Advertisement

Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives

  • Judith K. PellEmail author
  • Jason Baverstock
  • Helen E. Roy
  • Remy L. Ware
  • Michael E. N. Majerus

Abstract

As an effective generalist predator of aphids and other hemipteran pests H. axyridis has been a successful biological control agent. However, the very functional traits that have contributed to its success in this regard also implicate it as an intraguild predator that poses a significant risk not only to the diversity of other natural enemies of Hemiptera (and their associated ecosystem services), but to biodiversity more widely. In this paper we will specifically review the existing data on intraguild predation involving H. axyridis, and consider the strength and symmetry of such interactions both within its native guild and within exotic guilds where it has established as an invasive alien. We will use these studies to interpret the observed population declines in predator diversity in the field, predict species at risk in regions not yet invaded and consider implications for resulting ecosystem services. We will also indicate gaps in our knowledge that require further study in order to identify opportunities for mitigation.

Keywords

Coccinellidae Harmonia axyridis Aphidophagous guild Intraguild predation Predators Parasitoids Pathogens Ecosystem services 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Agarwala BK, Dixon AFG (1992) Laboratory study of cannibalism and interspecific predation in ladybirds. Ecol Entomol 17:303–309Google Scholar
  2. 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 23:497–499CrossRefGoogle Scholar
  3. Barbosa P (ed) (1998) Conservation biological control. Academic Press, San Diego, CA, 396 ppGoogle Scholar
  4. Baverstock J, Alderson PG, Pell JK (2005) Influence of the aphid pathogen Pandora neoaphidis on the foraging behaviour of the aphid parasitoid Aphidius ervi. Ecol Entomol 30:665–672CrossRefGoogle Scholar
  5. Berkvens N, Bonte J, Berkvens D, Deforce K, Tirry L, De Clercq P (2007) Pollen as an alternative food for Harmonia axyridis. BioControl (this issue). doi: 10.1007/s10526-007-9128-7 Google Scholar
  6. Brown MW, Miller SS (1998) Coccinellidae (Coleoptera) in apple orchards of eastern West Virginia and the impact of invasion by Harmonia axyridis. Entomol News 109:143–151Google Scholar
  7. Brown PMJ, Roy HE, Rothery P, Roy DB, Ware RL, Majerus MEN (2007) Harmonia axyridis in Great Britain: analysis of the spread and distribution of a non-native coccinellid. BioControl (this issue). doi: 10.1007/s10526-007-9124-y Google Scholar
  8. Buntin GD, Bouton JH (1997) Aphid (Homoptera: Aphididae) management in alfalfa by spring grazing cattle. J Entomol Sci 32:332–342Google Scholar
  9. Butt TM, Ibrahim L, Ball BV, Clark SJ (1994) Pathogenicity of the entomogenous fungi, Metarhizium anisopliae and Beauveria bassiana against crucifer pests and the honey bee. Biocontrol Sci Techn 4:207–214CrossRefGoogle Scholar
  10. Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, Sankaran M, Jouseau C (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–992PubMedCrossRefGoogle Scholar
  11. Casula P, Wilby A, Thomas MB (2006) Understanding biodiversity effects on prey in multi-enemy systems. Ecol Lett 9:995–1004PubMedCrossRefGoogle Scholar
  12. Chang GC (1996) Comparison of single versus multiple species of generalist predators for biological control. Environ Entomol 25:207–212Google Scholar
  13. 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 27:1574–1580Google Scholar
  14. Cottrell TE (2004) Suitability of exotic and native lady beetle eggs (Coleoptera: Coccinellidae) for development of lady beetle larvae. Biol Control 31:362–371CrossRefGoogle Scholar
  15. Cottrell TE (2007) Predation by adult and larval lady beetles (Coleoptera: Coccinellidae) on initial contact with lady beetles eggs. Environ Entomol 36:390–401PubMedCrossRefGoogle Scholar
  16. Cottrell TE, Yeargan KV (1998) Intraguild predation between an introduced lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae) and a native lady beetle, Coleomegilla maculata (Coleoptera: Coccinellidae). J Kansas Entomol Soc 71:159–163Google Scholar
  17. De Clercq P, Peeters I, Vergauwe G, Thas O (2003) Interaction between Podisus maculiventris and Harmonia axyridis, two predators used in augmentative biological control in greenhouse crops. BioControl 48:39–55CrossRefGoogle Scholar
  18. Denoth M, Frid L, Myers JH (2002) Multiple agents in biological control: improving the odds. Biol Control 24:20–30CrossRefGoogle Scholar
  19. Diehl S (1993) Relative consumer sizes and the strength of direct and indirect interactions in omnivorous feeding relationships. Oikos 68:151–157CrossRefGoogle Scholar
  20. Dixon AFG (2000) Insect predator-prey dynamics: ladybird beetles and biological control. Cambridge University Press, Cambridge, UKGoogle Scholar
  21. Elliott N, Kieckhefer R, Kauffman W (1996) Effects of an invading coccinellid on native cocccinellids in an agricultural landscape. Oecologia 105:537–544CrossRefGoogle Scholar
  22. Elmquist T, Folke C, Nyström M, Peterson G, Bengtsson J, Walker B, Norberg J (2003) Response diversity, ecosystem change and resilience. Front Ecol Environ 1:488–494Google Scholar
  23. Evans EW (1991) Intra versus interspecific interactions of ladybeetles (Coleoptera; Coccinellidae) attacking aphids. Oecologia 87:401–408CrossRefGoogle Scholar
  24. Evans EW (2000) Morphology of invasion: body size patterns associated with establishment of Coccinella septempunctata (Coleoptera: Coccinellidae) in western North America. Eur J Entomol 97:469–474Google Scholar
  25. Evans EW (2004) Habitat displacement of North American ladybirds by an introduced species. Ecology 85:637–647CrossRefGoogle Scholar
  26. 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 101:237–242Google Scholar
  27. Ferguson KI, Stiling P (1996) Non-additive effects of multiple natural enemies on aphid populations. Oecologia 108:375–379Google Scholar
  28. Finke DL, Denno RF (2004) Predator diversity dampens trophic cascades. Nature 429:407–410PubMedCrossRefGoogle Scholar
  29. Flowers RW, Salom SM, Kok LT (2006) Competitive interactions among two specialist predators and a generalist predator of hemlock woolly adelgid, Adelges tsugae (Hemiptera: Adelgidae) in south-western Virginia. Agr Forest Entomol 8:253–262CrossRefGoogle Scholar
  30. Foster SP, Devine G, Devonshire AL (2007) Insecticide resistance. In: Harrington R, van Emden H (eds) Aphids as crop pests. CABI International, pp 261–285, 717Google Scholar
  31. Fremlin M (2007) Intra-guild predation of harlequin ladybird larvae by lacewing larvae. Bull Amat Entomol Soc 66:110–116Google Scholar
  32. Fuentes-Contreras E, Pell JK, Niemeyer HM (1998) Influence of plant resistance at the third trophic level: interactions between parasitoids and entomopathogenic fungi of cereal aphids. Oecologia 117:426–432CrossRefGoogle Scholar
  33. 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 40:386–395CrossRefGoogle Scholar
  34. Godeau J-F (2000) Coccinelles amies des fourmis. 2/2/ Groupe de Travail Coccinula. Feuille de Contact 2:10–15Google Scholar
  35. Gordon RD (1985) The Coccinellidae (Coleoptera) of America North of Mexico. J New York Entomol Soc 93:1–912Google Scholar
  36. Gurr GM, Scarratt SL, Wratten SD, Berndt L, Irvin N (2004) Ecological engineering, habitat manipulation and pest management. In: Gurr GM, Wratten SD, Altieri MA (eds) Ecological engineering for pest management: advances in habitat manipulation for arthropods. CSIRO Publishing, pp 1–12Google Scholar
  37. Hemmati F (1999) Aerial dispersal of the entomopathogenic fungus Erynia neoaphidis. PhD Thesis, University of Reading 186 ppGoogle Scholar
  38. Hemptinne JL, Dixon AFG (2000) Defence, oviposition and sex: semiochemical parsimony in two species of ladybird beetles (Coleoptera: Coccinellidae)? A short review. Eur J Entomol 97:443–447Google Scholar
  39. Herrick NJ, Reitz SR (2004) Temporal occurrence of Podisus maculiventris (Hemiptera: Heteroptera: Pentatomidae) in North Florida. Fla Entomol 87:587–590CrossRefGoogle Scholar
  40. Hironori Y, Katsuhiro S (1997) Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Entomophaga 42:153–163CrossRefGoogle Scholar
  41. Hodek I (1996) Food relationships. In: Hodek I, Honek A (eds) Ecology of Coccinellidae. Kluwer Academic Publishers, Dordrecht pp 143–238Google Scholar
  42. Hodek I, Honek A (1988) Sampling, rearing and handling of aphid predators. In: Minks AK, Harrewijn P (eds) Aphids, their biology, natural enemies and control, Vol. 2B. Amsterdam, Elsevier, pp 311–321Google Scholar
  43. Hölldobler B, Wilson EO (1990) The ants. Springer Verlag, BerlinGoogle Scholar
  44. Holt RD, Polis GA (1997) A theoretical framework for intraguild predation. Am Nat 149:745–764CrossRefGoogle Scholar
  45. Hough-Goldstein J, Cox J, Armstrong A (1996) Podisus maculiventris (Hempitera: Pentatomidae) predation on ladybird beetles (Coleoptera: Coccinellidae). Fla Entomol 79:64–68CrossRefGoogle Scholar
  46. Huey RB, Pianka ER (1981) Ecological consequences of foraging mode. Ecology 62:991–999CrossRefGoogle Scholar
  47. Hufbauer RA, Roderick GK (2005) Microevolution in biological control: mechanisms, patterns and processes. Biol Control 35:227–239CrossRefGoogle Scholar
  48. Inglis GD, Goettel MS, Butt TM, Strasser H (2001) Use of hyphomycetous fungi for managing insect pests. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential. CABI, Wallingford, pp 23–69Google Scholar
  49. Itioka T, Inoue T (1996) The role of predators and attendant ants in the regulation of a population of the citrus mealybug Pseudococcus citriculus in a satsuma orange orchard. Appl Entomol Zool 31:195–202Google Scholar
  50. Ives AR, Cardinale BJ, Snyder WE (2005) A synthesis of subdisciplines: predator-prey interactions and biodiversity and ecosystem functioning. Ecol Lett 8:102–116CrossRefGoogle Scholar
  51. James RR, Lighthart B (1994) Susceptibility of the convergent lady beetle (Coleoptera, Coccinellidae) to four entomogenous fungi. Env Entomol 23:190–192Google Scholar
  52. Janssen A, Montserrat M, HilleRisLambers R, de Roos AM, Pallini A, Sabelis MW (2006) Intraguild predation usually does not disrupt biological control. In: Brodeur J, Boivin G (eds) Trophic and guild interactions in biological control. Springer, Dordrecht, The Netherlands, pp 21–44CrossRefGoogle Scholar
  53. Jiggins C, Majerus MEN, Gough U (1993) Ant defence of colonies of Aphis fabae Scopoli (Hemiptera: Aphididae), against predation by ladybirds. Brit J Entomol Nat Hist 6:129–138Google Scholar
  54. 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 35:473–479CrossRefGoogle Scholar
  55. Kajita Y, Yasuda H, Evans EW (2006) Effects of native ladybirds on oviposition of the exotic species, Adalia bipunctata (Coleoptera: Coccinellidae), in Japan. Appl Entomol Zool 41:57–61CrossRefGoogle Scholar
  56. Keller S, Zimmerman G (1989) Mycopathogens of soil insects. In: Wilding N, Collins NM, Hammond PM, Webber JF (eds) Insect-fungus interactions. Academic Press, LondonGoogle Scholar
  57. King A, Meinwald J (1996) Review of the defensive chemistry of coccinellids. Chem Rev 96:1105–1122CrossRefGoogle Scholar
  58. Koch RL (2003) The multicoloured Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control and non-target impacts. J Ins Sci 3:32–47Google Scholar
  59. Koch R, Venette R, Hutchison W (2006) Predicted impact of an exotic generalist predator on monarch butterfly (Lepidoptera: Nymphalidae) populations: a quantitative risk assessment. Biol Invasions 8:1179–1193CrossRefGoogle Scholar
  60. Koyama S, Majerus MEN (2007) Interactions between the parasitoid wasp Dinocampus coccinellae and two species of coccinellid from Japan and Britain. BioControl (this issue). doi: 10.1007/s10526-007-9138-5 Google Scholar
  61. Krauss U, Poehling HM (1996) Overwintering, oviposition and population dynamics of hoverflies (Diptera: Syrphidae) in northern Germany in relation to small and large-scale landscape structure. Acta Jutlandica 71:157–169Google Scholar
  62. Kuznetsov VN (1988) The Coccinellidae of the far East in Transcaucasia. Zashchita Rastenii. 5(19) (in Russian)Google Scholar
  63. Kuznetsov VN (1997) Lady beetles of the russian far east, (Memoir Series No. 1). Center for Systematic Entomology, Gainesville, FLGoogle Scholar
  64. LaMana ML, Miller JC (1996) Field observation on Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Oregon. Biol Control 6:232–237CrossRefGoogle Scholar
  65. Landis DA, Wratten SD, Gurr GM (2000) Habitat manipulation to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201PubMedCrossRefGoogle Scholar
  66. Loreau M, Mouquet N, Gonzales A (2003) Biodiversity as spatial insurance in heterogeneous landscapes. PNAS USA 100:12765–12770PubMedCrossRefGoogle Scholar
  67. Losey JE, Denno RF (1998) Positive predator-prey interactions: enhanced predation rates and synergistic suppression of aphid populations. Ecology 79:2143–2152Google Scholar
  68. Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56:311–323CrossRefGoogle Scholar
  69. Losey JE, Ives AR, Harmon J, Ballantyne F, Brown C (1997) A polymorphism maintained by opposite patterns of parasitism and predation. Nature 388:269–272CrossRefGoogle Scholar
  70. Lucas E (2005) Intraguild predation among aphidophagous predators. Eur J Entomol 102:351–364Google Scholar
  71. Lucas E, Coderre D, Brodeur J (1998) Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology 79:1084–1092CrossRefGoogle Scholar
  72. Lucas E, Gagne I, Coderre D (2002) Impact of the arrival of adults of Harmonia axyridis on adults of Coccinella septempunctata and Coleomegilla maculata (Coleoptera: Coccinellidae). Eur J Entomol 99:457–463Google Scholar
  73. Magalhaes BP, Lord JC, Wraight SP, Daoust RA, Roberts DW (1988) Pathogenicity of Beauveria bassiana and Zoophthora radicans to the coccinellid predators Coleomegilla maculata and Eriopis connexa. J Invertebr Pathol 52:471–473CrossRefGoogle Scholar
  74. 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 17:37–45CrossRefGoogle Scholar
  75. Majerus MEN (1994) Ladybirds. HarperCollins, London, 320 ppGoogle Scholar
  76. 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 31:207–215CrossRefGoogle Scholar
  77. Majerus MEN, Sloggett JJ, Godeau J-F, Hemptinne J-L (2007) Interactions between ants and aphidophagous and coccidophagous ladybirds. Popul Ecol 49:15–27CrossRefGoogle Scholar
  78. McPherson JE (1980) A list of the prey species of Podisus maculiventris (Hemiptera: Pentatomidae). Great Lakes Entomol 13:17–24Google Scholar
  79. Meyling NV, Pell JK (2006) Detection and avoidance of an entomopathogenic fungus by a generalist insect predator. Ecol Entomol 31:162–171CrossRefGoogle Scholar
  80. Michaud JP (2002) Invasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera: Coccinellidae) and asymmetric competition with a native species, Cycloneda sanguinea. Env Entomol 31:827–835CrossRefGoogle Scholar
  81. Müller CB, Brodeur J (2002) Intraguild predation in biological control and conservation biology. Biol Control 25:216–223CrossRefGoogle Scholar
  82. Musser FR, Shelton AM (2003) Bt sweet corn and selective insecticides: impacts on pests and predators. J Econ Entomol 96:71–80PubMedGoogle Scholar
  83. Naeem S, Li S (1997) Biodiversity enhances ecosystem reliability. Nature 390:507–509CrossRefGoogle Scholar
  84. Nakashima Y, Birkett MA, Pye BJ, Pickett JA, Powell W (2004) The role of semiochemicals in the avoidance of the seven-spot ladybird Coccinella septempunctata by the aphid parasitoid, Aphidius ervi. J Chem Ecol 30:1103–1116PubMedCrossRefGoogle Scholar
  85. Nault BA, Kennedy GG (2003) Establishment of multicoloured Asian lady beetle in Eastern North Carolina: seasonal abundance and crop exploitation within an agricultural landscape. BioControl 48:363–378CrossRefGoogle Scholar
  86. Ormond E (2007) The overwintering interactions of the seven spot ladybird (Coccinella septempunctata) and the entomopathogenic fungus Beauveria bassiana. PhD Thesis, Anglia Ruskin UniversityGoogle Scholar
  87. Ormond EL, Pell JK, Thomas APM, Roy HE (2006) Overwintering ecology of Coccinella septempunctata, Beauveria bassiana and Dinocampus coccinellae. In: Rossing WAH, Eggenschwiler L, Poehling H-M (eds) Working Group “Landscape management for functional biodiversity” at Zürich-Reckenholz (Switzerland), 16–19 May 2006 IOBC/WPRS Bulletin 29, pp 85–88Google Scholar
  88. Östman O, Ekbom B, Bengtsson J (2001) Farming practice and landscape heterogeneity influence biological control. Basic Appl Ecol 2:365–371CrossRefGoogle Scholar
  89. Pasteels JM, Deroe C, Tursch B, Braekman JC, Daloze D, Hootele C (1973) Distribution et activités des alcaloïdes défensives des Coccinellidae. J Insect Physiol 19:1771–1784CrossRefGoogle Scholar
  90. Pell JK (2008) Ecological approaches to pest management using entomopathogenic fungi; concepts, theory, practice and opportunities. In: Ekesi S, Maniania N (ed) Research Signpost (In press)Google Scholar
  91. Pell JK, Vandenberg JD (2002) Interactions among Diuraphis noxia, the fungal pathogen Paecilomyces fumosoroseus and the coccinellid Hippodamia convergens. Biocontrol Sci Tech 12:217–224CrossRefGoogle Scholar
  92. Pell JK, Pluke R, Clark SJ, Kenward MG, Alderson PG (1997) Interactions between two aphid natural enemies, the entomopathogenic fungus, Erynia neoaphidis and the predatory beetle, Coccinella septempunctata. J Invertebr Pathol 69:261–268CrossRefGoogle Scholar
  93. Pell JK, Eilenberg J, Hajek AE, Steinkraus DS (2001) Biology, ecology and pest management potential of entomophthorales. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential. CABI International, pp 71–154, 390Google Scholar
  94. Pervez A, Omkar (2006) Ecology and biological control application of multicoloured Asian ladybird, Harmonia axyridis. A review. Biocontrol Sci Tech 16:111–128CrossRefGoogle Scholar
  95. Phoofolo MW, Obrycki JJ (1998) Potential for intraguild predation and competition among predatory Coccinellidae and Chrysopidae. Entomol Exp Appl 89:47–55CrossRefGoogle Scholar
  96. Polis GA (1994) Food web, trophic cascade and community structure. Aust J Ecol 19:121–136CrossRefGoogle Scholar
  97. Polis GA, Holt RD (1992) Intraguild predation––the dynamics of complex trophic interactions. TREE 7:151–154Google Scholar
  98. Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intra-guild predation: potential competitors that eat each other. Annu Rev Entomol 20:297–330Google Scholar
  99. Powell W, Pell JK (2007) Biological control. In: Harrington R, van Emden H (eds) Aphids as crop pests. CABI International, pp 469–513, 717Google Scholar
  100. Powell W, Walters K, A’Hara S, Ashby J, Stevenson H, Northing P (2003) Using field margin diversification in agri-environment schemes to enhance aphid natural enemies. In: Rossing WAH, Poehling HM, Burgio G (eds) Landscape management for functional biodiversity. IOBC/WPRS Bulletin, 26/4, pp 123–128Google Scholar
  101. Powell W, A’Hara S, Harling R, Holland JM, Northing P, Thomas CFG, Walters KFA (2004) Managing biodiversity in field margins to enhance integrated pest control in arable crops (‘3D Farming’ Project). Project report No 356. HGCA, 226 ppGoogle Scholar
  102. Powell W, Pell JK, Nakashima Y, Baverstock J, Birkett M (2006) Functional biodiversity of aphid natural enemies: positive intra-guild interactions. In: Rossing WAH, Poehling HM, Burgio G (eds) Landscape management for functional biodiversity. IOBC/ WPRS Bulletin, 29(6), pp 101–104Google Scholar
  103. Roderick GK, Howarth FG (1999) Invasion genetics: natural colonisations, non-indigenous species and classical biological control. In: Yano E, Matsuo K, Shiyomi M, Andow D (eds) Biological invasions of pests and beneficial organisms. National Institute of Agro Environmental Sciences, Tsukuba, JapanGoogle Scholar
  104. Rosenheim JA (1998) Higher-order predators and the regulation of insect herbivore populations. Annu Rev Entomol 43:421–447PubMedCrossRefGoogle Scholar
  105. Rosenheim JA, Corbett SA (2003) Omnivory and the indeterminancy of predator function: can a knowledge of foraging behaviour help? Ecology 84:2438–2448CrossRefGoogle Scholar
  106. Rosenheim JA, Harmon JP (2006) The influence of intraguild predation on the suppression of a shared prey population: an empirical assessment. In: Brodeur J, Boivin G (eds) Trophic and guild interactions in biological control. Springer, Dordrecht, The Netherlands, pp 1–20CrossRefGoogle Scholar
  107. Rosenheim JA, Kaya HK, Ehler LE, Marois JJ, Jaffee BA (1995) Intraguild predation among biological control agents: theory and evidence. Biol Control 5:303–335CrossRefGoogle Scholar
  108. Rosenheim JA, Glik TE, Goeriz RE, Ramert B (2004a) Linking a predator’s foraging behaviour with its effects on herbivore population suppression. Ecology 85:3362–3372CrossRefGoogle Scholar
  109. Rosenheim JA, Limburg DD, Colfer RG, Fournier V, Hsu CL, Leonardo TE, Nelson EH (2004b) Herbivore population suppression by an intermediate predator, Phyoseiulus macropilis, is insensitive to the presence of an intraguild predator: an advantage of small body size? Oecologia 140:577–585PubMedCrossRefGoogle Scholar
  110. Roy HE, Pell JK (2000) Interactions between entomopathogenic fungi and other natural enemies: implications for biological control. Biocontrol Sci Tech 10:737–752CrossRefGoogle Scholar
  111. Roy HE, Pell JK, Clark SJ, Alderson PG (1998) Implications of predator foraging on aphid pathogen dynamics. J Invertebr Pathol 71:236–247PubMedCrossRefGoogle Scholar
  112. Roy HE, Pell JK, Alderson PG (2001) Targeted dispersal of the aphid pathogenic fungus Erynia neoaphidis by the aphid predator Coccinella septempunctata. Biocontrol Sci Tech 11:99–110CrossRefGoogle Scholar
  113. Roy HE, Brown P, Majerus MEN (2006) Harmonia axyridis: a successful biocontrol agent or an invasive threat? In: Eilenberg J, Hokkanen H (eds) An ecological and societal approach to biological control. Kluwer Academic Publishers, NetherlandsGoogle Scholar
  114. Roy HE, Brown PMJ, Rothery P, Ware RL, Majerus MEN (2007) Interactions between the fungal pathogen Beauveria bassiana and three species of coccinellid: Harmonia axyridis, Coccinella septempunctata and Adalia bipunctata. BioControl (this issue). doi: 10.1007/s10526-007-9122-0 Google Scholar
  115. Roy HE, Baverstock J, Ware RL, Clark SJ, Majerus MEN, Baverstock KE, Pell JK (2008). Intraguild predation of the aphid pathogenic fungus Pandora neoaphidis by the invasive coccinellid Harmonia axyridis. Ecol Entomol (In press)Google Scholar
  116. Sakuratani Y, Marsumoto Y, Oka M, Kubo T, Fuji A, Uotani M, Teraguchi T (2000) Life history of Adalia bipunctata (Coleoptera: Coccinellidae) in Japan. Eur J Entomol 97:555–558Google Scholar
  117. Sato S (2001) Ecology of ladybirds: factors influencing their survival. PhD Thesis, University of East Anglia, UKGoogle Scholar
  118. 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 6:21–24CrossRefGoogle Scholar
  119. Sato S, Dixon AFG, Hironori Y (2003) Effect of emigration on cannibalism and intraguild predation in aphidophagous ladybirds. Ecol Entomol 28:628–633CrossRefGoogle Scholar
  120. Sato S, Yasuda H, Evans EW (2005) Dropping behaviour of larvae of aphidophagous ladybirds and its effect on incidence of intraguild predation: interactions between the intraguild prey, Adalia bipunctata (L.) and Coccinella septempunctata (L.), and the intraguild predator, Harmonia axyridis Pallas. Ecol Entomol 30:220–224CrossRefGoogle Scholar
  121. Schellhorn NA, Andow D (2005) Response of coccinellids to their aphid prey at different spatial scales. Popul Ecol 47:281–288CrossRefGoogle Scholar
  122. Sengonca C, Frings B (1985) Interference and competitive behaviour of the aphid predators, Chrysoperla carnea and Coccinella septempunctata in the laboratory. Entomophaga 30:245–251CrossRefGoogle Scholar
  123. Sloggett JJ (1998) Interactions between Coccinellids (Coleoptera) and ants (Hymenoptera: Formicidae), and the evolution of Myrmecophily in Coccinella magnifica Redtenbacher. PhD thesis, University of CambridgeGoogle Scholar
  124. Sloggett JJ, Majerus MEN (2000) Aphid-mediated coexistence of ladybirds (Coleoptera: Coccinellidae) and the wood ant Formica rufa: seasonal effects, interspecific variability and the evolution of a coccinellid myrmecophile. Oikos 89:345–359CrossRefGoogle Scholar
  125. Sloggett JJ, Majerus MEN (2003) Adaptations of Coccinella magnifica, a myrmecophilous coccinellid to aggression by wood ants (Formica rufa group). II. Larval behaviour, and ladybird oviposition location. Eur J Entomol 100:337–344Google Scholar
  126. Sloggett JJ, Völkl W, Schulze W, von der Schulenberg JH, Majerus MEN (2002) The ant-associations and diet of the ladybird Coccinella magnifica (Coleoptera: Coccinellidae). Eur J Entomol 99:565–569Google Scholar
  127. Snyder WE, Evans EW (2006) Ecological effects of invasive arthropod generalist predators. Annu Rev Ecol Evol S 37:95–122CrossRefGoogle Scholar
  128. Snyder WE, Ives AR (2001) Generalist predators disrupt biological control by a specialist parasitoid. Ecology 82:705–716Google Scholar
  129. Snyder WE, Ives AR (2003) Interactions between specialist and generalist natural enemies: parasitoids, predators and pea aphid biocontrol. Ecology 84:91–107CrossRefGoogle Scholar
  130. Snyder WE, Ballard SN, Yang S, Clevenger GM, Miller TD, Ahn JJ, Hatten TD, Berryman AA (2004a) Complementary biocontrol of aphids by the ladybird beetle Harmonia axyridis and the parasitoid Aphelinus asychis on greenhouse roses. Biol Control 30:229–235CrossRefGoogle Scholar
  131. Snyder WE, Clevenger GM, Eigenbrode SD (2004b) Intraguild predation and successful invasion by introduced ladybird beetles. Oecologia 140:559–565PubMedCrossRefGoogle Scholar
  132. Stiling P, Cornelissen T (2005) What makes a successful biological control agent? A meta-analysis of biological control agent performance. Biol Control 34:236–246CrossRefGoogle Scholar
  133. Straub CS, Snyder WE (2006) Experimental approaches to understanding the relationship between predator diversity and conservation biological control. In: Brodeur J, Boivin G (eds) Trophic and guild interactions in biological control. Springer, Dordrecht, The Netherlands, pp 221–239CrossRefGoogle Scholar
  134. Straub CS, Finke DL, Snyder WE (2008) Are the conservation of natural enemy biodiversity and biological control compatible goals? Biol Control (In press)Google Scholar
  135. Takahashi K, Naito A (1984) Seasonal occurrence of aphids and their predators (Col. Coccinellidae) in alfalfa fields. Bulletin of the National Grassland Research Institute 29:62–66 [In Japanese with English summary]Google Scholar
  136. Takizawa T, Yasuda H, Agarwala BK (2000) Effect of three species of predatory ladybirds on oviposition of aphid parasitoids. Entomol Sci 3:465–469Google Scholar
  137. Taylor AJ, Müller CB, Godfray HCJ (1998) Effect of aphid predators on oviposition behaviour of aphid parasitoids. J Insect Behav 11:297–302CrossRefGoogle Scholar
  138. Tedders WL, Schaefer PW (1994) Release and establishment of Harmonia axyridis (Coleoptera: Coccinellidae) in the south-eastern United States. Entomol News 105:228–243Google Scholar
  139. Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity––ecosystem service management. Ecol Lett 8:857–874CrossRefGoogle Scholar
  140. Völkl W (1995) Behavioural and morphological adaptations of the coccinellid, Platynaspis luteorubra for exploiting ant-attending resources (Coleoptera: Coccinellidae). J Insect Behav 8:653–670CrossRefGoogle Scholar
  141. Völkl W, Mackauer M, Pell JK, Brodeur J (2007) Predators, parasitoids and fungal pathogens. In: Harrington R, van Emden H (eds) Aphids as crop pests. CABI International, pp 187–233Google Scholar
  142. Ware RL, Majerus MEN (2007) Intraguild predation of immature stages of British and Japanese coccinellids by the invasive ladybird Harmonia axyridis. BioControl (this issue). doi: 10.1007/s10526-007-9135-8 Google Scholar
  143. Ware RL, Majerus MEN, Roy HE, Symington F (2005) The harlequin ladybird arrives in Britain: a threat to our native species? Bull Amat Ent Soc 64:175–186Google Scholar
  144. Ware RL, Ramon-Portugal F, Magro A, Ducamp C, Hemptinne JL, Majerus, MEN (2007) Chemical protection of Calvia quatuordecimguttata eggs against intraguild predation by the invasive ladybird Harmonia axyridis. BioControl (this issue). doi: 10.1007/s10526-007-9129-6 Google Scholar
  145. Ware RL, Evans N, Malpas L, Michie LJ, O’Farrell K, Majerus MEN (2008) Intraguild predation by the invasive ladybird Harmonia axyridis: 1. British and Japanese coccinellid eggs. Neobiota (In press)Google Scholar
  146. Way MJ (1963) Mutualism between ants and honey-dew producing Homoptera. Annu Rev Entomol 8:307–344CrossRefGoogle Scholar
  147. Wells ML, McPherson RM (1999) Population dynamics of three coccinellids in flue-cured tobacco and functional response of Hippodamia convergens (Coleoptera: Coccinellidae) feeding on tobacco aphids (Homoptera: Aphididae). Environ Entomol 28:768–773Google Scholar
  148. Wells ML, McPherson RM, Ruberson JR, Herzog GA (2001) Coccinellids in cotton: population response to pesticide application and feeding response to cotton aphids (Homoptera: Aphididae). Environ Entomol 30:785–793Google Scholar
  149. Wheeler AG, Hayes JT, Stephens JL (1968) Insect predators of mummified aphids. Can Entomol 100:221–222CrossRefGoogle Scholar
  150. Wilby A, Thomas MB (2002a) Natural enemy diversity and pest control: patterns of pest emergence with agricultural intensification. Ecol Lett 5:353–360CrossRefGoogle Scholar
  151. Wilby A, Thomas MB (2002b) Are the ecological concepts of assembly and function of biodiversity useful frameworks for understanding natural pest control? Agr Forest Entomol 4:237–243CrossRefGoogle Scholar
  152. Yasuda H, Ohnuma N (1999) Effect of cannibalism and predation on the larval performance of two ladybird beetles. Ent Exp Appl 93:63–67CrossRefGoogle Scholar
  153. Yasuda H, Shinya Y (1997) Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Entomophaga 42:153–163CrossRefGoogle Scholar
  154. Yasuda H, Kikuchi T, Kindlmann P, Sato S (2001) Relationships between attacks and escape rates, cannibalism, and intraguild predation in larvae of two predatory ladybirds. J Ins Behav 14:373–384CrossRefGoogle Scholar
  155. Yasuda H, Evans EW, Kajita Y, Urakawa K, Takizawa T (2004) Asymmetric larval interactions between introduced and indigenous ladybirds in North America. Oecologia 141:722–731PubMedCrossRefGoogle Scholar
  156. Yeo H (2000) Mycoinsecticides for aphid management: a biorational approach. PhD Thesis, University of Nottingham 308 ppGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2007

Authors and Affiliations

  • Judith K. Pell
    • 1
    Email author
  • Jason Baverstock
    • 1
  • Helen E. Roy
    • 2
  • Remy L. Ware
    • 3
  • Michael E. N. Majerus
    • 3
  1. 1.Department of Plant and Invertebrate EcologyRothamsted ResearchHertfordshireUK
  2. 2.NERC Centre for Ecology and HydrologyHuntingdonUK
  3. 3.Department of GeneticsUniversity of CambridgeCambridgeUK

Personalised recommendations