Parasitoid communities and interactions with Diuraphis noxia in Australian cereal production systems

Abstract

New information is presented on previously introduced aphid parasitoids using the newly arrived Russian wheat aphid (RWA), Diuraphis noxia Kurdjumov 1913 (Hemiptera: Aphididae) in South Australia including species diversity and relative abundance, population dynamics and regional differences in communities. In total, eight species of primary braconids (Hymenoptera) were identified from D. noxia: Aphidius colemani Viereck, 1912 A. platensis Brèthes 1913, A. ervi Haliday 1834 (Hymenoptera: Braconidae), A. rhopalosiphi De Stefani Perez, 1902, A. salicis Haliday, 1834, A. smithi Sharma and Subba Rao, 1959, Diaeretiella rapae (McIntosh, 1855) and Lysiphlebus testaceipes (Cresson, 1880). The predominant parasitoids of D. noxia were D. rapae, A. colemani and A. platensis which was consistent across regions. This study indicates the pre-emptive importation of biological control agents (generalist parasitoid wasps) contributed to limiting an invasive pest. Data presented provides a baseline for further research on parasitoid species to reduce D. noxia, a new pest species in Australian cereal ecosystems.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Aalbersberg YK, van der Westhuizen MC, Hewitt PH (1988) Natural enemies and their impact on Diuraphis noxia (Mordvilko) (Hemiptera: Aphididae) populations. Bull Entomol Res 78:111–120

    Google Scholar 

  2. Aeschlimann JP, Hughes RD (1992) Collecting Aphelinus spp. (Hymenoptera: Aphelinidae) in southwestern CIS for "pre-emptive" biological control of Diuraphis noxia (Homoptera: Aphididae) in Australia. J Hymenopt Res 1:103–105

    Google Scholar 

  3. Avila GA, Davidson M, van Helden M, Fagan L (2019) The potential distribution of the Russian wheat aphid (Diuraphis noxia): an updated distribution model including irrigation improves model fit for predicting potential spread. Bull Entomol Res 109:90–101

    CAS  PubMed  Google Scholar 

  4. Baker DA, Loxdale HD, Edwards OR (2003) Genetic variation and founder effects in the parasitoid wasp, Diaeretiella rapae (M’intosh) (Hymenoptera: Braconidae: Aphidiidae), affecting its potential as a biological control agent. Mol Ecol 12:3303–3311

    CAS  PubMed  Google Scholar 

  5. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300

    Google Scholar 

  6. Bodlah I, Naeem M, Ul Mohsin A (2012) Distribution, hosts and biology of Diaeretiella rapae (M’Intosh) (Hymenoptera: Braconidae: Aphidiinae) in Punjab, Pakistan. Pak J Zool 44:1307–1315

    Google Scholar 

  7. Botha AM, Swanevelder ZH, Lapitan NL (2010) Transcript profiling of wheat genes expressed during feeding by two different biotypes of Diuraphis noxia. Environ Entomol 39:1206–1231

    CAS  PubMed  Google Scholar 

  8. Brewer MJ, Mornhinweg DW, Huzurbazar S (1999) Compatibility of insect management strategies: Diuraphis noxia abundance on susceptible and resistant barley in the presence of parasitoids. BioControl 43:479–491

    Google Scholar 

  9. Brewer MJ, Noma T, Elliott NC (2005) Hymenopteran parasitoids and dipteran predators of the invasive aphid Diuraphis noxia after enemy introductions: temporal variation and implication for future aphid invasions. Biol Control 33:315–323

    Google Scholar 

  10. Brewer MJ, Nelson DJ, Ahern RG, Donahue JD, Prokrym DR (2009) Recovery and range expansion of parasitoids (Hymenoptera: Aphelinidae and Braconidae) released for biological control of Diuraphis noxia (Homoptera: Aphididae) in Wyoming. Environ Entomol 30:578–588

    CAS  Google Scholar 

  11. Brodeur J, McNeil JN (1989) Biotic and abiotic factors involved in diapause induction of the parasitoid, Aphidius nigripes (Hymenoptera: Aphidiidae). J Insect Physiol 35:969–974

    Google Scholar 

  12. Calvo-Agudo M, González-Cabrera J, Picó Y, Calatayud-Vernich P, Urbaneja A, Dicke M, Tena A (2019) Neonicotinoids in excretion product of phloem-feeding insects kill beneficial insects. Proc Natl Acad Sci USA 116:16817–16822

    CAS  PubMed  Google Scholar 

  13. Carver M, Franzmann B (2001) Lysiphlebus Förster (Hymenoptera: Braconidae: Aphidiinae) in Australia. Aust J Agric Res 40:198–201

    Google Scholar 

  14. Carver M, Starý P (1974) A preliminary review of the Aphidiidae (Hymenoptera: Ichneumonoidea) of Australia and New Zealand. Aust J Entomol 13:235–240

    Google Scholar 

  15. Chen K, Hopper KR (1997) Diuraphis noxia (Homoptera: Aphididae) population dynamics and impact of natural enemies in the Montpellier region of southern France. Environ Entomol 26:866–875

    Google Scholar 

  16. Dean GJ (1974) Effects of parasites and predators on the cereal aphids Metopolophium dirhodum (Wlk.) and Macrosiphum avenae (f.) (Hemiptera: Aphididae). Bull Entomol Res 63:411–422

    Google Scholar 

  17. Dunn O (1964) Multiple comparisons using rank sums. Technometrics 6:241–252

    Google Scholar 

  18. Elliott NC, Mirik M, Yang Z, Dvorak T, Rao M, Thia M, Vasiie W, Phoofolo M, Giles KL, Royer T (2007) Airborne multi-spectral remote sensing of Russian wheat aphid injury to wheat. Southwest Entomol 32:213–219

    Google Scholar 

  19. Gilchrist LI, Rodriguez R, Burnett PA (1984) The extent of freestate streak and Diuraphis noxia in Mexico. In: Barley yellow dwarf, proceedings of workshop. International maize and wheat improvement centre (CIMMYT), Mexico City, pp 157–163

  20. Hǻgvar EB, Hofsvang T (1991) Aphid parasitoids (Hymenoptera: Aphidiidae): biology, host selection and use in biological control. Biocontrol News Inform 12:13–42

    Google Scholar 

  21. Hatting JL, Poprawski TJ, Miller RM (2000) Prevalences of fungal pathogens and other natural enemies of cereal aphids (Homoptera: Aphididae) in wheat under dryland and irrigated conditions in South Africa. BioControl 45:179–199

    Google Scholar 

  22. Havelka J, Tomanović Ž, Kavallieratos NG, Rakhshani E, Pons X, Petrović A, Pike KS, Starý P (2012) Review and key to the world parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Aphis ruborum (Hemiptera: Aphididae) and its role as a host reservoir. Ann Entomol Soc Am 105:386–394

    Google Scholar 

  23. Hughes RD, Maywald GF (1990) Forecasting the favourableness of the Australian environment for the Russian wheat aphid, Diuraphis noxia (Homoptera: Aphididae), and its potential impact on Australian wheat yields. Bull Entomol Res 80:165–175

    Google Scholar 

  24. Hughes RD, Hughes MA, Aeschlimann JP, Woolcock LT, Carver M (1994) An attempt to anticipate biological control of Diuraphis noxia (Homoptera: Aphididae). Entomophaga 39:211–223

    Google Scholar 

  25. Kavallieratos NG, Tomanović Ž, Starý P, Athanassiou CG, Sarlis GP, Petrović O, Niketić M, Veroniki MA (2004) A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of southeastern Europe and their aphid-plant associations. Appl Entomol Zool 39:527–563

    Google Scholar 

  26. Kavallieratos NG, Tomanović Ž, Athanassiou CG, Starý P, Žikić V, Sarlis GP, Fasseas C (2005) Aphid parasitoids infesting cotton, citrus, tobacco, and cereal crops in southeastern Europe: aphid–plant associations and keys. Can Entomol 137:516–531

    Google Scholar 

  27. Kindler SD, Springer TL (1989) Alternate hosts of Russian wheat aphid (Homoptera: Aphididae). J Econ Entomol 82:1358–1362

    Google Scholar 

  28. Kingwell R, Rice A, Pratley J, Mayfield A, van Rees H (1980s) Farms and farmers—conservation agriculture amid a changing farm sector: key changes in Australian agriculture since the 1980s. In: Pratley J, Kirkegaard J (eds) Australian agriculture in 2020: from conservation to automation. Agronomy Australia and Charles Sturt University, Wagga Wagga, pp 33–45

    Google Scholar 

  29. Krespi L, Dedryver CA, Rabasse JM, Nénon JP (1994) A morphometric comparison of aphid mummies containing diapausing vs. non-diapausing larvae of Aphidius rhopalosiphi (Hymenoptera: Braconidae, Aphidiinae). Bull Entomol Res 84:45–50

    Google Scholar 

  30. Kruskal WH, Wallis WA (1952) Use of ranks in one-criterion variance analysis. J Am Stat Assoc 47:583–621

    Google Scholar 

  31. Martinez AP (2019) pairwiseAdonis: pairwise multilevel comparison using adonis. R package version 0.3. https://github.com/pmartinezarbizu/pairwiseadonis

  32. Miksanek JR, Heimpel GE (2019) A matrix model describing host-parasitoid population dynamics: the case of Aphelinus certus and soybean aphid. PLoS ONE 14(6):e0218217

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Milne WM (1995) Use of trap plants as a means of measuring the activity of cereal aphid parasitoids in the field. Agric Ecosyst Environ 52:31–34

    Google Scholar 

  34. Mohamed AH, Lester PJ, Holtzer TO (2000) Abundance and effects of predators and parasitoids on the Russian wheat aphid (Homoptera: Aphididae) under organic farming conditions in Colorado. Environ Entomol 29:360–368

    Google Scholar 

  35. Nash M, Severtson D, Macfadyen S (2019) New approaches to manage invertebrate pests in conservation agriculture systems—uncoupling intensification. In: Pratley J, Kirkegaard J (eds) Australian agriculture in 2020: from conservation to automation. Agronomy Australia and Charles Sturt University, Wagga Wagga, pp 189–202

    Google Scholar 

  36. Ogle DH, Wheeler P, Dinno A (2019) FSA: fisheries stock analysis. R package version 0.8, 17, 636. https://github.com/droglenc/fsa

  37. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Szoecs E, Wagner H (2019) Vegan: community ecology package. R package version 1.17-4. https://cran.r-project.org/package=vegan

  38. Ortego J, Delfino MA (1994) Diuraphis noxia (Mordvilko) (Homoptera: Aphididae) in Argentina. Rev Fac Agron La Plata 70:51–55

    Google Scholar 

  39. Pike KS, Starý P, Miller T, Allison D, Boydston L, Graf G, Gillespie R (1997) Small-grain aphid parasitoids (Hymenoptera: Aphelinidae and Aphidiidae) of Washington: distribution, relative abundance, seasonal occurrence, and key to known North American species. Environ Entomol 26:1299–1311

    Google Scholar 

  40. Polgár L, Mackauer M, Völkl W (1991) Diapause induction in two species of aphid parasitoids: the influence of aphid morph. J Insect Physiol 37:699–702

    Google Scholar 

  41. Prinsloo GJ (1998) Aphelinus hordei (Kurdjumov) (Hymenoptera: Aphelinidae), a parasitoid released for the control of Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Homoptera: Aphididae), in South Africa. Afr Entomol 6:147–149

    Google Scholar 

  42. Prinsloo GL, Neser OC (1994) The southern African species of Aphelinus Dalman (Hymenoptera: Aphelinidae), parasitoids of aphids (Homoptera: Aphidoidea). J Afr Zool 108:143–162

    Google Scholar 

  43. Prinsloo G, Chen Y, Giles KL, Grenstone MH (2002) Release and recovery in South Africa of the exotic aphid parasitoid Aphelinus hordei verified by the polymerase chain reaction. BioControl 47:127–136

    CAS  Google Scholar 

  44. Quicke DL (2014) The braconid and ichneumonid parasitoid wasps: biology, systematics, evolution and ecology. Wiley, Chichester

    Google Scholar 

  45. R Core Team (2017) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. https://www.r-project.org/

    Google Scholar 

  46. Rakhshani E, Tomanović Ž, Starý P, Talebi AA, Kavallieratos NG, Zamani AA, Stamenković S (2008) Distribution and diversity of wheat aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) in Iran. Eur J Entomol 105:863–870

    Google Scholar 

  47. Starý P (1970) Biology of aphid parasites (Hymenoptera: Aphidiidae) with respect to integrated control. Ser Entomol 6. Junk Publishers, The Hague

    Google Scholar 

  48. Starý P (1999) Parasitoids and biocontrol of Russian wheat aphid, Diuraphis noxia (Kurdj.) expanding in central Europe. J Appl Entomol 123:273–279

    Google Scholar 

  49. Stoetzel MB (1987) Information on and identification of Diuraphis noxia (Homoptera: Aphididae) and other aphid species colonizing leaves of wheat and barley in the United States. J Econ Entomol 80:696–704

    Google Scholar 

  50. Tomanović Ž, Starý P, Kavallieratos NG, Gagić V, Plećas M, Janković M, Rakhshani E, Ćetković A, Petrović A (2012) Aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) in wetland habitats in western palaearctic: key and associated aphid parasitoid guilds. Ann Soc Entomol Fr 48:189–198

    Google Scholar 

  51. Tomanović PA, Mitrović M, Kavallieratos NG, Starý P, Rakhshani E, Rakhshanipour M, Popović A, Shukshuk AH, Ivanović A (2014) Molecular and morphological variability within the Aphidius colemani group with redescription of Aphidius platensis Brethes (Hymenoptera: Braconidae: Aphidiinae). Bull Entomol Res 104:552–565

    PubMed  Google Scholar 

  52. Tougeron K, Brodeur J, van Baaren J, Renault D, Le Lann C (2018) Sex makes them sleepy: change in host reproductive status induces diapause in parasitoids. bioRxiv 371385

  53. Valenzuela I, Hoffmann AA (2015) Effects of aphid feeding and associated virus injury on grain crops in Australia. Austral Entomol 54:292–305

    Google Scholar 

  54. van den Bosch R (1957) The spotted alfalfa aphid and its parasites in the Mediterranean region, Middle East, and east Africa. J Econ Entomol 50:352–356

    Google Scholar 

  55. van den Bosch R, Schlinger EI, Dietrick EJ, Hall IM (1959) The role of imported parasites in the biological control of the spotted alfalfa aphid in southern California in 1957. J Econ Entomol 52:142–154

    Google Scholar 

  56. van den Bosch R, Schlinger EI, Dietrick JC, Hall C, Puttler B (1964) Studies on succession, distribution, and phenology of imported parasites of Therioaphis trifolii (Monell) in southern California. Ecology 45:602–621

    Google Scholar 

  57. Vollhardt IMG, Tscharntke T, Wäckers FL, Bianchi FJJA, Thies C (2008) Diversity of cereal aphid parasitoids in simple and complex landscapes. Agric Ecosyst Environ 126:289–292

    Google Scholar 

  58. Walters MC, Penn F, Du Toit F, Botha TC, Aalbersberg YK, Hewitt PH, Broodryk SW (1980) The Russian wheat aphid. Farming in South Africa. Leaflet series, wheat C3. Government Printer, Pretoria, pp 1–6

    Google Scholar 

  59. Walton MP, Powell W, Loxdale HD, Allen-Williams L (1990) Electrophoresis as a tool for estimating levels of hymenopterous parasitism in field populations of the cereal aphid, Sitobion avenue. Entomol Exp Appl 54:271–279

    Google Scholar 

  60. Waterhouse DF, Sands DPA (2001) Classical biological control of arthropods in Australia. ACIAR monograph no. 77. CSIRO Entomology, Australian Centre for International Agricultural Research, Canberra

    Google Scholar 

  61. White B, Day C, Christopher M, van Klinken R (2016) Should we invest in cereal pre-breeding now for biosecurity threats? Working paper 1605. School of Agricultural and Resource Economics, University of Western Australia, Crawley

    Google Scholar 

  62. Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York

    Google Scholar 

  63. Yazdani M, Baker G, DeGraaf H, Henry K, Hill K, Kimber B, Malipatil M, Perry K, Valenzuela I, Nash MA (2018) First detection of Russian wheat aphid Diuraphis noxia Kurdjumov (Hemiptera: Aphididae) in Australia: a major threat to cereal production. Austral Entomol 57:410–417

    Google Scholar 

  64. Yu DS (1990) Comparative studies of a native and an imported Aphelinus parasitizing the Russian wheat aphid in southern Alberta. In: Johnson GD (ed) Proceedings of the fourth Russian wheat aphid workshop. Montana State University, Bozeman, p 176

Download references

Acknowledgements

The authors wish to acknowledge and thank Jo Kent for her help with the genetics, Helen Brodie for help with identification, Courtney Proctor, Millie Moore and Clare Svilans for help with the field work and finally Hannah Wittwer for helping edit the manuscript. We would also like to thank the reviewers and editors for their helpful advice in getting the manuscript to a publishable level.

Funding

This work was supported by South Australian Grain Industry Trust Fund [S1117] and Grains Research and Development Corporation [UOA1805-018RTX].

Author information

Affiliations

Authors

Corresponding author

Correspondence to Thomas Heddle.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

No research was conducted on Humans or Animals.

Additional information

Handling Editor: Dirk Babendreier.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Heddle, T., Van Helden, M., Nash, M. et al. Parasitoid communities and interactions with Diuraphis noxia in Australian cereal production systems. BioControl (2020). https://doi.org/10.1007/s10526-020-10030-1

Download citation

Keywords

  • Parasitoids
  • Diaeretiella rapae
  • Aphidius colemani
  • Diuraphis noxia