Biological Invasions

, Volume 15, Issue 9, pp 2115–2125 | Cite as

Saving a tropical ecosystem from a destructive ant-scale (Pheidole megacephala, Pulvinaria urbicola) mutualism with support from a diverse natural enemy assemblage

  • R. Gaigher
  • M. J. Samways
  • S. Van Noort
Original Paper


Ants can disrupt the natural biological control of serious hemipteran pests by interfering with natural enemies, resulting in a change in ecosystem functioning. We focus here on interference by a highly invasive ant Pheidole megacephala on the regulation of a tree destroying hemipteran scale insect Pulvinaria urbicola on Cousine Island in the Seychelles archipelago, a tropical island ecosystem. We show how a diverse natural enemy assemblage contributes substantially to the collapse of the ant-scale mutualism following managed ant suppression. Natural enemy abundance and species richness increased significantly after ant suppression, with varying responses among the different functional guilds. Primary parasitoids coexisted with tending ants before ant suppression, but could not regulate the enormously high scale densities alone. After ant suppression, a significant increase in predators caused a collapse of the scale population. Guilds external to the mutualism were also affected, with primary parasitoids of various non-hemipteran taxa also increasing, which contributed significantly to the recovery of the community to its pre-invasion composition. Our results highlight the far-reaching and pervasive effects of the hemipteran-tending invasive ant within the natural enemy assemblage. In turn, we also illustrate the potential to restore the tropical ecosystem by encouraging an array of natural enemies through precision management of the ant.


Parasitoids Predators Invasive species Island restoration Pheidole megacephala Pulvinaria urbicola 



This work was funded by DST-NRF Centre of Excellence for Invasion Biology (CIB) and the Working for Water Programme through their collaborative research project on “Integrated Management of Invasive Alien Species”. Arthropod identifications were provided by G. Prinsloo, J. Gerlach and A. Dippenaar-Schoeman. D.G. Nel assisted with statistical analyses. Two anonymous referees provided constructive comments on the manuscript.


  1. Bartlett BR (1961) The influence of ants upon parasites, predators, and scale insects. Ann Entomol Soc Am 54:543–551Google Scholar
  2. Barzman MS, Daane KM (2001) Host-handling behaviours in parasitoids of the black scale: a case for ant-mediated evolution. J Anim Ecol 70:237–247. doi: 10.1111/j.1365-2656.2001.00483.x CrossRefGoogle Scholar
  3. Cardinale BJ, Harvey CT, Gross K, Ives AR (2003) Biodiversity and biocontrol: emergent impacts of a multi-enemy assemblage on pest suppression and crop yield in an agroecosystem. Ecol Lett 6:857–865. doi: 10.1046/j.1461-0248.2003.00508.x CrossRefGoogle Scholar
  4. Chalcraft DR, Resetarits WJ (2003) Predator identity and ecological impacts: functional redundancy or functional diversity? Ecology 84:2407–2418CrossRefGoogle Scholar
  5. Clarke KR, Gorley RN (2001) PRIMER v5: User manual/tutorial. PRIMER-E, PlymouthGoogle Scholar
  6. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation. PRIMER-E, PlymouthGoogle Scholar
  7. Colfer RG, Rosenheim JA (2001) Predation on immature parasitoids and its impact on aphid suppression. Oecologia 126:292–304. doi: 10.1007/s004420000510 CrossRefGoogle Scholar
  8. Costamagna AC, Landis DA, Brewer MJ (2008) The role of natural enemy guilds in Aphis glycines suppression. Biol Control 45:368–379CrossRefGoogle Scholar
  9. Daane KM, Sime KR, Fallon J, Cooper ML (2007) Impacts of Argentine ants on mealybugs and their natural enemies in California’s coastal vineyards. Ecol Entomol 32:583–596. doi: 10.1111/j.1365-2311.2007.00910.x CrossRefGoogle Scholar
  10. Delabie JHC (2001) Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an Overview. Neotrop Entomol 30:501–516CrossRefGoogle Scholar
  11. Del-Claro K, Oliveira PS (2000) Conditional outcomes in a neotropical treehopper-ant association: temporal and species-specific variation in ant protection and homopteran fecundity. Oecologia 124:156–165. doi: 10.1007/s004420050002 CrossRefGoogle Scholar
  12. Denoth M, Frid L, Myers JH (2002) Multiple agents in biological control: improving the odds? Biol Control 24:20–30. doi: 10.1016/S1049-9644(02)00002-6 CrossRefGoogle Scholar
  13. Eubanks MD, Blackwell SA, Parrish CJ, Delamar ZD, Hull-Sanders H (2002) Intraguild predation of beneficial arthropods by red imported fire ants in cotton. Environ Entomol 31:1168–1174. doi: 10.1603/0046-225X-31.6.1168 CrossRefGoogle Scholar
  14. Gaigher R, Samways MJ (2013) Strategic management of an invasive ant-scale mutualism enables recovery of a threatened tropical tree species. Biotropica 45:128–134. doi: 10.1111/j.1744-7429.2012.00898.x CrossRefGoogle Scholar
  15. Gaigher R, Samways MJ, Henwood J, Jolliffe K (2011) Impact of a mutualism between an invasive ant and honeydew-producing insects on a functionally important tree on a tropical island. Biol Invasions 13:1717–1721. doi: 10.1007/s10530-010-9934-1 CrossRefGoogle Scholar
  16. Gaigher R, Samways MJ, Jolliffe KG, Jolliffe S (2012) Precision control of an invasive ant on an ecologically sensitive tropical island: a principle with wide applicability. Ecol Appl 22:1405–1412. doi: 10.1890/11-2002.1 PubMedGoogle Scholar
  17. Grover CD, Dayton KC, Menke SB, Holway DA (2008) Effects of aphids on foliar foraging by Argentine ants and the resulting effects on other arthropods. Ecol Entomol 33:101–106. doi: 10.1111/j.1365-2311.2007.00942.x Google Scholar
  18. Haines IH, Haines JB (1978) Pest status of the crazy ant, Anoplolepis longipes (Jerdon)(Hymenoptera:Formicidae), in the Seychelles. B Entomol Res 68:627–638CrossRefGoogle Scholar
  19. Handler AT, Gruner DS, Haines WP, Lange MW, Kaneshiro KY (2007) Arthropod surveys on Palmyra Atoll, Line Islands, and insights into the decline of the native tree Pisonia grandis (Nyctaginaceae). Pac Sci 61:485–502. doi: 10.2984/1534-6188 CrossRefGoogle Scholar
  20. Hill MG, Newbery DM (1982) An analysis of the origins and affinities of the coccid fauna (Coccoidea; Homoptera) of Western Indian Ocean islands, with special reference to Aldabra Atoll. J Biogeogr 9:223–229CrossRefGoogle Scholar
  21. 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 12:1969–1984. doi: 10.1023/A:1024151630204 CrossRefGoogle Scholar
  22. Hoffmann BD (2010) Ecological restoration following the local eradication of an invasive ant in northern Australia. Biol Invasions 12:959–969CrossRefGoogle Scholar
  23. Hulbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211CrossRefGoogle Scholar
  24. Jalali SK, Singh SP (1989) Biotic potential of three coccinellid predators on various diaspine hosts. J Biol Control 3:20–23Google Scholar
  25. 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
  26. Kaneko S (2002) Aphid-attending ants increase the number of emerging adults of the aphid’s primary parasitoid and hyperparasitoids by repelling intraguild predators. Entomol Sci 5:131–146Google Scholar
  27. Kaneko S (2003) Different impacts of two species of aphid-attending ants with different aggressiveness on the number of emerging adults of the aphid’s primary parasitoid and hyperparasitoids. Ecol Res 18:199–212. doi: 10.1046/j.1440-1703.2003.00547.x CrossRefGoogle Scholar
  28. Kaneko S (2007) Predator and parasitoid attacking ant-attended aphids: effects of predator presence and attending ant species on emerging parasitoid numbers. Ecol Res 22:451–458. doi: 10.1007/s11284-006-0025-9 CrossRefGoogle Scholar
  29. Kaplan I, Eubanks MD (2002) Disruption of cotton aphid (Homoptera: Aphididae)—natural enemy dynamics by red imported fire ants (Hymenoptera: Formicidae). Environ Entomol 31:1175–1183. doi: 10.1603/0046-225X-31.6.1175 CrossRefGoogle Scholar
  30. Kaplan I, Eubanks MD (2005) Aphids alter the community-wide impact of fire ants. Ecology 86:1640–1649. doi: 10.1890/04-0016 CrossRefGoogle Scholar
  31. Kaur H, Vink JS (2012) Feeding potential of Cryptolaemus montrouzieri against the mealybug Phenacoccus solenopsis. Phytoparasitica 40:2131–2136CrossRefGoogle Scholar
  32. Krushelnycky PD, Gillespie RG (2008) Compositional and functional stability of arthropod communities in the face of ant invasions. Ecol Appl 18:1547–1562PubMedCrossRefGoogle Scholar
  33. Letourneau DK, Andow DA (1999) Natural enemy food webs. Ecol Appl 9:363–364CrossRefGoogle Scholar
  34. Liang K, Zeger SL (1986) Longitudinal data analysis using generalized linear models. Biometrika 73:13–22CrossRefGoogle Scholar
  35. Liere H, Perfecto Y (2008) Cheating on a mutualism: indirect benefits of ant attendance to a coccidophagous coccinellid. Environ Entomol 37:143–149. doi: 10.1603/0046-225X PubMedCrossRefGoogle Scholar
  36. Majerus MEN, Sloggett JJ, Godeau JF, Hemptinne JL (2006) Interactions between ants and aphidophagous and coccidophagous ladybirds. Popul Ecol 49:15–27. doi: 10.1007/s10144-006-0021-5 CrossRefGoogle Scholar
  37. McCullagh P, Nelder JA (1989) Generalized linear models. Chapman and Hall, LondonGoogle Scholar
  38. Mgocheki N, Addison P (2009) Interference of ants (Hymenoptera: Formicidae) with biological control of the vine mealybug Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae). Biol Control 49:180–185. doi: 10.1016/j.biocontrol.2009.02.001 CrossRefGoogle Scholar
  39. Myers JH, Higgins C, Kovacs E (1989) How many insect species are necessary for the biological control of insects? Environ Entomol 18:541–547Google Scholar
  40. Noyes JS (2012) Universal Chalcidoidea Database. World Wide Web electronic publication. Accessed August 2012
  41. O’Neill P, Olds J, Elder R (1997) Report on investigations of Pulvinaria urbicola infestations of Pisonia grandis forests, and masked and brown booby populations in the Coral Sea, 25 Nov–18 Dec 1997. Environment Australia ReportGoogle Scholar
  42. Queiroz JM, Oliveira PS (2001) Tending ants protect honeydew-producing whiteflies (Homoptera: Aleyrodidae). Environ Entomol 30:295–297CrossRefGoogle Scholar
  43. 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
  44. Samways MJ (1984) Biology and economic value of the scale predator Chilocorus nigritus (F.) (Coccinellidae). Biocontrol News Inf 5:91–105Google Scholar
  45. Samways MJ (1988) A pictorial model of the impact of natural enemies on the population growth rate of the scale insect Aonidiella aurantii. S Afr J Sci 84:270–272Google Scholar
  46. Samways MJ, Wilson SJ (1988) Aspects of the feeding behaviour of Chilocorus nigritus (F.) (Col., Coccinellidae) relative to its effectiveness as a biocontrol agent. J Appl Entomol 106:177–182. doi: 10.1111/j.1439-0418.1988.tb00580.x CrossRefGoogle Scholar
  47. Scholtz CH, Holm E (2008) Insects of Southern Africa. Protea Book House, PretoriaGoogle Scholar
  48. Smith D, Papacek D (2002) Report On Visit to the Coringa—Herald Nature Reserve and SE Magdelaine Cay, 15–22 March, 2002 with regard to the releasing of parasitoids and ladybird predators of the pest scale Pulvinaria urbicola on Pisonia grandis and the assessment of biocontrol options for hawkmoths. Environment Australia ReportGoogle Scholar
  49. Smith D, Papacek D, Hallam M, Smith J (2004) Biological control of Pulvinaria urbicola (Cockerell) (Homoptera:Coccidae) in a Pisonia grandis forest on North East Herald Cay in the Coral Sea. Gen Appl Entomol 33:61–68Google Scholar
  50. Snyder WE, Ives AR (2003) Interactions between specialist and generalist natural enemies: parasitoids, predators and pea aphid biocontrol. Ecology 84:94–107. doi: 10.1890/0012-9658 Google Scholar
  51. SPSS Inc (2010) SPSS for Windows, Release 19.0.0. SPSS Inc, Chicago, USAGoogle Scholar
  52. Stokes ME, Davis CS, Koch GG (2000) Categorical data analysis using the SAS system, 3rd edn. SAS Institute Inc, CaryGoogle Scholar
  53. Straub CS, Snyder WE (2006) Species identity dominates the relationship between predator biodiversity and herbivore suppression. Ecology 87:277–282. doi: 10.1111/j.1461-0248.2006.00922.x PubMedCrossRefGoogle Scholar
  54. Styrsky JD, Eubanks MD (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proc R Soc B 274:151–164. doi: 10.1098/rspb.2006.3701 PubMedCrossRefGoogle Scholar
  55. Suzuki N, Ide T (2008) The foraging behaviors of larvae of the ladybird beetle, Coccinella septempunctata L., (Coleoptera: Coccinellidae) towards ant-tended and non-ant-tended aphids. Ecol Res 23:371–378. doi: 10.1007/s11284-007-0391-y CrossRefGoogle Scholar
  56. Vanek SJ, Potter DA (2010) Ant-exclusion to promote biological control of soft scales (Hemiptera: Coccidae) on woody landscape plants. Environ Entomol 39:1829–1837. doi: 10.1603/EN10093 PubMedCrossRefGoogle Scholar
  57. Völkl W (1992) Aphids or their parasitoids: who actually benefits from ant-attendance? J Anim Ecol 61:273–281CrossRefGoogle Scholar
  58. Völkl W, Mackauer M (1993) Interactions of ants attending Aphis fabae spp. cirsiiacanthoidis on thistles and foraging parasitoid wasps. J Insect Behav 6:301–312. doi: 10.1007/BF01048111 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of Conservation Ecology and Entomology, and DST/NRF Centre of Excellence for Invasion BiologyStellenbosch UniversityMatielandSouth Africa
  2. 2.Natural History DepartmentIziko South African MuseumCape TownSouth Africa

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