Arthropod-Plant Interactions

, Volume 3, Issue 2, pp 75–85 | Cite as

Honeydew collection by the invasive garden ant Lasius neglectus versus the native ant L. grandis

  • Carolina Ivon Paris
  • Xavier Espadaler
Original Paper


Honeydew collection performed by the invasive ant Lasius neglectus and by the native ant L. grandis was compared. The invasive ant collected 2.09 kg of honeydew per tree while the native ant collected 0.82 kg. The aphid Lachnus roboris was visited by both ant species. In holm oaks colonized by L. neglectus, aphid abundance tended to increase and its honeydew production increased twofold. The percentage of untended aphids was lower in holm trees occupied by L. neglectus. As tending ants also prey on insects, we estimated the percentage of carried insects. The native ant workers carried more insects than the invasive ant. Both ant species preyed mainly on Psocoptera and the rarely tended aphid, Hoplocallis picta. We conclude that the higher honeydew collection achieved by L. neglectus was the consequence of (1) its greater abundance, which enabled this ant to tend more Lachnus roboris and (2) its greater level of attention towards promoting an increase of honeydew production.


Aphid–ant mutualism Invasive ants Lachnus roboris Quercus ilex 



We thank Nicolas Pérez Hidalgo (University of León) for aphid identification, and Elizabeth Padilla, María Teresa Salvadó, and Montse Robledo for their help in the estimation of honeydew production. Carolina Paris would like to thank the Government of Catalonia for the grant for young researchers (2003FI 00342). Funding was provided by MEC/FEDER CGL 2004-05240-CO2/01 and CGL2007-64080-C02-01.


  1. Abbott KL (2005) Supercolonies of the invasive yellow crazy ant, Anoplolepis gracilipes, on an oceanic island: forager activity patterns, density and biomass. Insectes Soc 52:266–273. doi: 10.1007/s00040-005-0800-6 CrossRefGoogle Scholar
  2. Auclair JL (1963) Aphid feeding and nutrition. Annu Rev Entomol 8:439–490. doi: 10.1146/annurev.en.08.010163.002255 CrossRefGoogle Scholar
  3. Ayre GL (1959) Foods habits of Formica subnitens Creighton (Hymenoptera: Formicidae) at Westbank, British Columbia. Insectes Soc 4:105–114. doi: 10.1007/BF02225946 CrossRefGoogle Scholar
  4. Banks C, Nixon H (1958) Effects of the ant Lasius niger, on the feeding and excretion of the bean aphid, Aphis fabae Scop. Exp Biol 35:703–711Google Scholar
  5. Blüthgen N, Stork N, Fiedler K (2004) Bottom–up control and co-occurrence in complex communities: honeydew and nectar determine a rainforest ant mosaic. Oikos 106:344–358. doi: 10.1111/j.0030-1299.2004.12687.x CrossRefGoogle Scholar
  6. Breton LM, Addicott JF (1992) Density-dependent mutualism in an aphid–ant interaction. Ecology 73:2175–2180. doi: 10.2307/1941465 CrossRefGoogle Scholar
  7. Canadell J, Riba M, Pilar A (1988) Biomass equations for Quercus ilex L. in the Montseny Massif, northeastern Spain. Forestry 61:137–147. doi: 10.1093/forestry/61.2.137 CrossRefGoogle Scholar
  8. Cannon C, Fell R (2002) Patterns of macronutrient collection in the black carpenter ant Camponotus pennsylvanicus (De Geer) (Hymenoptera: Formicidae). Environ Entomol 31(6):977–981Google Scholar
  9. Carroll CR, Janzen DH (1973) Ecology of foraging by ants. Annu Rev Ecol Syst 4:231–257. doi: 10.1146/ CrossRefGoogle Scholar
  10. Collins M, Leather S (2002) Ant-mediated dispersal by the black willow aphid Pterocoma salicis L.; does the ant Lasius niger L. judge aphid-host quality? Ecol Entomol 27:238–241. doi: 10.1046/j.1365-2311.2002.00390.x CrossRefGoogle Scholar
  11. Cremer S, Ugelvig L, Lommen S, Petersen K, Pedersen J (2006) Attack of the invasive garden ant: aggression behaviour of Lasius neglectus (Hymenoptera: Formicidae) against native Lasius species in Spain. Myrmecol News 9:13–19Google Scholar
  12. Cushman JH (1991) Host–plant mediation of insect mutualism: variable outcomes in herbivore–ant interactions. Oikos 61:138–144. doi: 10.2307/3545416 CrossRefGoogle Scholar
  13. Davidson DW (1998) Resource discovery vs resource domination in ants: a functional mechanism for breaking the trade-off. Ecol Entomol 23:484–490. doi: 10.1046/j.1365-2311.1998.00145.x CrossRefGoogle Scholar
  14. Degen AA, Gersani M (1989) Environmental effects on activity and honeydew collection by the weaver ant Polyrhachis simplex (Hymenoptera: Formicidae) when attending the mealybug Trabutina sp (Homoptera: Pseudococcidae). J Zool (Lond) 218:421–432CrossRefGoogle Scholar
  15. Del Claro K, Oliveira PS (1996) Honeydew flicking by treehoppers provides cues to potential tending ants. Anim Behav 51:1071–1075. doi: 10.1006/anbe.1996.0108 CrossRefGoogle Scholar
  16. Dixon AFG (1997) Aphid ecology. Chapman & Hall, LondonGoogle Scholar
  17. Dreisig H (1988) Foraging rate of ants collecting honeydew or extrafloral nectar, and some possible constrains. Ecol Entomol 13:143–154. doi: 10.1111/j.1365-2311.1988.tb00342.x CrossRefGoogle Scholar
  18. Dungan RJ, Kelly D (2003) Effect of host tree and environmental variables on honeydew production by scale insects (Ultracoelostoma sp.) in a high elevation Nothofagus solandri forest. N Z J Ecol 27:169–177Google Scholar
  19. Espadaler X, Rey S, Bernal V (2004) Queen number in a supercolony of the invasive garden ant, Lasius neglectus. Insectes Soc 51:232–238. doi: 10.1007/s00040-003-0732-y CrossRefGoogle Scholar
  20. Feller JH (1989) Daily and seasonal activity in woodland ants. Oecologia 78:69–76. doi: 10.1007/BF00377199 CrossRefGoogle Scholar
  21. Fisher M, Völk W, Schopf R, Hoffmann K (2002) Age-specific patterns in honeydew production and honeydew composition in the aphid Metopeurum fuscoviride: implications for ant-attendance. J Insect Physiol 48:319–326. doi: 10.1016/S0022-1910(01)00179-2 CrossRefGoogle Scholar
  22. Flatt T, Weisser W (2000) The effects of mutualistic ants on aphid life history traits. Ecology 81:3522–3529Google Scholar
  23. Fowles AP (1994) A review of the ecology of the red wood ant Fomica rufa and its status in Wales. Conserv Ecol Wales 1:1–25Google Scholar
  24. Fritz RS (1983) Ant protection of a host plant’s defoliator: consequence of an ant-membracid mutualism. Ecology 64:789–797. doi: 10.2307/1937202 CrossRefGoogle Scholar
  25. Gibb H, Hochuli D (2003) Colonisation by a dominant ant facilitated by anthropogenic disturbance: effects on ant assemblage composition, biomass and resource use. Oikos 103:469–478. doi: 10.1034/j.1600-0706.2003.12652.x CrossRefGoogle Scholar
  26. Harada Y (2005) Diel and seasonal patterns of foraging activity in the arboreal ant Crematogaster matsumurai Forel. Entomol Sci 8:167–172. doi: 10.1111/j.1479-8298.2005.00115.x CrossRefGoogle Scholar
  27. Helms KR, Vinson SB (2002) Wide spread association of the invasive ant Solenopsis invicta with an invasive mealybug. Ecology 83:2425–2438Google Scholar
  28. Herzig J (1937) Ameisen und Blattläuse. Z Angew Entomol 24:367–435Google Scholar
  29. Holec M, Frouz J (2005) Ant (Hymenoptera: Formicidae) communities in reclaimed and unreclaimed brown coal mining spoil dumps in the Czech Republic. Pedobiologia (Jena) 49:345–357. doi: 10.1016/j.pedobi.2005.03.001 CrossRefGoogle Scholar
  30. Hölldobler B, Wilson E (1990) The ants. Belknap, CambridgeGoogle Scholar
  31. Holway D, Lach L, Suarez A, Tsutsui N, Case T (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
  32. Itioka T, Inoue T (1999) The alternation of mutualistic ant species affects the population growth of their trophobiont mealybug. Ecography 22:169–177. doi: 10.1111/j.1600-0587.1999.tb00465.x CrossRefGoogle Scholar
  33. Ito F, Higashi S (1991) Variance of ant effects on different life forms of moth caterpillars. J Anim Ecol 60:327–334. doi: 10.2307/5463 CrossRefGoogle Scholar
  34. James DG, Stevens MM, O’Malley KJ, Faulder RJ (1999) Ant foraging reduces the abundance of beneficial and incidental arthropods in citrus canopies. Biol Control 14:121–126. doi: 10.1006/bcon.1998.0678 CrossRefGoogle Scholar
  35. Jensen TF (1976) An energy budget for a field population of Formica pratensis Retz (Hymenoptera: Formicidae). Nat Jutl 20:203–226Google Scholar
  36. Katayama N, Suzuki N (2002) Cost and benefit of ant attendance of Aphis craccivora (Hemiptera: Aphididae) with reference to aphid colony size. Can Entomol 134:241–249CrossRefGoogle Scholar
  37. Kindlmann P, Hulle M, Stadler B (2007) Timing of dispersal: effect of ants on aphids. Oecologia 152:625–631. doi: 10.1007/s00442-007-0684-4 PubMedCrossRefGoogle Scholar
  38. Lach L (2003) Invasive ants: unwanted partners in ant–plant interactions? Ann Mo Bot Gard 90:91–108. doi: 10.2307/3298529 CrossRefGoogle Scholar
  39. Mailleux AC, Deneubourg JL, Detrain C (2003) Regulation of ants’ foraging to resource productivity. Proc R Soc Lond B Biol Sci 270:1609–1616. doi: 10.1098/rspb.2003.2398 CrossRefGoogle Scholar
  40. Matsuura K, Yashiro Y (2006) Aphid egg protection by ants: a novel aspect of the mutualism between the tree-feeding aphid Stomaphis hirukawai and its attendant ant Lasius productus. Naturwissenschaften 93:06–510CrossRefGoogle Scholar
  41. Melia A, Cabezuelo P, Fernández de Córdoba J (1993) Incidencia de pulgones (Homoptera, Aphididae) en encinares de Córdoba. Bol Sanid Veg Plagas 19:355–360Google Scholar
  42. Michel E (1942) Beiträge zur Kenntnis von Lachnus (Pterochlorus) roboris L., einer wichtigen Honigtauerzeugerin an der Eiche. Z Angew Entomol 29:243–281Google Scholar
  43. Mittler T (1958) The excretion of honeydew by Tuberolachnus salignus (Gmelin) (Homoptera: Aphididae). Proc R Ent Soc Lond A 33:49–55Google Scholar
  44. Mooney K, Tillberg C (2005) Temporal and spatial variation to ant omnivory in pine forests. Ecology 86:1225–1235. doi: 10.1890/04-0938 CrossRefGoogle Scholar
  45. Ness JH, Bronstein JL (2004) The effects of invasive ants on prospective ant mutualists. Biol Inv 6:445–461. doi: 10.1023/B:BINV.0000041556.88920.dd CrossRefGoogle Scholar
  46. Nixon GEJ (1951) The association of ants with aphids and coccids. Commonwealth Institute of Entomology, LondonGoogle Scholar
  47. Nonacs P (2002) Patterns of energy allocation within foragers of Formica planipilis and Pogonomyrmex salinus. West N Am Nat 62:188–196Google Scholar
  48. Offenberg J (2001) Balancing between mutualism and exploitation: the symbiotic interaction between Lasius ants and aphids. Behav Ecol Sociobiol 49:304–310. doi: 10.1007/s002650000303 CrossRefGoogle Scholar
  49. Paris C (2005) Mutualismo de la hormiga invasora Lasius neglectus (Hymenoptera: Formicidae) y el áfido Lachnus roboris (Homoptera: Lachnidae) en un encinar urbano. MSc thesis. Autonomous University of Barcelona, BarcelonaGoogle Scholar
  50. Pontin AJ (1960) Observations on the keeping of aphid eggs by ants of the genus Lasius. Ent Month Mag 96:198–199Google Scholar
  51. Renault CK, Buffa LM, Delfino MA (2005) An aphid–ant interaction: effects on different trophic levels. Ecol Res 20:71–74. doi: 10.1007/s11284-004-0015-8 CrossRefGoogle Scholar
  52. Rico-Gray V, Castro G (1996) Effect of an ant–aphid interaction on the reproductive fitness of Paullinia fuscecens (Sapindaceae). Southwest Nat 41:434–440Google Scholar
  53. Sakata H (1995) Density-dependant predation of the ant Lasius niger (Hymenoptera: Formicidae) on two attended aphids Lachnus tropicallis and Myzocallis kuricola (Homoptera: Aphididae). Res Popul Ecol (Kyoto) 37:159–164. doi: 10.1007/BF02515816 CrossRefGoogle Scholar
  54. Santini G, Tucci L, Ottonetti L, Frizzi F (2007) Competition trade-offs in the organisation of a Mediterranean ant assemblage. Ecol Entomol 32:319–326. doi: 10.1111/j.1365-2311.2007.00882.x CrossRefGoogle Scholar
  55. Seifert B (1992) A taxonomic revision of the Palaeartic members of the ant subgenus Lasius s.str. (Hymenoptera, Formicidae). Abh Ber Naturkundemus Gorlitz 66:1–67Google Scholar
  56. Simberloff D, Von Holle B (1999) Positive interactions of nonidigenous species: invasional meltdown? Biol Inv 1:21–32. doi: 10.1023/A:1010086329619 CrossRefGoogle Scholar
  57. Sipura M (2002) Contrasting effects of ants on the herbivory and growth of two willow species. Ecology 83:2680–2690CrossRefGoogle Scholar
  58. Skinner GJ (1980) The feeding habitats of the wood ant Formica rufa (Hymenoptera: Formicidae), in limestone woodland in northwest England. J Anim Ecol 49:417–433. doi: 10.2307/4255 CrossRefGoogle Scholar
  59. Stadler B, Dixon AFG (1999) Ant attendance in aphid: why different degrees of myrmecology? Ecol Entomol 24:363–369. doi: 10.1046/j.1365-2311.1999.00195.x CrossRefGoogle Scholar
  60. Stadler B, Andreas Schramm A, Kalbitz K (2005) Ant-mediated effects on spruce litter decomposition, solution chemistry, and microbial activity. Soil Biol Biochem 38:561–572. doi: 10.1016/j.soilbio.2005.06.010 CrossRefGoogle Scholar
  61. StatSoft Inc (2001) Statistica (data analysis software system), version 6. StatSoft, Tulsa, OK. Available at:
  62. Sudd JH, Sudd ME (1985) Seasonal changes in the responses of wood ants (Formica lugubris) to sucrose baits. Ecol Entomol 10:89–97. doi: 10.1111/j.1365-2311.1985.tb00538.x CrossRefGoogle Scholar
  63. Takeda S, Kinomura K, Sakurai H (1982) Effects of ant attendance on the honeydew excretion and larviposition of the cowpea aphid Aphis craccivora Koch. Appl Entomol Zool (Jpn) 17:133–135Google Scholar
  64. Völk W (1992) Aphids or their parasitoids: who actually benefits from ant-attendance? J Anim Ecol 61:273–281. doi: 10.2307/5320 CrossRefGoogle Scholar
  65. Way MJ (1963) Mutualisms between ants and honeydew producing homoptera. Annu Rev Entomol 8:307–344. doi: 10.1146/annurev.en.08.010163.001515 CrossRefGoogle Scholar
  66. Wetterer JK, Miller SE, Wheeler DE, Olson CA, Polhemus DA, Pitts M, Ashton W, Himler AG, Yospin MM, Helms KR, Harken EL, Gallaher CE, Dunning CE, Nelson M, Litsinger J, Southern A, Burgess TL (1999) Ecological dominance by Paratrechina longicornis (Hymenoptera: Formicidae), an invasive tramp ant, in Biosphere 2. Fla Entomol 82:381–388. doi: 10.2307/3496865 CrossRefGoogle Scholar
  67. Wool D, Hendrix DL, Shukry O (2006) Seasonal variation in honeydew sugar content of galling aphids (Aphidoidea: Pemphigidae: Fordinae) feeding on Pistacia: host ecology and aphid physiology. Basic Appl Ecol 7:141–151. doi: 10.1016/j.baae.2005.02.009 CrossRefGoogle Scholar
  68. Wright PJ, Bonser R, Chukwu UO (2000) The size–distance relationship in the wood ant Formica rufa. Ecol Entomol 25:226–233. doi: 10.1046/j.1365-2311.2000.00253.x CrossRefGoogle Scholar
  69. Yao I, Akimoto S (2001) Ant attendance changes the sugar composition of the honeydew of the drepanosiphid aphid Tuberculatus quercicola. Oecologia 128:36–43. doi: 10.1007/s004420100633 CrossRefGoogle Scholar
  70. Yao I, Shibao H, Akimoto S (2000) Costs and benefits of ant attendance to the drepanosiphid aphid Tuberculatus quercicola. Oikos 89:3–10. doi: 10.1034/j.1600-0706.2000.890101.x CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Animal Biodiversity Research Group, Ecology Unit and CREAFAutonomous University of BarcelonaBellaterraSpain
  2. 2.Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos AiresBuenos AiresArgentina

Personalised recommendations