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BioControl

, Volume 62, Issue 3, pp 331–340 | Cite as

Reaping benefits from an invasive species: role of Harmonia axyridis in natural biological control of Aphis glycines in North America

  • Robert L. KochEmail author
  • Alejandro C. Costamagna
Review

Abstract

Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) is an invasive species present in numerous agroecosystems in North America. Despite adverse impacts as a threat to native biodiversity, a nuisance household invader and a pest in fruit production, H. axyridis also plays a beneficial role as a major component of assemblages of generalist predators in several agricultural crops. Here, we review the role of H. axyridis as a natural enemy of Aphis glycines Matsumura (Hemiptera: Aphididae), an invasive pest of soybean, Glycine max (L.) Merrill (Fabales: Fabaceae), in North America. Harmonia axyridis is often the most abundant predator species attacking A. glycines in soybean agroecosystems. This predator has the potential to both prevent and suppress A. glycines outbreaks. Further studies are needed to fully understand and utilize the potential of H. axyridis as a natural enemy in the management of A. glycines and other agricultural pests in agroecosystems worldwide.

Keywords

Aphididae Coccinellidae Coleoptera Hemiptera Integrated pest management Invasive species Soybean 

Notes

Acknowledgments

We thank Christopher Philips, Jordan Bannerman, Anh Tran, Walter Rich, Sandra Nogueira Koch, and two anonymous reviewers for providing reviews of an earlier version of this paper. This paper originated from a presentation by R.L.K. at the 2nd International Congress on Biological Invasions in Qingdao, China from 23 to 27 October 2013. The work was supported by the Minnesota Soybean Research and Promotion Council and the Natural Sciences and Engineering Research Council of Canada (Discovery Grant 1503).

References

  1. Bahlai CA, Welsman JA, Macleod EC, Schaafsma AW, Hallett RH, Sears MK (2008) Role of visual and olfactory cues from agricultural hedgerows in the orientation behavior of multicolored Asian lady beetle (Coleoptera: coccinellidae). Environ Entomol 37:973–979CrossRefPubMedGoogle Scholar
  2. Bahlai CA, Xue Y, McCreary CM, Schaafsma AW, Hallett RH (2010) Choosing organic pesticides over synthetic pesticides may not effectively mitigate environmental risk in soybeans. PLoS ONE 5(6):e11250CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bahlai CA, Colunga-Garcia M, Gage SH, Landis DA (2013) Long-term functional dynamics of an aphidophagous coccinellid community remain unchanged despite repeated invasions. PLoS ONE 8(12):e83407CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bahlai CA, van der Werf W, O’Neal M, Hemerik L, Landis DA (2015) Shifts in dynamic regime of an invasive lady beetle are linked to the invasion and insecticidal management of its prey. Ecol Appl 25:1807–1818CrossRefPubMedGoogle Scholar
  5. Bannerman JA, Costamagna AC, McCornack BP, Ragsdale DW (2015) Comparison of relative bias, precision and efficiency of sampling methods for natural enemies of soybean aphid. J Econ Entomol 108:1381–1397CrossRefPubMedGoogle Scholar
  6. Brosius TR, Higley LG, Hunt TE (2007) Population dynamics of soybean aphid and biotic mortality at the edge of its range. J Econ Entomol 100:1268–1275CrossRefPubMedGoogle Scholar
  7. Brown PMJ, Thomas CE, Lombaert E, Jeffries DL, Estoup A, Handley LJL (2011) The global spread of Harmonia axyridis (Coleoptera: coccinellidae): distribution, dispersal and routes of invasion. BioControl 56:623–641CrossRefGoogle Scholar
  8. Chacón JM, Landis DA, Heimpel GE (2008) Potential for biotic interference of a classical biological control agent of the soybean aphid. Biol Control 46:216–225CrossRefGoogle Scholar
  9. Chapin JB, Brou VA (1991) Harmonia axyridis (Pallas), the third species of the genus to be found in the United States (Coleoptera: Coccinellidae). Proc Entomol Soc Wash 93:630–635Google Scholar
  10. Conway HE, Steinkraus DC, Ruberson JR, Kring TJ (2006) Experimental treatment threshold for the cotton aphid (Homoptera: Aphididae) using natural enemies in Arkansas cotton. J Entomol Sci 41:361–373Google Scholar
  11. Costamagna AC, Landis DA (2006) Predators exert top-down control of soybean aphid across a gradient of agricultural management systems. Ecol Appl 16:1619–1628CrossRefPubMedGoogle Scholar
  12. Costamagna AC, Landis DA (2007) Quantifying predation on soybean aphid through direct field observations. Biol Control 42:16–24CrossRefGoogle Scholar
  13. Costamagna AC, Landis DA (2011) Lack of strong refuges allows top-down control of soybean aphid by generalist natural enemies. Biol Control 57:184–192CrossRefGoogle Scholar
  14. Costamagna AC, Landis DA, Brewer MJ (2008) The role of natural enemy guilds in Aphis glycines suppression. Biol Control 45:368–379CrossRefGoogle Scholar
  15. Costamagna AC, Venables WN, Schellhorn NA (2015) Landscape-scale pest suppression is mediated by timing of predator arrival. Ecol Appl 25:1114–1130CrossRefPubMedGoogle Scholar
  16. Cox R, O’Neal M, Hessel R, Schulte LA, Helmers M (2014) The impact of prairie strips on aphidophagous predator abundance and soybean aphid predation in agricultural catchments. Environ Entomol 43:1185–1197CrossRefPubMedGoogle Scholar
  17. Desneux N, O’Neil RJ, Yoo HJS (2006) Suppression of population growth of the soybean aphid, Aphis glycines Matsumura, by predators: the identification of a key predator and the effects of prey dispersion, predator abundance, and temperature. Environ Entomol 35:1342–1349CrossRefGoogle Scholar
  18. Donaldson JR, Myers SW, Gratton C (2007) Density-dependent responses of soybean aphid (Aphis glycines Matsumura) populations to generalist predators in mid to late season soybean fields. Biol Control 43:111–118CrossRefGoogle Scholar
  19. Fox TB (2002) Biological control of the soybean aphid, Aphis glycines Matsumura (Homoptera: Aphididae). M.S. thesis, Michigan State University, East Lansing, USAGoogle Scholar
  20. Fox TB, Landis DA, Cardoso FF, Difonzo CD (2004) Predators suppress Aphis glycines Matsumura population growth in soybean. Environ Entomol 33:608–618CrossRefGoogle Scholar
  21. Fox TB, Landis DA, Cardoso FF, Difonzo CD (2005) Impact of predation on establishment of the soybean aphid, Aphis glycines in soybean, Glycine max. BioControl 50:545–563CrossRefGoogle Scholar
  22. Gagnon A-È, Heimpel GE, Brodeur J (2011) The ubiquity of intraguild predation among predatory arthropods. PLoS ONE 6(11):e28061CrossRefPubMedPubMedCentralGoogle Scholar
  23. 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
  24. Gardiner M, Landis D, Gratton C, DiFonzo C, O’Neal M, Chacon J, Wayo M, Schmidt N, Mueller E, Heimpel G (2009a) Landscape diversity enhances biological control of an introduced crop pest in the north-central USA. Ecol Appl 19:143–154CrossRefPubMedGoogle Scholar
  25. Gardiner M, Landis D, Gratton C, Schmidt N, O’Neal M, Mueller E, Chacon J, Heimpel G, DiFonzo C (2009b) Landscape composition influences patterns of native and exotic lady beetle abundance. Divers Distrib 15:554–564CrossRefGoogle Scholar
  26. Hallet RH, Bahlai CA, Xue Y, Schaarsma AW (2014) Incorporating natural enemy units into a dynamic action threshold for the soybean aphid, Aphis glycines (Homoptera: Aphididae). Pest Manag Sci 70:879–888CrossRefGoogle Scholar
  27. Harwood JD, Desneux N, Yoo HJS, Rowley DL, Greenstone MH, Obrycki JJ (2007) Tracking the role of alternative prey in soybean aphid predation by Orius insidiosus: a molecular approach. Mol Ecol 16:4390–4400CrossRefPubMedGoogle Scholar
  28. Heimpel GE, Frelich LE, Landis DA, Hopper KR, Hoelmer KA, Sezen Z, Asplen MK, Wu K (2010) European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biol Invasions 12:2913–2931CrossRefGoogle Scholar
  29. Heimpel GE, Yang Y, Hill J, Ragsdale DW (2013) Environmental consequences of invasive species: greenhouse gas emissions of insecticide use and the role of biological control in reducing emissions. PLoS ONE 8(8):e72293CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hesler LS (2014) Inventory and assessment of foliar natural enemies of the soybean aphid (Hemiptera: Aphididae) in South Dakota. Environ Entomol 43:577–588CrossRefPubMedGoogle Scholar
  31. Hesler LS, Chiozza MV, O’Neal ME, MacIntosh GC, Tilmon KJ, Chandrasena DI, Tinsely NA, Cianzio SR, Costamagna AC, Cullen EM, DiFonzo CD, Potter BD, Ragsdale DW, Steffey K, Koehler KJ (2013) Performance and prospects of Rag genes for management of soybean aphid. Entomol Exp Appl 147:201–216CrossRefGoogle Scholar
  32. Hodgson EW, McCornack BP, Tilmon K, Knodel JJ (2012) Management recommendations for soybean aphid (Hemiptera: Aphididae) in the United States. J Integr Pest Mngmt 3:E1–E10CrossRefGoogle Scholar
  33. Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398CrossRefGoogle Scholar
  34. Hurley T, Mitchell PD (2014) The value of neonicotinoids in North American agriculture: value of insect pest management to US and Canadian corn, soybean, and canola farmers. AgInfomatics, LLC. http://growingmatters.org/wp-content/themes/growingmatters/pdf/FINAL_AgInfomatics_ValueReport_2014_R1.pdf
  35. Koch RL (2003) The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. J Insect Sci 3:32PubMedPubMedCentralGoogle Scholar
  36. Koch RL, Galvan TL (2008) Bad side of a good beetle: the North American experience with Harmonia axyridis. BioControl 53:23–35CrossRefGoogle Scholar
  37. Koch RL, Hutchison WD (2003) Phenology and blacklight trapping of the multicolored Asian lady beetle (Coleoptera: Coccinellidae) in a Minnesota agricultural landscape. J Entomol Sci 38:477–480Google Scholar
  38. Koch RL, Burkness EC, Hutchison WD (2006a) Spatial distribution and fixed-precision sampling plans for the ladybird Harmonia axyridis in sweet corn. BioControl 51:741–751CrossRefGoogle Scholar
  39. Koch RL, Venette RC, Hutchison WD (2006b) Invasions by Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in the Western Hemisphere: implications for South America. Neotrop Entomol 35:421–434CrossRefPubMedGoogle Scholar
  40. Koch RL, Porter PM, Harbur MM, Abrahamson MD, Wyckhuys KAG, Ragsdale DW, Buckman K, Sezen Z, Heimpel GE (2012) Response of soybean insects to an autumn-seeded rye cover crop. Environ Entomol 41:750–760CrossRefGoogle Scholar
  41. Koch RL, Sezen Z, Porter PM, Ragsdale DW, Wyckhuys KA, Heimpel GE (2015) On-farm evaluation of a fall-seeded rye cover crop for suppression of soybean aphid (Hemiptera: Aphididae) on soybean. Agric Forest Entomol 17:239–246CrossRefGoogle Scholar
  42. Kraiss H, Cullen EM (2008a) Efficacy and nontarget effects of reduced-risk insecticides on Aphis glycines (Hemiptera: Aphididae) and its biological control agent Harmonia axyridis (Coleoptera: Coccinellidae). J Econ Entomol 101:391–398CrossRefPubMedGoogle Scholar
  43. Kraiss H, Cullen EM (2008b) Insect growth regulator effects of azadirachtin and neem oil on survivorship, development and fecundity of Aphis glycines (Homoptera: Aphididae) and its predator, Harmonia axyridis (Coleoptera: Coccinellidae). Pest Manag Sci 64:660–668CrossRefPubMedGoogle Scholar
  44. Lamana ML, Miller JC (1996) Field observations on Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in Oregon. Biol Control 6:232–237CrossRefGoogle Scholar
  45. Landis DA, Gardiner MM, van der Werf W, Swinton SM (2008) Increasing corn for biofuel production reduces biocontrol services in agricultural landscapes. Proc Natl Acad Sci USA 105:20552–20557CrossRefPubMedPubMedCentralGoogle Scholar
  46. Liu J, Xu W, Wang Q, Zhao K (2012) Insect predators in northeast China and their impacts on Aphis glycines. Can Entomol 144:779–789CrossRefGoogle Scholar
  47. Lombaert E, Guillemaud T, Lundgren J, Koch R, Facon B, Grez A, Loomans A, Malausa T, Nedved O, Rhule E, Staverlokk A, Steenberg T, Estoup A (2014) Complementarity of statistical treatments to reconstruct worldwide routes of invasion: the case of the Asian ladybird, Harmonia axyridis. Mol Ecol 23:1579–1597CrossRefGoogle Scholar
  48. Lucas E, Vincent C, Labrie G, Chouinard G, Fournier F, Pelletier F, Bostanian NJ, Coderre D, Mignault MP, Lafontaine P (2007) The multicolored Asian ladybeetle Harmonia axyridis (Coleoptera: Coccinellidae) in Quebec agroecosystems ten years after its arrival. Eur J Entomol 104:737–743CrossRefGoogle Scholar
  49. Lundgren JG, Hesler LS, Tilmon K, Dashiell K, Scott R (2009) Direct effects of soybean varietal selection and Aphis glycines-resistant soybeans on natural enemies. Arth-Plant Int 3:9–16CrossRefGoogle Scholar
  50. Meihls LN, Clark TL, Bailey WC, Ellersieck MR (2010) Population growth of soybean aphid, Aphis glycines, under varying levels of predator exclusion. J Insect Sci 10:144CrossRefPubMedPubMedCentralGoogle Scholar
  51. Mignault MP, Roy M, Brodeur J (2006) Soybean aphid predators in Quebec and the suitability of Aphis glycines as prey for three Coccinellidae. BioControl 51:89–106CrossRefGoogle Scholar
  52. Murdoch WW, Chesson J, Chesson PL (1985) Biological control in theory and practice. Am Nat 125:344–366CrossRefGoogle Scholar
  53. National Agricultural Statistics Service [NASA] (2015) United States Department of Agriculture http://www.nass.usda.gov/index.asp Acessed 15 June 2016
  54. Nielsen C, Hajek AE (2005) Control of invasive soybean aphid, Aphis glycines (Hemiptera: Aphididae), populations by existing natural enemies in New York State, with emphasis on entomopathogenic fungi. Environ Entomol 34:1036–1047CrossRefGoogle Scholar
  55. Noma T, Gratton C, Colunca-Garcia M, Brewer MJ, Mueller EE, Wyckhuys KAG, Heimpel GE, O’Neal ME (2010) Relationship of soybean aphid (Hemiptera: Aphididae) to soybean plant nutrients, landscape structure, and natural enemies. Environ Entomol 39:31–41CrossRefPubMedGoogle Scholar
  56. Obata S (1986) Determination of hibernation site in the ladybird beetle, Harmonia axyridis Pallas (Coleoptera, Coccinellidae). Kontyu 54:218–223Google Scholar
  57. Obrycki JJ, Kring TJ (1998) Predaceous Coccinellidae in biological control. Annu Rev Entomol 43:295–321CrossRefPubMedGoogle Scholar
  58. Obrycki JJ, Harwood JD, Kring TJ, O’Neil RJ (2009) Aphidophagy by Coccinellidae: application of biological control in agroecosystems. Biol Control 51:244–254CrossRefGoogle Scholar
  59. Ohnesorg WJ, Johnson KD, O’Neal ME (2009) Impact of reduced-risk insecticides on soybean aphid and associated natural enemies. J Econ Entomol 102:1816–1826CrossRefPubMedGoogle Scholar
  60. Osawa N (2000) Population field studies on the aphidophagous ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae): resource tracking and population characteristics. Popul Ecol 42:115–127CrossRefGoogle Scholar
  61. Pedigo LP, Rice ME (2014) Entomology and pest management, 6th edn. Waveland, Long GoveGoogle Scholar
  62. Pell JK, Baverstock J, Roy HE, Ware RL, Majerus ME (2008) Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. BioControl 53:147–168CrossRefGoogle Scholar
  63. Pezzini D, Koch RL (2015) Compatibility of flonicamid and a formulated mixture of pyrethrins and azadirachtin with predators for soybean aphid (Hemiptera: Aphididae) management. Biocontrol Sci Technol 25:1024–1035CrossRefGoogle Scholar
  64. Ragsdale DW, McCornack BP, Venette RC, Potter BD, MacRae IV, Hodgson EW, O’Neal ME, Difonzo CD, Hunt TE, Glogoza PA, Cullen EM (2007) Economic threshold for soybean aphid (Hemiptera: Aphididae). J Econ Entomol 100:1258–1267CrossRefPubMedGoogle Scholar
  65. Ragsdale DW, Landis DA, Brodeur J, Heimpel GE, Desneux N (2011) Ecology and management of the soybean aphid in North America. Annu Rev Entomol 56:375–399CrossRefPubMedGoogle Scholar
  66. Rhainds M, Roy M, Daigle G, Brodeur J (2007) Toward management guidelines for the soybean aphid in Québec. I. Feeding damage in relationship to seasonality of infestation and incidence of native predators. Can Entomol 139:728–741CrossRefGoogle Scholar
  67. Roy H, Brown P, Majerus M (2006) Harmonia axyridis: a successful biocontrol agent or an invasive threat? In: Eilenberg J, Hokkanen HMT (eds) An ecological and societal approach to biological control. Springer, Dodretch, pp 295–309CrossRefGoogle Scholar
  68. Rutledge CE, O’Neil RJ, Fox TB, Landis DA (2004) Soybean aphid predators and their use in integrated pest management. Ann Entomol Soc Am 97:240–248CrossRefGoogle Scholar
  69. Schmidt NP, O’Neal ME, Dixon PM (2008) Aphidophagous predators in Iowa soybean: a community comparison across multiple years and sampling methods. Ann Entomol Soc Am 101:341–350CrossRefGoogle Scholar
  70. Schmidt NP, O’Neal ME, Moore LAS (2011) Effects of grassland habitat and plant nutrients on soybean aphid and natural enemy populations. Environ Entomol 40:260–272CrossRefGoogle Scholar
  71. Seagraves MP, Kajita Y, Weber DC, Obrycki JJ, Lundgren JG (2011) Sugar feeding by coccinellids under field conditions: the effects of sugar sprays in soybean. BioControl 56:305–314CrossRefGoogle Scholar
  72. Smith CM (2005) Plant resistance to arthropods: molecular and conventional approaches. Springer, DordrechtCrossRefGoogle Scholar
  73. Snyder WE, Evans EW (2006) Ecological effects of invasive arthropod generalist predators. Ann Rev Ecol Syst 37:95–122CrossRefGoogle Scholar
  74. Song F, Swinton SM, DiFonzo C, O’Neal M, Ragsdale DW (2006) Profitability analysis of soybean aphid control treatments in three north-central states. Michigan State University Department of Agricultural Economics. http://ageconsearch.umn.edu/bitstream/11489/1/sp06-24.pdf Cited 15 June 2016
  75. Statistics Canada (2015) Statistics Canada. http://www.statcan.gc.ca/start-debut-eng.html Accessed 15 June 2016
  76. The White House (1999) Executive order 13112 of February 3, 1999: invasive species. Fed Reg 64:6183–6186Google Scholar
  77. Varenhorst AJ, O’Neal ME (2012) The response of natural enemies to selective insecticides applied to soybean. Environ Entomol 41:1565–1574CrossRefPubMedGoogle Scholar
  78. Venette RC, Ragsdale DW (2004) Assessing the invasion by soybean aphid (Homoptera: Aphididae): where will it end? Ann Entomol Soc Am 97:219–226CrossRefGoogle Scholar
  79. Welsman JA, Bahlai C, Sears M, Schaafsma A (2007) Decline in soybean aphid (Homoptera: Aphididae) egg populations from autumn to spring on the primary host Rhamnus cathartica L. Environ Entomol 36:541–548CrossRefPubMedGoogle Scholar
  80. Woltz JM, Landis DA (2013) Coccinellid immigration to infested host patches influences suppression of Aphis glycines in soybean. Biol Control 64:330–337CrossRefGoogle Scholar
  81. Woltz JM, Isaacs R, Landis DA (2012) Landscape structure and habitat management differentially influence insect natural enemies in an agricultural landscape. Agric Ecosyst Env 152:40–49CrossRefGoogle Scholar
  82. Wu Z, Schenk-Hamlin D, Zhan W, Ragsdale WD, Heimpel EG (2004) The soybean aphid in China: a historical review. Ann Entomol Soc Am 97:209–218CrossRefGoogle Scholar
  83. Xue Y, Bahlai CA, Frewin A, Sears MK, Schaafsma AV, Hallett RH (2009) Predation by Coccinella septempunctata and Harmonia axyridis (Coleoptera: Coccinellidae) on Aphis glycines (Homoptera: Aphididae). Environ Entomol 38:708–714CrossRefPubMedGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2016

Authors and Affiliations

  1. 1.Department of EntomologyUniversity of MinnesotaSaint PaulUSA
  2. 2.Department of EntomologyUniversity of ManitobaWinnipegCanada

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