:1–16Google Scholar
  52. Ward DF, Harris RJ (2005) Invasibility of native habitats by Argentine ants, Linepithema humile, in New Zealand. N Z J Ecol 29:215–219Google Scholar
  53. Way MJ (1963) Mutualism between ants and honeydew-producing homoptera. Annu Rev Entomol 8:307–344CrossRefGoogle Scholar
  54. Westoby M (1998) A leaf-height-seed (LHS) plant ecology strategy scheme. Plant Soil 199:213–227CrossRefGoogle Scholar
  55. Westoby M, Leishman M, Lord J (1996) Comparative ecology of seed size and dispersal. Philos Trans R Soc B 351:1309–1318CrossRefGoogle Scholar
  56. Williams ML, Kosztarab M (1972) Morphology and systematics of the Coccidae of Virginia with notes on their biology. Virginia Polytech Inst & State Univ Res Div Bull 74:84–90Google Scholar
  57. Williams L, Martinson TE (2003) Nondestructive leaf area estimation of ‘Niagara’ and ‘DeChaunac’ grapevines. Sci Hortic 98:493–498CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Department of EntomologyNorth Carolina State UniversityRaleighUSA

Personalised recommendations