Intraguild interactions and aphid predators: Biological efficiency of Harmonia axyridis and Episyrphus balteatus

Journal of Applied Entomology

Volumn 134, Issue 1, 2010, Pages 34-44

  Alhmedi, A ^a   Haubruge, E ^a   Francis, F ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Biological control; Cannibalism; Intraguild predation; Invasion; Larval mobility; Natural enemy

Indexed keywords

APHID; BEETLE; BIOLOGICAL CONTROL; CANNIBALISM; EGG PRODUCTION; FLY; INTRAGUILD INTERACTION; LARVA; MICROCOSM; NATURAL ENEMY; OVIPOSITION; PREDATOR;

BELGIUM;

APHIDIDAE; EPISYRPHUS BALTEATUS; HARMONIA AXYRIDIS; MEGOURA VICIAE; VICIA FABA;

EID: 74349096202     PISSN: 09312048     EISSN: 14390418     Source Type: Journal    
DOI: 10.1111/j.1439-0418.2009.01445.x     Document Type: Article

References (100)

1. Adriaens T, San Martin y, Gomez G, Maes D, 2008. Invasion history, habitat preferences and phenology of the invasive ladybird Harmonia axyridis in Belgium. Biocontrol 53, 69 88.
2. Agarwala BK, Dixon AFG, 1992. Laboratory study of cannibalism and interspecific predation in ladybirds. Ecol. Entomol. 17, 303 309.
3. Agarwala BK, Yasuda H, 2001. Overlapping oviposition and chemical defense of eggs in two co-occurring species of ladybird predators of aphids. J. Ethol. 19, 47 53.
4. Alam N, Choi IS, Song KS, Hong J, Lee CO, Jung JH, 2002. A new alkaloid from two coccinellid beetles Harmonia axyridis and Aiolocaria haexapilota. B. Kor. Chem. Soc. 23, 497 499.
5. Alhmedi A, Francis F, Bodson B, Haubruge E, 2006. Étude de la diversité des pucerons et des auxiliaires aphidiphages relatives à la présence d'ortie à Gembloux. Notes Fauniq. Gembloux. 59, 121 124.
6. Alhmedi A, Haubruge E, Bodson B, Francis F, 2007. Aphidophagous guilds on nettle (Urtica dioica) strips close to fields of green pea, rape and wheat. Insect Sci. 14, 419 424.
7. Allan JD, Flecker AS, McClintock NL, 1987. Prey preference of stoneflies: sedentary vs. mobile prey. Oikos 49, 323 331.
8. Alyokhin A, Sewell G, 2004. Changes in a lady beetle community following the establishment of three alien species. Biol. Invasions 6, 463 471.
9. Ankersmith GW, Dijman H, Keuning NJ, Mertens H, Sins A, Tacoma HM, 1986. Episyrphus balteatus as a predator of aphid Sitobion avenae on winter wheat. Entomol. Exp. Appl. 42, 271 277.
10. Ayer WA, Browne LM, 1977. The ladybug alkaloids including synthesis and biosynthesis. Heterocycles 7, 685 707.
11. Bathon H, 2003. Invasive Nutzlingsarten, ein Problem fur den biologischen Pflanzenschutz. DGaaE Nachrichten, Darmstadt. 17, 8.
12. Branquart E, Hemptinne J-L, Bauffe C, Benfekih L, 1997. Cannibalism in Episyrphus balteatus (Diptera: Syrphidae). Entomophaga 42, 145 152.
13. Brown PMJ, Adriaense T, Bathon H, Cuppen J, Goldarazena A, Hägg T, Kenis M, Klausnitzer BEM, Kovar I, Loomans AJM, Majerus MEN, Nedved O, Pedersen J, Rabitsch W, Roy HE, Ternois V, Zakharov IA, Roy DB, 2008. Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. Biocontrol 53, 5 21.
14. Burgio G, Santi F, Maini S, 2005. Intra-guild predation and cannibalism between Harmonia axyridis and Adalia bipunctata adults and larvae: laboratory experiments. Bull. Insectol. 58, 135 140.
15. Chambers RJ, Adams THL, 1986. Quantification of the impact of hoverflies (Diptera: Syrphidae) on cereal aphids in winter wheat: an analysis of field populations. J. Appl. Ecol. 23, 895 904.
16. Chandler AEF, 1968a. The relationship between aphid infestations and oviposition by aphidophagous Syrphidae. Ann. Appl. Biol. 61, 425 434.
17. Chandler AEF, 1968b. Some factors influencing the occurrence and site of oviposition by aphidophagous Syrphidae (Diptera). Ann. Appl. Biol. 61, 435 446.
18. Chandler AEF, 1969. Locomotory behaviour of first instar larvae of aphidophagous Syrphidar (Diptera) after contact with aphids. Anim. Behav. 17, 673 678.
19. Chapman JW, Williams T, Escribano A, Caballero P, Cave RD, Goulson D, 1999. Age-related cannibalism and horizontal transmission of a nuclear polyhedrosis cirus in larval Spodoptera frugiperda. Ecol. Entomol. 24, 268 275.
20. Colunga-Garcia M, Gage SH, 1998. Arrival, establishment, and habitat use of the multicolored Asian lady beetle (Coleoptera: Coccinellidae) in a Michigan landscape. Environ. Entomol. 27, 1574 1580.
21. Costamagna AC, Landis DA, 2006. Predators exert top-down control of soybean aphid across a gradient of agricultural management systems. Ecol. Appl. 16, 1619 1628.
22. Cottrell TE, 2004. Suitability of exotic and native lady beetle eggs (Coleoptera: Coccinellidae) for development of lady beetle larvae. Biol. Control 31, 362 371.
23. Cottrell TE, 2005. Predation and cannibalism of lady beetle eggs by adult lady beetles. Biol. Control 34, 159 164.
24. Cottrell TE, 2007. Predation by adult and larval lady beetles (Coleoptera: Coccinellidae) on initial contact with lady beetles eggs. Environ. Entomol. 36, 390 401.
25. Cottrell TE, Yeargan KV, 1998a. Influence of a native weed, Acalypha ostryaefolia (Euphorbiaceae), on Coleomegilla maculata (Coleoptera: Coccinellidae) population density, predation, and cannibalism in sweet corn. Environ. Entomol. 27, 1375 1385.
26. Cottrell TE, Yeargan KV, 1998b. Effect of pollen on Coleomegilla maculata (Coleoptera: Coccinellidae) population density, predation, and cannibalism in sweet corn. Environ. Entomol. 27, 1402 1410.
27. Cottrell TE, Yeargan KV, 1999. Intraguild predation between an introduced lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae), and a native lady beetle, Coleomegilla maculate (Coleoptera: Coccinellidae). J. Kans. Entomol. Soc. 71, 159 163.
28. De Almeida LM, Da Silva VB, 2002. Primeiro registro de Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae): um coccinelideo originario da regiao Paleartica. Rev. Bras. Zool. 19, 941 944.
29. Dixon AFG, 2000. Insect predator-prey dynamics: ladybird beetles and biological control. Cambridge University Press, Cambridge.
30. Elliott N, Kieckhefer R, Kauffman W, 1996. Effects of an invading coccinellid on native cocccinellids in an agricultural landscape. Oecologia 105, 537 544.
31. Evans EW, 1991. Intra versus interspecific interactions of ladybeetles (Coleoptera: Coccinellidae) attacking aphids. Oecologia 87, 401 408.
32. Felix S, Soares AO, 2004. Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera: Coccinellidae): the role of body weight. Eur. J. Entomol. 101, 237 242.
33. Ferran A, Niknam H, Kabiri F, Picart J-L, De Herce C, Brun J, Iperti G, Lapchin L, 1996. The use of Harmonia axyridis larvae (Coleoptera: Coccinellidae) against Macrosiphum rosae (Hemiptera: Sternorrhyncha: Aphididae) on rose bushes. Eur. J. Entomol. 93, 59 67.
34. Fox LR, 1975. Cannibalism in natural population. Annu. Rev. Ecol. Syst. 6, 87 106.
35. Galvan TL, Burkness EC, Hutchison WD, 2006. Wine grapes in the Midwest: reducing the risk of the multicolored Asian lady beetle. Publication 08232. University of Minnesota Extension Service, St Paul, MN, 2 p.
36. Garcia MF, Becerra VC, Reising CE, 1999. Harmonia axyridis Pallas (Coleoptera, Coccinellidae) estudio biologico. Rev. FCA UNCuyo 31, 85 91.
37. Gardiner MM, Landis DA, 2007. Impact of intraguild predation by adult Harmonia axyridis (Coleoptera: Coccinellidae) on Aphis glycines (Hemiptera: Aphididae) biological control in cage studies. Biol. Control 40, 386 395.
38. Hahn J, Kovach J (Eds 2004. Multicolored Asian lady beetles in agriculture and urban environments: instant Symposium. Am. Entomol. 50, 152 168.
39. Hassan SA, 1975. Über die Massenzucht von Chrysopha carnea. Zeitschr. Angewand. Entomol. 7, 310 315.
40. Hemptinne JL, Dixon AFG, Coffin J, 1992. Attack strategy of ladybird beetle (Coccinellidae): factors shaping their numerical response. Oecologia 90, 238 245.
41. Hemptinne J-L, Lognay G, Gauthier C, Dixon AFG, 2000a. Role of surface chemical signals in egg cannibalism and intraguild predation in ladybirds (Coleoptera: Coccinellidae). Chemoecology 10, 123 128.
42. Hemptinne J-L, Dixon AFG, Gauthier C, 2000b. Nutritive cost of intraguild predation on eggs of Coccinella septempunctata and Adalia bipunctata (Coleoptera: Coccinellidae). Eur. J. Entomol. 97, 559 562.
43. Hindayana D, 2001. Resource exploitation by Episyrphus balteatus DeGeer (Diptera: Syrphidae) and intraguild predation. PhD Thesis, University Hannover, Germany, 95 p.
44. Hindayana D, Meyhöfer R, Scholz D, Poehling H-M, 2001. Intraguild predation among the hoverfly Episyrphus balteatus de Geer (Diptera: Syrphidae) and other aphidophagous predators. Biol. Control 20, 236 246.
45. Hodek I, Honèk A, 1996. Ecology of Coccinellidae. Kluwer Academic Publishers, Dordrecht, Boston, London. Series Entomologica 54, 464 p.
46. Iablokoff-Khnzorian SM, 1982. Les coccinelles; Coléoptères- Coccinellidae. Société Nouvelle des Éditions Boubée, Paris.
47. Janssen A, Montserrat M, HilleRisLambers R, de Roos AM, Pallini A, Sabelis MW, 2006. Intraguild predation usually does not disrupt biological control. Trophic Guild Interact. Biol. Control 3, 21 44.
48. Kajita Y, Takano F, Yasuda H, Agarwala BK, 2000. Effects of indigenous ladybird species (Coleoptera : Coccinellidae) on the survival of an species in relation to prey abundance. Appl. Entomol. Zool. 35, 473 479.
49. Klausnitzer B, 2004. Harmonia axyridis (Pallas, 1773) in Basel-Stadt (Coleptera, Coccinellidae). Mitt. Entomol. Ges. Basel 54, 115 122.
50. Koch RL, 2003. The multicoloured Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control and non-target impacts. J. Insect Sci. 3, 1 16.
51. Koch RL, Burkness EC, Wold Burkness SJ, Hutchison WD, 2004. Phytophagous preferences of the multicolored Asian lady beetle (Coleoptera Coccinellidae) for autumn-ripening fruit. J. Econ. Entomol. 97, 539 544.
52. Lanzoni A, Accinelli G, Bazzocchi GG, Burgio G, 2004. Biological traits and life table of the exotic Harmonia axyridis compared with Hippodamia variegata, and Adalia bipunctata (Col., Coccinellidae). J. Appl. Entomol. 128, 298 306.
53. van Lenteren JC, Babendreier D, Bigler F, Burgio G, Hokkanen HMT, Kuske S, Loomans AJM, Menzler-Hokkanen I, Van Rijn PCJ, Thomas MB, Tommasini MG, Zeng Q-Q, 2003. Environmental risk assessment of exotic natural enemies in inundative biological control. Biocontrol 48, 3 38.
54. Losey JE, Denno RF, 1998. Positive predator-prey interactions: enhanced predation rates and synergistic suppression of aphid populations. Ecology 79, 2143 2152.
55. Lucas E, 2005. Intraguild predation among aphidophagous predators. Eur. J. Entomol. 102, 351 364.
56. Lucas E, Coderre D, Brodeur J, 1998. Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology 79, 1084 1092.
57. Lucas E, Gagne I, Coderre D, 2002. Impact of the arrival of Harmonia axyridis on adults of Coccinella septempunctata and Coleomegilla maculata (Coleoptera: Coccinellidae). Eur. J. Entomol. 99, 457 463.
58. Lucas E, Vincent C, Labrie G, Chouinard G, Fournier F, Pelletier F, Bostanian NJ, Coderre D, Mignault M-P, Lafontaine P, 2007. The multicolored Asian ladybeetle Harmonia axyridis (Coleoptera: Coccinellidae) in Quebec agroecosystems ten years after its arrival. Eur. J. Entomol. 104, 737 743.
59. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA, 2000. Biotic invasions: causes, epidemiology, global consequences, and control. Ecol. Appl. 10, 689 710.
60. Magro A, Tene JN, Bastin N, Dixon AFG, Hemptinne JL, 2007. Assessment of patch quality by ladybirds: relative response to conspecific and heterospecific larval tracks a consequence of habitat similarity? Chemoecology 17, 37 45.
61. Majerus MEN, Roy HE, 2005. Scientific opportunities presented by the arrival of the harlequin ladybird, Harmonia axyridis, in Britain. Antenna Lond. 29, 196 208.
62. Majerus MEN, Strawson V, Roy HE, 2006. The potential impacts of the arrival of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain. Ecol. Entomol. 31, 207 215.
63. Michaud JP, 2002. Invasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera: Coccinellidae) and asymmetric competition with a native species, Cycloneda sanguinea. Environ. Entomol. 31, 827 835.
64. Michaud JP, 2003. A comparative study of larval cannibalism in three species of ladybirds (Coleoptera: Coccinellidae). J. Entomol. Sci. 28, 92 101.
65. Michaud JP, Grant AK, 2003. Intraguild predation among ladybeetles and a green lacewing: do the larval spines of Curinus coeruleus (Coleoptera: Coccinellidae) serve a defensive function? Bull. Entomol. Res. 93, 499 505.
66. New TR, 1991. Insects as predators. The New South Wales Univ Press, Australian Institute of Biology, Kensington, NSW, Australia, 178 pp.
67. Nordlund DA, Morrison RK, 1990. Handling time, prey preference and functional response for Chrysoperla rufilabris in the laboratory. Entomol. Exp. Appl. 57, 237 242.
68. Obrycki JJ, Giles KL, Ormrod AM, 1998. Interactions between an introduced and indigenous coccinellid species at different prey densities. Oecologia 117, 279 285.
69. Osawa N, 1993. Population studies of the aphidophagous ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae): life tables and key factor analysis. Res. Popul. Ecol. 35, 335 348.
70. Osawa N, 2000. Population field studies on the aphidophagous ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae): resource tracking and population characteristics. Popul. Ecol. 42, 115 127.
71. Pell JK, Baverstock J, Roy HE, Ware RL, Majerus MEN, 2008. Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. Biocontrol 53, 147 168.
72. Pickering G, Lin J, Riesen R, Reynolds A, Brindel I, Soleas G, 2004. Influence of Harmonia axyridis on the sensory properties of white and red wine. Am. J. Enol. Vitic. 55, 153 159.
73. Poehling H-M, 1988. Influence of cereal aphid control on specific predators in winter wheat (Homoptera: Aphididae). Entomol. Gen. 13, 163 174.
74. Poehling H-M, Tenhumberg B, Groeger U, 1991. Different pattern of cereal aphid population dynamics in northern and southern areas of West Germany. IOBC/WPRS Bull. 14, 1 12.
75. Polis GA, Holt RD, 1992. Intraguild predation: the dynamics of complex trophic interactions. Trends Ecol. Evol. 7, 151 154.
76. 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.
77. Prasad RP, Snyder WE, 2004. Predator interference limits fly egg biological control by a guild of ground-active beetles. Biol. Control 31, 428 437.
78. Putra NS, Yasuda H, Sato S, 2009. Oviposition preference of two hoverfly species in response to risk of intraguild predation. Appl. Entomol. Zool. 44, 29 36.
79. Rosenheim JA, Glik TE, Goeriz RE, Ramert B, 2004. Linking a predator's foraging behaviour with its effects on herbivore population suppression. Ecology 85, 3362 3372.
80. Roy HE, Brown P, Majerus MEN, 2006. Harmonia axyridis: a successful biocontrol agent or an invasive threat? In : An ecological and societal approach to biological control. Ed. by Eilenberg J, Hokkanen H, Kluwer Academic Publishers, Dordrecht, The Netherlands, 295 309.
81. Santi F, Burgio G, Maini S, 2003. Intra-guild predation and cannibalism of Harmonia axyridis and Adalia bipunctata in choice conditions. Bull. Insectol. 56, 207 210.
82. SAS, 1998. SAS, version 6.1. SAS Institute, Cary, NC.
83. Sato S, Dixon AFG, 2004. Effect of intraguild predation on the survival and development of three species of aphidophagous ladybirds: consequences for invasive species. Agr. Forest. Entomol. 6, 21 24.
84. Sato S, Dixon AFG, Hironori Y, 2003. Effect of emigration on cannibalism and intraguild predation in aphidophagous ladybirds. Ecol. Entomol. 28, 628 633.
85. Scholz D, Poehling H-M, 2000. Oviposition site selection of Episyrphus balteatus. Entomol. Exp. Appl. 94, 149 158.
86. Snyder WE, Evans EW, 2006. Ecological effects of invasive arthropod generalist predators. Annu. Rev. Ecol. Evol. 37, 95 122.
87. Snyder WE, Ives AR, 2003. Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid biocontrol. Ecology 84, 91 107.
88. Snyder WE, Wise DH, 1999. Predator interference and the establishment of generalist predators populations for biocontrol. Biol. Control 15, 283 292.
89. Snyder WE, Clevenger GM, Eigenbrode SD, 2004. Intraguild predation and successful invasion by introduced ladybird beetles. Oecologia 140, 559 565.
90. Straub CS, Finke DL, Snyder WE, 2008. Are the conservation of natural enemy biodiversity and biological control compatible goals? Biol. Control 45, 225 237.
91. Tenhumberg B, Poehling H-M, 1995. Syrphids as natural enemies of cereal aphids in Germany: aspects of their biology and efficacy in different years and regions. Agr. Ecosyst. Environ. 52, 39 43.
92. 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.
93. Ware RL, Ramon-Portugal F, Magro A, Ducamp C, Hemptinne JL, Majerus MEN, 2008. Chemical protection of Calvia quatuordecimguttata eggs against intraguild predation by the invasive ladybird Harmonia axyridis. Biocontrol 53, 189 200.
94. Weisser WW, 2003. Additive effects of pea aphid natural enemies despite intraguild predation. Arquipelago, Life Mar. Sci. 5 (Suppl. 11 15.
95. Williamson M, 1996. Biological invasions. Chapman and Hall, London.
96. With KA, Pavuk DM, Worchuck JL, Oates RK, Fisher JL, 2002. Threshold effects of landscape structure on biological control in agroecosystems. Ecol. Appl. 12, 52 65.
97. Yasuda H, Ohnuma N, 1999. Effect of cannibalism and predation on the larval performance of two ladybird beetles. Entomol. Exp. Appl. 93, 63 67.
98. Yasuda H, Takagi T, Kogi K, 2000. Effects of conspecific and heterospecific larval tracks on the oviposition behaviour of the predatory ladybird, Harmonia axyridis (Coleoptera: Coccinellidae). Eur. J. Entomol. 97, 551 553.
99. Yasuda H, Kikuchi T, Kindlmann P, Sato S, 2001. Relationships between attack and escape rates, cannibalism, and intraguild predation in larvae of two predatory ladybirds. J. Insect. Behav. 14, 373 384.
100. Yasuda H, Evans EW, Kajita Y, Urakawa K, Takizawa T, 2004. Asymmetric larval interactions between introduced and indigenous ladybirds in North America. Oecologia 141, 722 731.