Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids?

BioControl

Volumn 56, Issue 4, 2011, Pages 451-468

  Roy, H E ^a   Handley, L J Lawson ^b   Schonrogge K ^a   Poland, R L ^c   Purse, B V ^a  

^a CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^b UNIVERSITY OF HULL   (United Kingdom)

^c Clifton College   (United Kingdom)

Author keywords

Arthropod predators; Modelling; Molecular; Natural enemy release hypothesis; Parasitoids

Indexed keywords

ABUNDANCE; BIOLOGICAL INVASION; INTRODUCED SPECIES; INVERTEBRATE; NATURAL ENEMY; POPULATION DISTRIBUTION; POPULATION GROWTH; VULNERABILITY;

ARTHROPODA; INVERTEBRATA;

EID: 80052204912     PISSN: 13866141     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10526-011-9349-7     Document Type: Review

References (110)

1. Aebi A, Schönrogge K, Melika G, Alma A, Bosio G, Quacchia A, Picciau L, Abe Y, Moriya S, Yara K, Seljak G, Stone GN (2006) Parasitoid recruitment to the globally invasive chestnut gall wasp Dryocosmus kuriphilus. In: Ozaki K, Yukawa J, Ohgushi T, Price PW (eds) Ecology and evolution of galling arthropods and their associates. Springer, Tokyo.
2. Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294: 321-326.
3. Agrawal AA, Kotanen PM (2003) Herbivores and the success of exotic plants: a phylogenetically controlled experiment. Ecol Lett 6: 712-715.
4. Aliabadi BK, Juliano SA (2002) Escape from gregarine parasites affects the competitive impact of an invasive mosquito. Biol Invasions 4: 283-297.
5. Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17: 24-30.
6. Arnaud PH (1978) A host-parasite catalog of North American Tachinidae (Diptera). US Dep Agric Misc Publ 1319.
7. Askew RR, Shaw MR (1986) Parasitoid communities: their size, structure, and development. In: Waage J, Greathead D (eds) Insect parasitoid. Academic Press, London, UK.
8. Baalen MV, Křivan V, Rijn PV, Sabelis MW (2001) Alternative food, switching predators, and the persistence of predator-prey systems. Am Nat 157: 512-524.
9. Bailey R, Schönrogge K, Cook JM, Melika G, Csóka G, Thuróczy C, Stone GN (2009) Host niches and defensive extended phenotypes structure parasitoid wasp communities. PLoS Biol 7: e1000179.
10. Barney J (2006) North American history of two invasive plant species: phytogeographic distribution, dispersal vectors, and multiple introductions. Biol Invasions 8: 703-717.
11. Barney JN, Whitlow TH (2008) A unifying framework for biological invasions: the state factor model. Biol Invasions 10: 259-272.
12. Berkvens NJ, Moens J, Berkvens D, Samih MA, Tirry L, De Clercq P (2010) Dinocampus coccinellae as a parasitoid of the invasive ladybird Harmonia axyridis in Europe. Biol Control 53: 92-99.
13. Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83: 887-889.
14. Blumenthal D, Mitchell CE, Pysěk P, Jarošík V (2009) Synergy between pathogen release and resource availability in plant invasion. Proc Natl Acad Sci 106: 7899-7904.
15. Brooks DR, McLennan DA (2002) The nature of diversity: an evolutionary voyage of discovery. University of Chicago Press, Chicago.
16. Carroll SP (2007) Natives adapting to invasive species: ecology, genes and the sustainability of conservation. Ecol Res 22: 892-901.
17. Claridge MF (1962) Andricus quercuscalicis (Burgsdorf) in Britain (Hym., Cynipidae). Entomologist 95: 60-61.
18. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac Hj (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7: 721-733.
19. Collins M, Crawley MJ, McGavin GC (1983) Survivorship of the sexual and agamic generations of Andricus quercuscalicis on Quercus cerris and Q. robur. Ecol Entomol 8: 133-138.
20. Cornell HV, Hawkins BA (1993) Accumulation of native parasitoid species on introduced herbivores: a comparison of "host as natives" and "host as invaders". Am Nat 141: 847-865.
21. Cottrell TE, Shapiro-Ilan DI (2003) Susceptibility of a native and an exotic lady beetle (Coleoptera: Coccinellidae) to Beauveria bassiana. J Invertebr Pathol 84: 137-144.
22. Cox GW (2004) Alien species and evolution: the evolutionary ecology of exotic plants, animals, microbes, and interacting native species. Island Press, Washington.
23. Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, Quan PL, Briese T, Hornig M, Geiser DM, Martinson V, van Engelsdorp D, Kalkstein AL, Drysdale A, Hui J, Zhai J, Cui L, Hutchison SK, Simons JF, Egholm M, Pettis JS, Lipkin WI (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318: 283-287.
24. Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88: 528-534.
25. De Moraes CM, Mescher MC (2005) Intrinsic competition between larval parasitoids with different degrees of host specificity. Ecol Entomol 30: 564-570.
26. Debach P, Rosen D (1991) Biological control by natural enemies, 2nd edn. University Press, Cambridge.
27. Drake JM (2003) The paradox of the parasites: implications for biological invasion. Proc R Soc Lond B (Suppl) Biol Lett 270: S133-S135.
28. Ehrlich PR, Birch L (1967) The "balance of nature" and "population control". Am Nat 101: 97-107.
29. Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London, UK.
30. Gamboa GJ, Noble MA, Thom MC, Togal JL, Srinivasan R, Murphy BD (2004) The comparative biology of two sympatric paper wasps in Michigan, the native Polistes fuscatus and the invasive Polistes dominulus (Hymenoptera, Vespidae). Insectes Sociaux 51: 153-157.
31. Georgiev BB, Sánchez MI, Vasileva GP, Nikolov PN, Green AJ (2007) Cestode parasitism in invasive and native brine shrimps (Artemia spp.) as a possible factor promoting the rapid invasion of A. franciscana in the Mediterranean region. Parasitol Res 101: 1647-1655.
32. Gibbs M, Schönrogge K, Alma A, Melika G, Quacchia A, Stone G, Aebi A (2011) Torymus sinensis: a viable management option for the biological control of Dryocosmus kuriphilus in Europe? BioControl. doi: 10. 1007/s10526-011-9364-8.
33. Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Princeton.
34. González AL, Kominoski JS, Danger M, Ishida S, Iwai N, Rubach A (2010) Can ecological stoichiometry help explain patterns of biological invasions? Oikos 119: 779-790.
35. Grill CP, Juliano SA (1996) Predicting species interactions based on behaviour: predation and competition in container-dwelling mosquitoes. J Anim Ecol 65: 63-76.
36. Griswold MW, Lounibos LP (2005) Does differential predation permit invasive and native mosquito larvae to coexist in Florida? Ecol Entomol 30: 122-127.
37. Gross J, Eben A, Müller I, Wensing A (2010) A well protected intruder: the effective antimicrobial defense of the invasive ladybird Harmonia axyridis. J Chem Ecol 36: 1180-1188.
38. Hails RS, Crawley MJ (1992) Spatial density dependence in populations of a Cynipid gall-former Andricus quercuscalicis. J Anim Ecol 61: 567-583.
39. Hails RS, Askew RR, Notton DG (1990) The parasitoids and inquilines of the agamic generation of Andricus quercuscalicis (Hym.; Cynipidae) in Britain. Entomologist 109: 165-172.
40. Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94: 421-425.
41. Hassell MP (1985) Insect natural enemies as regulating factors. J Anim Ecol 54: 323-334.
42. Hassell MP, May RM (1986) Generalist and specialist natural enemies in insect predator-prey interactions. J Anim Ecol 55: 923-940.
43. Hatcher MJ, Dick JTA, Dunn AM (2006) How parasites affect interactions between competitors and predators. Ecol Lett 9: 1253-1271.
44. Hawkins BA (1992) Parasitoid-host food webs and donor control. Oikos 65: 159-162.
45. Hobbs RJ, Huenneke LF (1992) Disturbance, diversity, and invasion: implications for conservation. Conserv Biol 6: 324-337.
46. Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73: 723-732.
47. Jeffries MJ, Lawton JH (1984) Enemy free space and the structure of ecological communities. Biol J Linn Soc 23: 269-286.
48. Joshi J, Vrieling K (2005) The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol Lett 8: 704-714.
49. Juliano SA, Lounibos LP, Nishimura N, Greene K (2010) Your worst enemy could be your best friend: predator contributions to invasion resistance and persistence of natives. Oecologia 162: 709-718.
50. Keane R, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17: 164-170.
51. Kesavaraju B, Juliano SA (2004) Differential behavioral responses to water-borne cues to predation in two container-dwelling mosquitoes. Ann Entomol Soc Am 97: 194-201.
52. Koyama S, Majerus MEN (2008) Interactions between the parasitoid wasp Dinocampus coccinellae and two species of coccinellid from Japan and Britain. BioControl 53: 253-264.
53. Krebs JR, McCleery RH (1984) Optimization in behavioural ecology. In: Krebs JR, Davies NB (eds) Behavioural ecology, an evolutionary approach. Blackwell Scientific, Oxford, UK.
54. Lawson Handley JL, Estoup A, Thomas CE, Lombaert E, Facon B, Aebi A, Evans DM, Roy HE (2011) Ecological genetics of invasive alien species. BioControl. doi: 10. 1007/s10526-011-9386-2.
55. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442: 806-809.
56. Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8: 1535-1545.
57. Lively CM (2006) The ecology of virulence. Ecol Lett 9: 1089-1095.
58. MacNeil C, Dick JTA, Hatcher MJ, Terry RS, Smith JE, Dunn A (2003a) Parasite-mediated predation between native and invasive amphipods. Proc R Soc Lond B 270: 1309-1314.
59. MacNeil C, Fielding NJ, Hulme KD, Dick JTA, Elwood RW, Hatcher MJ, Dunn AM (2003b) Parasite altered micro-distribution of Gammarus pulex (Crustacea: Amphipoda). Int J Parasitol 33: 57-64.
60. Mills NJ (2005) Selecting effective parasitoids for biological control introductions: codling moth as a case study. Biol Control 34: 274-282.
61. Müller-Schärer H, Schaffner U, Steinger T (2004) Evolution in invasive plants and implications for biological control. Trends Ecol Evol 19: 417-422.
62. Murdoch WW (1966) Community structure, population control and competition-a critique. Am Nat 100: 219-226.
63. Murdoch WW, Chesson J, Chesson PL (1985) Biological control in theory and practice. Am Nat 125: 344-366.
64. Nicholls JA, Preuss S, Hayward A, Melika G, Csoka G, Nieves-Aldrey J-L, Askew RR, Tavakoli M, Schönrogge K, Stone GN (2010a) Concordant phylogeography and cryptic speciation in two Western Palaearctic oak gall parasitoid species complexes. Mol Ecol 19: 592-609.
65. Nicholls JA, Fuentes-Utrilla P, Hayward A, Melika G, Csóka G, Nieves-Aldrey J-L, Pujade-Villar J, Tavakoli M, Schönrogge K, Stone GN (2010b) Community impacts of anthropogenic disturbance: natural enemies exploit multiple routes in pursuit of invading herbivore hosts. BMC Evol Biol 10: 322.
66. Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20: 297-330.
67. Reichert SE, Lockley T (1984) Spiders as biological control agents. Annu Rev Entomol 29: 299-320.
68. Reynolds JD (1988) Crayfish extinctions and crayfish plague in central Ireland. Biol Conserv 45: 279-285.
69. Rizzo DM, Garbelotto M (2003) Sudden oak death: endangering California and Oregon forest ecosystems. Front Ecol Environ 1: 197-204.
70. Rosenheim JA, Limburg DD, Colfer RG (1999) Impact of generalist predators on a biological control agent, Chrysoperla carnea: direct observations. Ecol Appl 9: 409-417.
71. Roy HE, Pell JK (2000) Interactions between entomopathogenic fungi and other natural enemies: implications for biological control. Biocontrol Sci Tech 10: 737-752.
72. Roy HE, Brown PMJ, Rothery P, Ware RL, Majerus MEN (2008) Interactions between the fungal pathogen Beauveria bassiana and three species of ladybird: Harmonia axyridis, Coccinella septempunctata and Adalia bipunctata. BioControl 53: 265-276.
73. Sato H (1990) Comparison of community composition of parasitoids that attack leaf-mining moths (Lepidoptera: Gracillariidae). Environ Entomol 24: 879-888.
74. Sax DF, Stachowicz JJ, Brown JH, Bruno JF, Dawson MN, Gaines SD, Grosberg RK, Hastings A, Holt RD, Mayfield MM, O'Connor MI, Rice WR (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22: 465-471.
75. Schönrogge K, Crawley MJ (2000) Quantitative webs as a means of assessing the impact of alien insects. J Anim Ecol 69: 841-868.
76. Schönrogge K, Stone GN, Crawley MJ (1996) Abundance patterns and species richness of the parasitoids and inquilines of the alien gall-former Andricus quercuscalicis (Hymenoptera: Cynipidae). Oikos 77: 507-518.
77. Schönrogge K, Walker P, Crawley MJ (1998) Invaders on the move: parasitism in the sexual galls of four alien gall wasps in Britain (Hymenoptera: Cynipidae). Proc R Soc B 265: 1643-1650.
78. Schönrogge K, Walker P, Crawley MJ (2000) Parasitoid and inquiline attack in the galls of four alien, cynipid gall wasps: host switches and the effect on parasitoid sex ratios. Ecol Entomol 25: 208-219.
79. Schönrogge K, Napper EKV, Birkett MA, Woodcock C, Pickett JA, Thomas JA (2008) Host recognition by the specialist hoverfly Microdon mutabilis, a social parasite of the ant Formica lemani. J Chem Ecol 34: 168-178.
80. Schutzenhofer MR, Knight TM (2007) Population-level effects of augmented herbivory on Lespedeza cuneata: implications for biological control. Ecol Appl 17: 965-971.
81. Schutzenhofer MR, Valone TJ, Knight TM (2009) Herbivory and population dynamics of invasive and native Lespedeza. Oecologia 161: 57-66.
82. Shapiro-Ilan DI, Cottrell TE (2005) Susceptibility of ladybeetles (Coleoptera: Coccinellidae) to entomopathogenic nematodes. J Invertebr Pathol 89: 150-156.
83. Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17: 170-176.
84. Sheehan W, Hawkins BA (1991) Attack strategy as an indicator of host range in metopiine and pimpline Ichneumonidae (Hymenoptera). Ecol Entomol 16: 129-131.
85. Shinen JS, Morgan SG, Chan AL (2009) Invasion resistance on rocky shores: direct and indirect effects of three native predators on an exotic and a native prey species. Mar Ecol Prog Ser 378: 47-54.
86. Slothouber Galbreath JGM, Smith JE, Becnel JJ, Butlin RK, Dunn AM (2010) Reduction in post-invasion genetic diversity in Crangonyx pseudogracilis (Amphipoda: Crustacea): a genetic bottleneck or the work of hitchhiking vertically transmitted microparasites? Biol Invasions 12: 191-209.
87. Snyder WE, Ives AR (2001) Generalist predators disrupt biological control by a specialist parasitoid. Ecology 82: 705-716.
88. Snyder WE, Ives AR (2003) Interactions between specialist and generalist natural enemies: parasitoids, predators and pea aphid biocontrol. Ecology 84: 91-107.
89. Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored "rare biosphere". Proc Natl Acad Sci USA 103: 12115-122120.
90. Stastny M, Schaffner U, Elle E (2005) Do vigour of introduced populations and escape from specialist herbivores contribute to invasiveness? J Ecol 93: 27-37.
91. Steenberg T, Harding S (2009) Entomopathogenic fungi recorded from the harlequin ladybird, Harmonia axyridis. J Invertebr Pathol 102: 88-89.
92. Strauss SY, Lau JA, Carroll SP (2006) Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett 9: 357-374.
93. Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47: 561-594.
94. Tompkins DM, White AR, Boots M (2003) Ecological replacement of native red squirrels by invasive greys driven by disease. Ecol Lett 6: 189-196.
95. Torchin ME, Mitchell CE (2003) Parasites, pathogens, and invasions by plants and animals. Front Ecol Environ 2: 183-190.
96. Torchin ME, Mitchell CE (2004) Parasites, pathogens, and invasions by plants and animals. Front Ecol Environ 2: 183-190.
97. Torchin ME, Lafferty KD, Kuris AM (2001) Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biol Invasions 3: 333-345.
98. Torchin ME, Lafferty KD, Kuris AM (2002) Parasites and marine invasions. Parasitology 124: S137-S151.
99. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421: 628-630.
100. van der Meijden E (1996) Plant defence, an evolutionary dilemma: contrasting effects of (specialist and generalist) herbivores and natural enemies. Entomol Exper Appl 80: 307-310.
101. Vermeij GJ (1982) Phenotypic evolution in a poorly dispersing snail after arrival of a predator. Nature 299: 349-350.
102. Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37: 141-172.
103. Walker P (2001) The developing community on the introduced oak Quercus cerris: a catkin gall-forming wasp Andricus grossulariae New to Britain. Entomol Mon Mag 137: 145-147.
104. Wanger TC, Wielgoss AC, Motzke I, Clough Y, Brook BW, Sodhi NS, Tscharntke T (2010) Endemic predators, invasive prey and native diversity. Proc R Soc B 278: 690-694.
105. Ware RL, Majerus MEN (2008) Intraguild predation of immature stages of British and Japanese coccinellids by the invasive ladybird Harmonia axyridis. BioControl 53: 169-188.
106. Wattier RA, Haine ER, Beguet J, Martin G, Bollache L, Muskó IB, Platvoet D, Rigaud T (2007) No genetic bottleneck or associated microparasite loss in invasive populations of a freshwater amphipod. Oikos 116: 1941-1953.
107. Wells PM, Baverstock J, Majerus MEN, Jiggins FM, Roy HE, Pell JK (2011) The effect of the coccinellid Harmonia axyridis on transmission and dispersal of the fungal pathogen Pandora neoaphidis. Eur J Entomol 108: 87-90.
108. Wolfe LM (2002) Why alien invaders succeed: support for the escape-from-enemy hypothesis. Am Nat 160: 705-711.
109. Yang C-C, Yu Y-C, Valles SM, Oi DH, Chen Y-C, Shoemaker DW, Wu W-J, Shih C-J (2010) Loss of microbial (pathogen) infections associated with recent invasions of the red imported fire ant Solenopsis invicta. Biol Invasions 3: 333-345.
110. Zuharah WF, Lester PJ (2010) Can adults of the New Zealand mosquito Culex pervigilans (Bergorth) detect the presence of a key predator in larval habitats? J Vector Ecolgy 35: 100-105.