, Volume 162, Issue 3, pp 709–718 | Cite as

Your worst enemy could be your best friend: predator contributions to invasion resistance and persistence of natives

  • Steven A. Juliano
  • L. Philip Lounibos
  • Naoya Nishimura
  • Krystle Greene
Community ecology - Original Paper


Native predators are postulated to have an important role in biotic resistance of communities to invasion and community resilience. Effects of predators can be complex, and mechanisms by which predators affect invasion success and impact are understood for only a few well-studied communities. We tested experimentally whether a native predator limits an invasive species’ success and impact on a native competitor for a community of aquatic insect larvae in water-filled containers. The native mosquito Aedes triseriatus alone had no significant effect on abundance of the invasive mosquito Aedes albopictus. The native predatory midge Corethrella appendiculata, at low or high density, significantly reduced A. albopictus abundance. This effect was not caused by trait-mediated oviposition avoidance of containers with predators, but instead was a density-mediated effect caused by predator-induced mortality. The presence of this predator significantly reduced survivorship of the native species, but high predator density also significantly increased development rate of the native species when the invader was present, consistent with predator-mediated release from interspecific competition with the invader. Thus, a native predator can indirectly benefit its native prey when a superior competitor invades. This shows the importance of native predators as a component of biodiversity for both biotic resistance to invasion and resilience of a community perturbed by successful invasion.


Density-mediated effects Invasive species Keystone predator Mosquitoes Trait-mediated behavioral effects 



We thank R. Escher for his extensive efforts rearing A. triseriatus and C. appendiculata, and for other assistance in the laboratory, M. Reiskind, B. Kesavaraju, K. Smith, and J. Chase for informative discussion, and two anonymous referees for helpful comments. This research was supported by a grant from the National Institute of Allergy and Infectious Disease (R01-AI44793). Experiments comply with the current laws of the US.


  1. Aliabadi BK, Juliano SA (2002) Escape from gregarine parasites affects the competitive impact of an invasive mosquito. Biol Invasions 4:283–297CrossRefPubMedGoogle Scholar
  2. Alto BW, Kesavaraju B, Juliano SA, Lounibos LP (2009) Stage-dependent predation on competitors: consequences for the outcome of a mosquito invasion. J Anim Ecol 78:928–936CrossRefPubMedGoogle Scholar
  3. Armistead JS, Arias JR, Lounibos LP (2008) Interspecific larval competition between Aedes albopictus and Aedes japonicus (Diptera: Culicidae) in northern Virginia. J Med Entomol 45:629–637CrossRefPubMedGoogle Scholar
  4. Baltz DM, Moyle PB (1993) Invasion resistance to introduced species by a native assemblage of California stream fishes. Ecol Appl 3:246–255CrossRefGoogle Scholar
  5. Bevins SN (2007) Timing of resource input and larval competition between invasive and native container-inhabiting mosquitoes (Diptera: Culicidae). J Vector Ecol 32:252–262CrossRefPubMedGoogle Scholar
  6. Blaustein L, Blaustein J, Chase J (2005) Chemical detection of the predator Notonecta irrorata by ovipositing Culex mosquitoes. J Vector Ecol 30:299–301PubMedGoogle Scholar
  7. Borkent A (2008) The frog-biting midges of the world (Corethrellidae: Diptera). Zootaxa 1804:1–456Google Scholar
  8. Bradshaw WE, Holzapfel CM (1988) Drought and the organization of tree-hole mosquito communities. Oecologia 74:507–514CrossRefGoogle Scholar
  9. Braks MAH, Honório NA, Lourenço-de-Oliveira R, Juliano SA, Lounibos LP (2003) Convergent habitat segregation of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in southeastern Brazil and Florida, USA. J Med Entomol 40:785–794CrossRefPubMedGoogle Scholar
  10. Braks MAH, Honório NA, Lounibos LP, Lourenço-de-Oliveira R, Juliano SA (2004) Interspecific competition between two invasive species of container mosquitoes, Aedes aegypti and Aedes albopictus (Diptera: Culicidae), in Brazil. Ann Entomol Soc Am 97:130–139CrossRefGoogle Scholar
  11. Byers JE (2002) Physical habitat attribute mediates biotic resistance to non-indigenous species invasion. Oecologia 130:146–156Google Scholar
  12. Chase JM, Abrams PA, Grover JP, Diehl S, Chesson P, Holt RD, Richards SA, Nisbet RM, Case TJ (2002) The interaction between predation and competition: a review and synthesis. Ecol Lett 5:302–315CrossRefGoogle Scholar
  13. Costanzo KS, Kesavaraju B, Juliano SA (2005) Condition-specific competition in container mosquitoes: the role of non-competing life-history stages. Ecology 86:3289–3295CrossRefPubMedGoogle Scholar
  14. Darwin C (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. Murray, LondonGoogle Scholar
  15. DeRivera CE, Ruiz GM, Hines AH, Jivoff P (2005) Biotic resistance to invasion: native predator limits abundance and distribution of an introduced crab. Ecology 86:3364–3376CrossRefGoogle Scholar
  16. Duncan RP, Williams PA (2002) Ecology: Darwin’s naturalization hypothesis challenged. Nature 417:608–6099CrossRefPubMedGoogle Scholar
  17. Elton C (1958) The ecology of invasions by animals and plants. Wiley, New YorkGoogle Scholar
  18. Fisher DO, Hoyle SD, Blomberg SP (2000) Population dynamics and survival of an endangered wallaby: a comparison of four methods. Ecol Appl 10:901–910CrossRefGoogle Scholar
  19. Griswold MW, Lounibos LP (2005a) Does differential predation permit invasive and native mosquito larvae to coexist in Florida? Ecol Entomol 30:122–127CrossRefGoogle Scholar
  20. Griswold MW, Lounibos LP (2005b) Competitive outcomes of aquatic container Diptera depend on predation and resource levels. Ann Entomol Soc Am 98:673–681CrossRefGoogle Scholar
  21. Hawley WA (1988) The biology of Aedes albopictus. J Am Mosq Control Assoc 4(Supplement):1–40Google Scholar
  22. Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Popul Biol 12:197–229CrossRefPubMedGoogle Scholar
  23. Juliano SA (1998) Species introduction and replacement among mosquitoes: interspecific resource competition or apparent competition? Ecology 79:255–268CrossRefGoogle Scholar
  24. Juliano SA (2009) Species interactions among larval mosquitoes: context dependence across habitat gradients. Annu Rev Entomol 54:37–56CrossRefPubMedGoogle Scholar
  25. Juliano SA, Lounibos LP (2005) Ecology of invasive mosquitoes: effects on resident species and on human health. Ecol Lett 8:558–574CrossRefPubMedGoogle Scholar
  26. Juliano SA, O’Meara GF, Morrill JR, Cutwa MM (2002) Desiccation and thermal tolerance of eggs and the coexistence of competing mosquitoes. Oecologia 130:458–469CrossRefGoogle Scholar
  27. Juliano SA, Lounibos LP, O’Meara GF (2004) A field test for competitive effects of Aedes albopictus on Aedes aegypti in South Florida: differences between sites of coexistence and exclusion? Oecologia 139:583–593CrossRefPubMedGoogle Scholar
  28. Kesavaraju B, Juliano SA (2004) Differential behavioral responses to water-borne cues to predation in two container-dwelling mosquitoes. Ann Entomol Soc Am 97:194–201CrossRefPubMedGoogle Scholar
  29. Kesavaraju B, Alto BW, Lounibos LP, Juliano SA (2007) Behavioural responses of larval container mosquitoes to a size-selective predator. Ecol Entomol 32:262–272CrossRefPubMedGoogle Scholar
  30. Kesavaraju B, Damal K, Juliano SA (2008) Do natural container habitats impede invader dominance? Predator-mediated coexistence of invasive and native container-dwelling mosquitoes. Oecologia 155:631–639CrossRefPubMedGoogle Scholar
  31. Kiflawi M, Blaustein L, Mangel M (2003) Predation-dependent oviposition habitat selection by the mosquito Culiseta longiareolata: a test of competing hypotheses. Ecol Lett 6:35–40CrossRefGoogle Scholar
  32. Leibold MA (1996) A graphical model of keystone predators in food webs: trophic regulation of abundance, incidence, and diversity patterns in communities. Am Nat 147:784–812CrossRefGoogle Scholar
  33. Livdahl TP, Willey MS (1991) Prospects for an invasion: competition between Aedes albopictus and native Aedes triseriatus. Science 253:189–191CrossRefPubMedGoogle Scholar
  34. Lodge DM (1993) Biological invasions: lessons for ecology. Trends Ecol Evol 8:133–136CrossRefGoogle Scholar
  35. Lounibos LP (1983) The mosquito community of treeholes in subtropical Florida. In: Frank JH, Lounibos LP (eds) Phytotelmata: terrestrial plants as hosts for aquatic insect communities. Plexus, Medford, pp 223–246Google Scholar
  36. Lounibos LP (1985) Interactions influencing production of treehole mosquitoes in South Florida. In: Lounibos LP, Rey JR, Frank JH (eds) Ecology of mosquitoes: proceedings of a workshop. Florida Medical Entomology Laboratory, Vero Beach, pp 65–77Google Scholar
  37. Lounibos LP (2002) Invasions by insect vectors of human diseases. Annu Rev Entomol 47:233–266CrossRefPubMedGoogle Scholar
  38. Lounibos LP, O’Meara GF, Escher RL, Nishimura N, Cutwa M, Nelson T, Campos R, Juliano SA (2001) Testing predictions of displacement of native Aedes by the invasive Asian tiger mosquito Aedes albopictus in Florida, USA. Biol Invasions 3:151–166CrossRefGoogle Scholar
  39. Morin PJ (1983) Predation, competition, and the composition of larval anuran guilds. Ecol Monogr 53:119–138CrossRefGoogle Scholar
  40. Noonberg EG, Byers JE (2005) More harm than good: when invader vulnerability to predators enhances impact on native species. Ecology 86:2555–2560CrossRefGoogle Scholar
  41. Novak MG, Higley LG, Christianssen CA, Rowley WA (1993) Evaluating larval competition between Aedes albopictus and A. triseriatus (Diptera, Culicidae) through replacement series experiments. Environ Entomol 22:311–318Google Scholar
  42. Nunez MA, Simberloff D, Relva MA (2008) Seed predation as a barrier to alien conifer invasions. Biol Invasions 10:1389–1398CrossRefGoogle Scholar
  43. O’Meara GF, Evans LF, Gettman AD, Cuda JP (1995) Spread of Aedes albopictus decline of Ae aegypti (Diptera: Culicidae) in Florida. J Med Entomol 32:554–562PubMedGoogle Scholar
  44. Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75CrossRefGoogle Scholar
  45. Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? Behavioral effects dominate predator–prey interactions. Ecology 86:501–509CrossRefGoogle Scholar
  46. Reusch TBH (1998) Native predators contribute to invasion resistance to the non-indigenous bivalve Musculista senhousia in southern California, USA. Mar Ecol Prog Ser 170:159–168CrossRefGoogle Scholar
  47. Robinson JV, Wellborn GA (1988) Ecological resistance to the invasion of a freshwater clam, Corbicula fluminea: fish predation effects. Oecologia 77:445–452CrossRefGoogle Scholar
  48. Roemer GW, Wayne RK (2003) Conservation in conflict: the tale of two endangered species. Conserv Biol 17:1251–1260CrossRefGoogle Scholar
  49. Salo P, Nordström M, Thomson RL, Korpimäki E (2008) Risk induced by a native top predator reduces alien mink movements. J Anim Ecol 77:1092–1098CrossRefPubMedGoogle Scholar
  50. SAS Institute (2003) SAS user’s guide: statistics, version 9 1. SAS Institute, CaryGoogle Scholar
  51. Scheiner SM (2001) MANOVA: multiple response variables and multispecies interaction. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments, 2nd edn. Oxford University Press, Oxford, pp 99–115Google Scholar
  52. Shea KP, Chesson P (2002) Community ecology as a framework for biological invasions. Trends Ecol Evol 5:302–315Google Scholar
  53. Smith KG (2006) Keystone predators eastern newts, Notophthalmus viridescens reduce the impacts of an aquatic invasive species. Oecologia 148:342–349CrossRefPubMedGoogle Scholar
  54. Teng H-J, Apperson CS (2000) Development and survival of immature Aedes albopictus and Aedes triseriatus Diptera: Culicidae in the laboratory: effects of density, food, and competition on response to temperatures. J Med Entomol 37:40–52CrossRefPubMedGoogle Scholar
  55. Wellborn GA (2002) Trade-off between competitive ability and antipredator adaptation in a freshwater amphipod species complex. Ecology 83:129–136CrossRefGoogle Scholar
  56. Werner EE, Anholt BR (1993) Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. Am Nat 142:242–272CrossRefPubMedGoogle Scholar
  57. Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100CrossRefGoogle Scholar
  58. Yee DA, Kaufman MG, Juliano SA (2007) The significance of ratios of detritus types and microorganism productivity to competitive interactions between aquatic insect detritivores. J Anim Ecol 76:1105–1115CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Steven A. Juliano
    • 1
  • L. Philip Lounibos
    • 2
  • Naoya Nishimura
    • 2
  • Krystle Greene
    • 2
  1. 1.Behavior, Ecology, Evolution, and Systematics Section, School of Biological SciencesIllinois State UniversityNormalUSA
  2. 2.Florida Medical Entomology LaboratoryUniversity of FloridaVero BeachUSA

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