A 'Goldilocks' hypothesis for dispersal of biological control agents

BioControl

Volumn 56, Issue 4, 2011, Pages 441-450

  Heimpel, George E ^a   Asplen, Mark K ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Allee effect; Aphis glycines; Binodoxys communis; Biological control; Dispersal; Goldilocks; Soybean aphid

Indexed keywords

ALLEE EFFECT; APHID; BIOCONTROL AGENT; DISPERSAL; MIGRATORY SPECIES; PARASITOID; PROBABILITY; SOYBEAN;

APHIDIDAE; APHIS GLYCINES; BINODOXYS; GLYCINE MAX;

EID: 80052193938     PISSN: 13866141     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10526-011-9381-7     Document Type: Review

References (100)

1. Andow DA, Prokrym DR (1991) Release density, efficiency and disappearance of Trichogramma nubilale for control of European corn borer. Entomophaga 36: 105-113.
2. Asplen MK, Wyckhuys KAG, Heimpel GE Parasitism of autumnal morphs of the soybean aphid, Aphis glycines (Hemiptera: Aphididae), by Binodoxys communis (Hymenoptera: Braconidae) on buckthorn. Ann Entomol Soc Am (in press).
3. Asplen MK, Hardin JA, Byrne DN (2009) The relationship between pre-oviposition flight behaviour and reproductive timing in whitefly parasitoids. Physiol Entomol 34: 350-358.
4. Bellamy DE, Byrne DN (2001) Effects of gender and mating status on self-directed dispersal by the whitefly parasitoid Eretmocerus eremicus. Ecol Entomol 26: 571-577.
5. Bellamy DE, Asplen MK, Byrne DN (2004) Impact of Eretmocerus eremicus (Hymenoptera: Aphelinidae) on open-field Bemisia tabaci (Hemiptera: Aleyrodidae) populations. Biol Control 29: 227-234.
6. Berlow EL, Brose U, Martinez ND (2008) The "Goldilocks factor" in food webs. Proc Natl Acad Sci USA 105: 4079-4080.
7. Blackmer JL, Cross D (2001) Response of Eretmocerus eremicus to skylight and plant cues in a vertical flight chamber. Entomol Exp Appl 100: 295-300.
8. Byrne DN, Buchmann SL, Spangler HG (1988) Relationship between wing loading, wingbeat frequency and body mass in homopterous insects. J Exp Biol 135: 9-23.
9. Byrne DN, Rathman RJ, Orum TV, Palumbo JC (1996) Localized migration and dispersal by the sweet potato whitefly, Bemisia tabaci. Oecologia (Heidelbg) 105: 320-328.
10. Caltagirone LE, Doutt RL (1989) The history of the vedalia beetle importation to California and its impact on the development of biological control. Annu Rev Entomol 34: 1-16.
11. Chacón JM, Heimpel GE (2010) Density-dependent intraguild predation of an aphid parasitoid. Oecologia (Heidelbg) 164: 213-220.
12. Cohen JC, Lundblad LK, Bates JHT, Levitzky M, Larson JE (2004) The "Goldilocks effect" in cystic fibrosis: identification of a lung phenotype in the cftr knockout and heterozygous mouse. BMC Genet 5: 21. doi: 10. 1186/1471-2156-5-21.
13. Collier T, van Steenwyk R (2004) A critical evaluation of augmentative biological control. Biol Control 31: 245-256.
14. Collier T, van Steenwyk R (2006) How to make a convincing case for augmentative biological control. Biol Control 39: 119-120.
15. Compton SG, Ellwood MDF, Davis AJ, Welch K (2000) The flight heights of chalcid wasps (Hymenoptera, Chalcidoidea) in a lowland bornean rain forest: fig wasps are the high fliers. Biotropica 32: 515-522.
16. Corbett A (1998) The importance of movement in the response of natural enemies to habitat manipulation. In: Pickett CH, Bugg RL (eds) Enhancing biological control. University of California Press, Berkeley, pp 25-48.
17. Corbett A, Plant RE (1993) Role of movement in the response of natural enemies to agroecosystem diversification: a theoretical evaluation. Environ Entomol 22: 519-531.
18. Corbett A, Rosenheim JA (1996) Quantifying movement of a minute parasitoid, Anagrus epos (Hymenoptera: Mymaridae), using fluorescent dust marking and recapture. Biol Control 6: 35-44.
19. De Clerck-Floate RA, Wikeem B, Bourchier RS (2005) Early establishment and dispersal of the weevil, Mogulones cruciger (Coleoptera: Curculionidae) for biological control of houndstongue (Cynoglossum officinale) in British Columbia, Canada. Biocontrol Sci Technol 15: 173-190.
20. Demmon AS, Nelson HJ, Ryan PJ, Ives AR, Synder WE (2004) Aphidius ervi increases its adult size by disrupting host wing development. Environ Entomol 33: 1523-1527.
21. Desneux N, Barta RJ, Hoelmer KA, Hopper KR, Heimpel GE (2009a) Multifaceted determinants of host specificity in an aphid parasitoid. Oecologia (Heidelbg) 160: 387-398.
22. Desneux N, Stary P, Delebecque CJ, Gariepy TD, Barta RJ, Hoelmer KA, Heimpel GE (2009b) Cryptic species of parasitoids attacking the soybean aphid (Hemiptera: Aphididae) in Asia: Binodoxys communis and Binodoxys koreanus (Hymenoptera: Braconidae: Aphidiinae). Ann Entomol Soc Am 102: 925-936.
23. Dixon AFG (2000) Insect predator-prey dynamics. Cambridge University Press, Cambridge.
24. Drea JJ, Hendrickson RM (1986) Analysis of a successful classical biological control project: the alfalfa blotch leafminer (Diptera: Agromyzidae) in the Northeastern United States. Environ Entomol 15: 448-455.
25. Fagan WF, Lewis MA, Neubert MG, van den Driessche P (2002) Invasion theory and biological control. Ecol Lett 5: 148-157.
26. Fauvergue X, Hopper KR (2009) French wasps in the New World: experimental biological control introductions reveal a demographic Allee effect. Popul Ecol 51: 385-397.
27. Fauvergue X, Malausa J-C, Giuge L, Courchamp F (2007) Invading parasitoids suffer no allele effect: a manipulative field experiment. Ecology 88: 2392-2403.
28. Feng M, Chen C, Shang S, Ying S, Shen Z, Chen X (2007) Aphid dispersal flight disseminates fungal pathogens and parasitoids as natural biological control agents of aphids. Ecol Entomol 32: 97-104.
29. Fournier F, Boivin G (2000) Comparative dispersal of Trichogramma evanescens and Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) in relation to environmental conditions. Environ Entomol 29: 55-63.
30. Gascoigne J, Berec L, Gregory S, Courchamp F (2009) Dangerously few liaisons: a review of mate-finding Allee effects. Popul Ecol 51: 355-372.
31. Gerling D, Alomar O, Arno J (2001) Biological control of Bemisia tabaci using predators and parasitoids. Crop Prot 20: 779-799.
32. Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Princeton.
33. Gordon RJ (1998) Foundations of the Goldilocks economy: supply shocks and the time-varying NAIRU. Brookings Pap Econ Act 2: 297-346.
34. Greatti M, Zandigiacomo P (1995) Postrelease dispersal of Trichogramma brassicae Bezdenko in corn fields. J Appl Entomol 119: 671-675.
35. Grevstad FS (1999) Factors influencing the chance of population establishment: implications for release strategies in biocontrol. Ecol Appl 9: 1439-1447.
36. Grevstad FS (2006) Ten-year impacts of the biological control agents Galerucella pusilla and G. calmariensis (Coleoptera: Chrysomelidae) on purple loosestrife (Lythrum salicaria) Central New York State. Biol Control 39: 1-8.
37. Gurr GM, Wratten S (1999) Integrated biological control: a proposal for enhancing success in biological control. Int J Pest Manag 45: 81-84.
38. Heimpel GE, De Boer JG (2008) Sex determination in the Hymenoptera. Annu Rev Entomol 53: 209-230.
39. Heimpel GE, Ragsdale DW, Venette R, Hopper KR, O'Neil RJ, Rutledge CE, Wu ZS (2004) Prospects for importation biological control of the soybean aphid: anticipating potential costs and benefits. Ann Entomol Soc Am 97: 249-258.
40. Heimpel GE, Frelich LE, Landis DA, Hopper KR, Hoelmer KA, Sezen Z, Asplen MK, Wu KM (2010) European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biol Invasions 12: 2913-2931.
41. Hoddle MS, van Driesche RG, Sanderson JP, Minkenberg OPJM (1998) Biological control of Bemisia argentifolii (Hemiptera: Aleyrodidae) on poinsettia with inundative releases of Eretmocerus eremicus (Hymenoptera: Aphelinidae): do release rates affect parasitism? Bull Entomol Res 88: 47-58.
42. Hodson JL, Hoffmann JH, Zimmermann HG (2003) Biological control of spear thistle, Cirsium vulgare (Asteraceae), in South Africa: a modest start for Rhinocyllus conicus (Coleoptera: Curculionidae). Afr Entomol 11: 15-20.
43. Hoelmer KA, Kirk AA (2005) Selecting arthropod biological control agents against arthropod pests: can the science be improved to decrease the risk of releasing ineffective agents. Biol Control 34: 255-264.
44. Hopper KR, Roush RT (1993) Mate finding, dispersal, number released, and the success of biological control introductions. Ecol Entomol 18: 321-331.
45. Hougardy E, Mills NJ (2006) The influence of host deprivation and egg expenditure on the rate of dispersal of a parasitoid following field release. Biol Control 37: 206-213.
46. Ireson JE, Webb WR (1996) Redistribution and establishment of Neomolgus capillatus (Kramer) (Acarina: Bdellidae) for the biological control of Sminthurus viridis (L) (Collembola: Sminthuridae) in Tasmania. Aust J Entomol 35: 243-246.
47. Ireson JE, Gourlay AH, Holloway RJ, Chatterton WS, Foster SD, Kwong RM (2008) Host specificity, establishment and dispersal of the gorse thrips, Sericothrips staphylinus Haliday (Thysanoptera: Thripidae), a biological control agent for gorse, Ulex europaeus L. (Fabaceae), in Australia. Biol Control 45: 460-471.
48. James DG (2003) Synthetic herbivore-induced plant volatiles as field attractants for beneficial insects. Environ Entomol 32: 977-982.
49. James DG, Price TS (2004) Field-testing of methyl salicylate for recruitment and retention of beneficial insects in grapes and hops. J Chem Ecol 8: 1613-1628.
50. Johnson KD, O'Neal ME, Ragsdale DW, Difonzo CD, Swinton SM, Dixon PM, Potter BD, Hodgson EW, Costamagna AC (2009) Profitability of cost-effective management of soybean aphid (Hemiptera: Aphididae) in North America. J Econ Entomol 102: 2101-2108.
51. Jones TH, Godfray HCJ, Hassell MP (1996) Relative movement patterns of a tephritid fly and its parasitoid wasps. Oecologia (Heidelbg) 106: 317-324.
52. Jonsen ID, Bourchier RS, Roland J (2001) The influence of matrix habitat on Aphthona flea beetle immigration to leafy spurge patches. Oecologia (Heidelbg) 127: 287-294.
53. Jonsen ID, Bourchier RS, Roland J (2007a) Effect of matrix habitat on the spread of flea beetle introductions for biological control of leafy spurge. Landsc Ecol 22: 883-896.
54. Jonsen ID, Bourchier RS, Roland J (2007b) Influence of dispersal, stochasticity, and an Allee effect on the persistence of weed biocontrol introductions. Ecol Model 203: 521-526.
55. Jonsson M, Wratten SD, Landis DA, Tompkins JL, Cullen R (2010) Habitat manipulation to mitigate the impacts of invasive arthropod pests. Biol Invasions 12: 2933-2945.
56. Kean JM, Barlow ND (2000) Effects of dispersal on local population increase. Ecol Lett 3: 479-482.
57. Keller MA, Lewis WJ, Stinner RE (1985) Biological and practical significance of movement by Trichogramma species - a review. Southwest Entomol 8: 138-155.
58. Kimberling DN (2004) Lessons from history: predicting successes and risks of intentional introductions for arthropod biological control. Biol Invasions 6: 301-318.
59. Kölliker-Ott UM, Bigler F, Hoffmann AA (2004) Field dispersal and host location of Trichogramma brassicae is influenced by wing size but not wing shape. Biol Control 31: 1-10.
60. Lavandero B, Wratten S, Hagler J, Jervis M (2004) The need for effective marking and tracking techniques for monitoring the movements of insect predators and parasitoids. Int J Pest Manag 50: 147-151.
61. Lee JC (2010) Effect of methyl salicylate-based lures on beneficial and pest arthropods in strawberry. Environ Entomol 39: 653-660.
62. Lee JC, Heimpel GE (2005) Impact of flowering buckwheat on lepidopteran cabbage pests and their parasitoids at two spatial scales. Biol Control 34: 290-301.
63. Levin DA, Kelley CD, Sarkar S (2009) Enhancement of Allee effects in plants due to self-incompatibility alleles. J Ecol 97: 518-527.
64. Lewis MA, Kareiva P (1993) Allee dynamics and the spread of invading organisms. Theor Popul Biol 43: 141-158.
65. Liebhold AM, Tobin PC (2008) Population ecology of insect invasions and their management. Annu Rev Entomol 53: 387-408.
66. Lommen STE, Middendorp CW, Luijten CA, van Schelt J, Brakefield PM, de Jong PW (2008) Natural flightless morphs of the ladybird beetle Adalia bipunctata improve biological control of aphids on single plants. Biol Control 47: 340-346.
67. Martinez-Ghersa MA, Ghersa CM (2006) The relationship of propagule pressure to invasion potential in plants. Euphytica 148: 87-96.
68. Mays WT, Kok LT (2003) Population dynamics and dispersal of two exotic biological control agents of spotted knapweed, Urophora affinis and U. quadrifasciata (Diptera: Tephritidae), in southwestern Virginia from 1986 to 2000. Biol Control 27: 43-52.
69. McDougall SJ, Mills NJ (1997) Dispersal of Trichogramma platneri Nagarkatti (Hym., Trichogrammatidae) from point-source releases in an apple orchard in California. J Appl Entomol 121: 205-209.
70. Memmott J, Fowler SV, Hill RL (1998) The effect of the release size on the probability of establishment of biological control agents: gorse thrips (Sericothrips staphylinus) released against gorse (Ulex europaeus) in New Zealand. Biocontrol Sci Technol 8: 103-115.
71. Obrycki JJ, Kring TJ (1998) Predaceous Coccinellidae in biological control. Annu Rev Entomol 43: 295-321.
72. Petit JN, Hoddle MS, Grandgirard J, Roderick GK, Davies N (2009) Successful spread of a biocontrol agent reveals a biosecurity failure: elucidating long distance invasion pathways for Gonatocerus ashmeadi in French Polynesia. BioControl 54: 485-495.
73. Pineda A, Marcos-Garcia MA (2008) Evaluation of several strategies to increase the residence time of Episyrphus balteatus (Diptera, Syrphidae) releases in sweet pepper greenhouses. Ann Appl Biol 152: 271-276.
74. Posthuma-Doodeman CJAM, van Lenteren JC, Sebestyen I, Ilovai Z (1996) Short-range flight test for quality control of Encarsia formosa. Proc Sect Exp Appl Entomol Neth Entomol Soc 7: 153-158.
75. Pratt PD, Slone DH, Rayamajhi MB, van TK, Center TD (2003) Geographic distribution and dispersal rate of Oxyops vitiosa (Coleoptera: Curculionidae), a biological control agent of the invasive tree Melaleuca quinquenervia in South Florida. Environ Entomol 32: 397-406.
76. Ragsdale DW, Voegtlin DJ, O'Neil RJ (2004) Soybean aphid biology in North America. Ann Entomol Soc Am 97: 204-208.
77. Ragsdale DW, McCornack BP, Venette RC, Potter BD, MacRae IV, Hodgson EW, O'Neal ME, Johnson KD, O'Neil RJ, Difonzo CD, Hunt TE, Glogoza PA, Cullen EM (2007) Economic threshold for soybean aphid (Hemiptera: Aphididae). J Econ Entomol 100: 1258-1267.
78. Ragsdale DW, Landis DA, Brodeur J, Heimpel GE, Desneux N (2011) Ecology and management of the soybean aphid in North America. Annu Rev Entomol 56: 375-399.
79. Rauwald KS, Ives AR (2001) Biological control in disturbed agricultural systems and the rapid re-establishment of parasitoids. Ecol Appl 11: 1224-1234.
80. Savary MA, Bloem KA, Bloem S, Carpenter JE, Hight SD, Dorn S (2008) Diel flight pattern and flight performance of Cactoblastis cactorum (Lepidoptera: Pyralidae) measured on a flight mill: influence of age, gender, mating status, and body size. J Econ Entomol 101: 314-324.
81. Seko T, Miura K (2009) Effects of artificial selection for reduced flight ability on survival rate and fecundity of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Appl Entomol Zool 44: 587-594.
82. Seko T, Yamashita K, Miura K (2008) Residence period of a flightless strain of the ladybird beetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in open fields. Biol Control 47: 194-198.
83. Shea K, Possingham HP (2000) Optimal release strategies for biological control agents: an application of stochastic dynamic programming to population management. J Appl Ecol 37: 77-86.
84. Solbreck C (1974) Maturation of post-hibernation flight behaviour in the coccinellid Coleomegilla maculata (DeGeer). Oecologia (Heidelbg) 17: 265-275.
85. Stahl SM (2001) Dopamine system stabilizers, aripiprazole, and the next generation of antipsychotics, Part 1: "Goldilocks" actions at dopamine receptors. J Clin Psychiatry 62: 841-842.
86. Stephens PA, Sutherland WJ, Freckleton RP (1999) What is the Allee effect? Oikos 87: 185-190.
87. Stouthamer R, Luck RF, Werren JH (1992) Genetics of sex determination and improvement of biological control using parasitoids. Environ Entomol 21: 427-435.
88. Taylor LR (1965) Flight behavior and aphid migration. Proc North Central Branch Entomol Soc Am 20: 9-19.
89. van Hezewijk BH, Bourchier RS, De Clerck-Floate RA (2010) Regional-scale impact of the weed biocontrol agent Mecinus janthinus on Dalmatian toadflax (Linaria dalmatica). Biol Control 55: 197-202.
90. van Lenteren JC (2006) How not to evaluate augmentative biological control. Biol Control 39: 115-118.
91. Vorley WT, Wratten SD (1987) Migration of parasitoids (Hymenoptera: Braconidae) of cereal aphids (Hemiptera: Aphididae) between grassland, early-sown cereals and late-sown cereals in southern England. Bull Entomol Res 77: 555-568.
92. Williams DM, Kasting JF, Wade RA (1997) Habitable moons around extrasolar giant planets. Nature 385: 234-236.
93. Wright MG, Hoffmann MP, Chenus SA, Gardner J (2001) Dispersal behavior of Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) in sweet corn fields: implications for augmentative releases against Ostrinia nubilalis (Lepidoptera: Crambidae). Biol Control 22: 29-37.
94. Wyckhuys KAG, Heimpel GE (2007) Response of the soybean aphid parasitoid Binodoxys communis to olfactory cues from target and non-target host-plant complexes. Entomol Exp Appl 123: 149-158.
95. Wyckhuys KAG, Koch RL, Heimpel GE (2007) Physical and ant-mediated refuges from parasitism: implications for non-target effects in biological control. Biol Control 40: 306-313.
96. Wyckhuys KAG, Stone L, Desneux N, Hoelmer KA, Hopper KR, Heimpel GE (2008) Parasitism of the soybean aphid Aphis glycines by Binodoxys communis: the role of aphid defensive behaviour and parasitoid reproductive performance. Bull Entomol Res 98: 361-370.
97. Wyckhuys KAG, Koch RL, Kula RR, Heimpel GE (2009) Potential exposure of a classical biological control agent of the soybean aphid, Aphis glycines, on non-target aphids in North America. Biol Invasions 11: 857-871.
98. Yamasaki L (1999) Balancing proliferation and apoptosis in vivo: the Goldilocks theory of E2F/DP action. Biochem Biopohys Acta Rev Cancer 1423: M9-M15.
99. Yu H, Zhang Y, Wu KM, Wyckhuys KAG, Guo Y (2009) Flight potential of Microplitis mediator, a parasitoid of various lepidopteran pests. Biocontrol 54: 183-193.
100. Zhang Y, Wu KM, Wyckhuys KAG, Heimpel GE (2009) Effect of parasitism on flight behavior of the soybean aphid, Aphis glycines. Biol Control 51: 475-479.