Advertisement

Journal of Pest Science

, Volume 90, Issue 2, pp 495–505 | Cite as

Efficacy of entomopathogenic nematodes for control of large pine weevil, Hylobius abietis: effects of soil type, pest density and spatial distribution

  • Apostolos KapranasEmail author
  • Ben Malone
  • Sarajane Quinn
  • Louise Mc Namara
  • Christopher D. Williams
  • Padraig O’Tuama
  • Arne Peters
  • Christine T. Griffin
Original Paper

Abstract

The large pine weevil Hylobius abietis (L.), LPW, is a major pest of trees in replanted coniferous forests in northern Europe. The use of entomopathogenic nematodes (EPNs) applied against developing stages for population suppression is increasingly recognized as an effective alternative to plant protection using chemical pesticides. Here, we report results from a series of trials we conducted over 2 years using two species of EPN, Steinernema carpocapsae (Weiser) and Heterorhabitis downesi (Stock, Griffin, and Burnell) with different foraging strategies. Trials were conducted at lodgepole pine sites in Ireland on both mineral and peat soil type. EPN suspension was applied to the stumps of felled pine trees, and EPN efficacy was determined afterwards by directly assessing parasitism rates after debarking one quarter of the stumps and by collecting emerging adult weevils from traps erected over other treated and control stumps. Our results suggest that both species of EPN are equally effective in suppressing LPW populations to below the current, informal thresholds of economic damage. EPN were equally efficient in controlling LPW in peat and in mineral (lithosols/regosols and acid brown earth/brown podzolics) soils. Weevil density and distribution within pine stumps in peat versus mineral sites can explain patterns of LPW parasitism and suppression. Our results also suggest that infestation level (number of weevils per stump) can be an important factor in forecasting EPN application success as there is evidence of negative density-dependent parasitism when weevil densities were high.

Keywords

Forest pest Root-feeding insect Entomopathogenic nematodes Foraging strategy Soil type Density-dependent parasitism 

Notes

Acknowledgements

We thank Abigail Maher for technical support, and numerous forest managers and technicians from Coillte, Ireland, for providing access to sites and helping with trials. This research was funded by the BIOCOMES project co-funded by EU FP7.

Compliance with ethical standards

Conflict of interest

This research was funded by the European Union FP7 under grant agreement n° 612713 (BIOCOMES project). LM was supported by the Irish Government (Department of Agriculture, Food and the Marine) under the National Development Plan 2007–2013. All authors declare that they have no conflict of interest. This article does not contain any studies with animals performed by any of the authors.

Supplementary material

10340_2016_823_MOESM1_ESM.docx (148 kb)
Supplementary material 1 (DOCX 147 kb)

References

  1. Anonymous (2007) National forest inventory—Republic of Ireland—results. Forest Service, Johnstown CastleGoogle Scholar
  2. Anonymous (2014) FSC pesticide derogation approval: use of alpha-cypermethrin in UK. FSC-DER-30-V2-0 EN alpha-cypermethrin UK 150614. Forest Stewardship CouncilGoogle Scholar
  3. Ansari MA, Butt TM (2011) Effect of potting media on the efficacy and dispersal of entomopathogenic nematodes for the control of black vine weevil, Otiorhynchus sulcatus (Coleoptera: Curculionidae). Biol Control 58:310–318CrossRefGoogle Scholar
  4. Barredo JI, Strona G, de Rigo D, Caudullo G, Stancanelli G, San-Miguel-Ayanz J (2015) Assessing the potential distribution of insect pests: case studies on large pine weevil (Hylobius abietis L.) and horse-chestnut leaf miner (Cameraria ohridella) under present and future climate conditions in European forests. Bull EPPO 45:273–281. doi: 10.1111/epp.12208 CrossRefGoogle Scholar
  5. BIOCOMES Consortium. http://www.biocomes.eu/
  6. Brixey JM, Moore R, Milner AD (2006) Effect of entomopathogenic nematode (Steinernema carpocapsae Weiser) application technique on the efficacy and distribution of infection of the large pine weevil (Hylobius abietis L.) in stumps of Sitka spruce (Picea sitchensis Carr.) created at different times. For Ecol Manag 226:161–172CrossRefGoogle Scholar
  7. Choo HY, Kaya HK (1991) Influence of soil texture and presence of roots on host finding by Heterorhabditis bacteriophora. J Invertebr Pathol 58:279–280CrossRefGoogle Scholar
  8. Crawley MJ (1997) GLIM for ecologists. Blackwell Science, OxfordGoogle Scholar
  9. De Altube MDMM, Strauch O, De Castro GF, Pena AM (2008) Control of the flat–headed root borer Capnodis tenebrionis (Linne) (Coleoptera: Buprestidae) with the entomopathogenic nematode Steinernema carpocapsae (Weiser) (Nematoda: Steinernematidae) in a chitosan formulation in apricot orchards. Biocontrol 53:531–539CrossRefGoogle Scholar
  10. Dillon AB, Ward D, Downes MJ, Griffin CT (2006) Suppression of the large pine weevil Hylobius abietis (L.) (Coleoptera: Curculionidae) in pine stumps by entomopathogenic nematodes with different foraging strategies. Biol Control 38:217–226CrossRefGoogle Scholar
  11. Dillon AB, Downes MJ, Ward D, Griffin CT (2007) Optimizing application of entomopathogenic nematodes to manage large pine weevil, Hylobius abietis L. (Coleoptera: Curculionidae) populations developing in pine stumps, Pinus sylvestris. Biol Control 40:253–263CrossRefGoogle Scholar
  12. Dillon AB, Moore CP, Downes MJ, Griffin CT (2008) Evict or infect? Managing populations of the large pine weevil, Hylobius abietis, using a bottom-up and top-down approach. For Ecol Manag 255:2634–2642CrossRefGoogle Scholar
  13. Dillon AB, Foster A, Williams CD, Griffin CT (2012) Environmental safety of entomopathogenic nematodes—effects on abundance, diversity and community structure of non-target beetles in a forest ecosystem. Biol Control 63:107–114CrossRefGoogle Scholar
  14. EC (1991) Council Directive 91/414/EEC concerning the placing of plant protection products on the market. Off J Eur Union 230:1–32Google Scholar
  15. EC (2009a) Council Directive 2009/128/EC establishing a framework for Community action to achieve the sustainable use of pesticides. Off J Eur Union 309:71–86Google Scholar
  16. EC (2009b) Directive Regulation 1107/2009/EC concerning the placing of plant protection products on the market and repealing Council Directives 79/117/EEC and 91/414/EEC. Off J Eur Union 309:1–50Google Scholar
  17. Ehlers R-U, Hokkanen HMT (1996) Insect biocontrol with non-endemic entomopathogenic nematodes (Steinernema and Heterorhabditis spp.): conclusions and recommendations of a combined OECD and COST workshop on scientific and regulatory policy issues. Biocontrol Sci Technol 6:295–302CrossRefGoogle Scholar
  18. Ehlers R-U, Shapiro-Ilan DI (2005) Mass production. In: Grewal PS, Ehlers R-U, Shapiro-Ilan D (eds) Nematodes as biocontrol agents. CABI, Wallingford, pp 65–78CrossRefGoogle Scholar
  19. Eidmann HH, Lindelow A (1997) Estimates and measurements of pine weevil feeding on conifer seedlings: their relationships and application. Can J For Res 27:1068–1073CrossRefGoogle Scholar
  20. Ennis DE, Dillon AB, Griffin CT (2010) Simulated roots and host feeding enhance infection of subterranean insects by the entomopathogenic nematode Steinernema carpocapsae. J Invertebr Pathol 103:140–143CrossRefPubMedGoogle Scholar
  21. Evans H, Moore R, Heritage S, Wainhouse D (2004) Developments in the integrated management of pine weevil, a pest of restocking in conifer plantations. Forest research annual reports and accounts 2003–2004. Edinburgh, UKGoogle Scholar
  22. Evans H, McAllister F, Saunders T, Moore R, Jenkins T, Butt T, Ansari M., Griffin C, Williams C, Teck, R, Sweeney J (2015) The Impact project guide to Hyalobius management 2015. http://www.impactproject.eu/uploads/impact_hylobius_publication.pdf
  23. Gaugler R, Lewis E, Stuart RJ (1997) Ecology in the service of biological control: the case of entomopathogenic nematodes. Oecologia 109:483–489CrossRefGoogle Scholar
  24. Grant JA, Villani MG (2003) Soil moisture effects on entomopathogenic nematodes. J Nematol 15:329–332Google Scholar
  25. Grewal PS, Peters A (2005) Formulation and quality. In: Grewal PS, Ehlers R-U, Shapiro-Ilan D (eds) Nematodes as biocontrol agents. CABI, Wallingford, pp 79–90CrossRefGoogle Scholar
  26. Grewal PS, Selvan S, Gaugler R (1994) Thermal adaptation of entomopathogenic nematodes: niche breadth for infection, establishment, and reproduction. J Therm Biol 19:245–253CrossRefGoogle Scholar
  27. Grewal PS, Ehlers R-U, Shapiro-Ilan D (2005) Nematodes as biocontrol agents. CABI, WallingfordCrossRefGoogle Scholar
  28. Griffin CT (2015) Behaviour and population dynamics of entomopathogenic nematodes following application. In: Campos-Herrera R (ed) Nematode pathogenesis of insects and other pests: ecology and applied technologies for sustainable plant and crop protection. Springer International Publishing, Berlin, pp 57–96CrossRefGoogle Scholar
  29. Heritage S, Moore R (2001) The assessment of site characteristics as part of a management strategy to reduce damage by Hylobius. Forestry Commission Information Note 38, HMSO, UKGoogle Scholar
  30. Hiltpold I, Turlings TCJ (2008) Belowground chemical signaling in maize: when simplicity rhymes with efficiency. J Chem Ecol 34:628–635CrossRefPubMedGoogle Scholar
  31. Inward DJG, Wainhouse D, Peace A (2012) The effect of temperature on the development and life cycle regulation of the pine weevil Hylobius abietis and the potential impacts of climate change. Agric For Entomol 14:348–357CrossRefGoogle Scholar
  32. Jansson RK, Lecrone SH, Gaugler R (1993) Field efficacy and persistance of entomopathogenic nematodes (Rhabditida, Steinernematidae, Heterorhabditidae) for control of sweet–potato weevil (Coleoptera, Apionidae) in southern Florida. J Econ Entomol 86:1055–1063CrossRefGoogle Scholar
  33. Kennedy F (2002) The identification of soils for forest management. Forestry Commission field guide 19. Forestry Commission, Edinburgh, ScotlandGoogle Scholar
  34. Koppenhöfer AM, Fuzy EMJ (2006) Effect of soil type on infectivity and persistence of the entomopathogenic nematodes Steinernema scarabaei, Steinernema glaseri, Heterorhabditis zealandica, and Heterorhabditis bacteriophora. J Invertebr Pathol 92:11–22CrossRefPubMedGoogle Scholar
  35. Kruitbos LM, Heritage S, Hapca S, Wilson MJ (2010) The influence of habitat quality on the foraging strategies of the entomopathogenic nematodes Steinernema carpocapsae and Heterorhabditis megidis. Parasitology 137:303–309CrossRefPubMedGoogle Scholar
  36. Leather SR, Day KR, Salisbury AN (1999) The biology and ecology of the large pine weevil, Hylobius abietis (Coleoptera: Curculionidae): a problem of dispersal? Bull Entomol Res 89:3–16CrossRefGoogle Scholar
  37. Meier U (2006) A note on the power of Fisher’s least significant difference procedure. Pharm Stat 5:253–263CrossRefPubMedGoogle Scholar
  38. Moore R (2001) Emergence trap developed to capture adult large pine weevil Hylobius abietis (Coleoptera: Curculionidae) and its parasite Bracon hylobii (Hymenoptera: Braconidae). Bull Entomol Res 91:109–115PubMedGoogle Scholar
  39. Nielsen A, Lewis EE (2011) Designing the ideal habitat for entomopathogen use in nursery production. Pest Manag Sci 68:1053–1061CrossRefGoogle Scholar
  40. Örlander GR, Nilsson U (1999) Effect of reforestation methods on pine weevil (Hylobius abietis) damage and seedling survival. Scand J For Res 14:341–354CrossRefGoogle Scholar
  41. Örlander GR, Nordlander GR (2003) Effects of field vegetation control on pine weevil (Hylobius abietis) damage to newly planted Norway spruce seedlings. Ann For Sci 60:667–671CrossRefGoogle Scholar
  42. Paavilainen E, Päivänen J (1995) Peatland forestry ecology and principles. Ecological studies, vol 111. Springer-Verlag, BerlinCrossRefGoogle Scholar
  43. Preisser EL, Strong DR (2004) Climate affects predator control of an herbivore outbreak. Am Nat 163:754–762CrossRefPubMedGoogle Scholar
  44. Renou F, Farrell EP (2005) Reclaiming peatlands for forestry the Irish experience. In: Stanturf JA, Madsen P (eds) Restoration of boreal and temperate forests. CRC Press, Boca RatonGoogle Scholar
  45. Shapiro-Ilan D, Han R, Dolinski C (2012) Entomopathogenic nematode production and application technology. J Nematol 44:206–217PubMedPubMedCentralGoogle Scholar
  46. Stock P, Griffin CT, Burnell AM (2002) Morphological characterisation of three isolates of Heterorhabditis Poinar, 1997 from the ‘Irish group’ (Nematoda: Rhabditida: Heterorhabditidae) and additional evidence supporting their recognition as a distinct species, H. downesi sp. Syst Parasitol 51:95–106CrossRefPubMedGoogle Scholar
  47. Tan JY, Wainhouse D, Day KR, Morgan G (2010) Flight ability and reproductive development in newly emerged pine weevil Hylobius abietis and potential effects of climate change. Agric For Entomol 12:427–434CrossRefGoogle Scholar
  48. Thorpe KV, Day KR (2002) The impact of host plant species on the larval development of the large pine weevil Hylobius abietis L. Agric For Entomol 4:187–194CrossRefGoogle Scholar
  49. Torr PS, Wilson MJ, Heritage S (2005) Forestry applications. In: Grewal PS, Ehlers R-U, Shapiro-Ilan DI (eds) Nematodes as biocontrol agents. CABI Publishing, Oxfordshire, pp 281–293CrossRefGoogle Scholar
  50. Turlings TCJ, Hiltpold I, Rasmann S (2012) The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil 358:51–60CrossRefGoogle Scholar
  51. von Sydow F, Birgersson G (1997) Conifer stump condition and pine weevil (Hylobius abietis) reproduction. Can J For Res 27:1254–1262CrossRefGoogle Scholar
  52. Wainhouse D, Brough S, Greenacre B (2007) Managing the pine weevil on lowland pine. Forestry Commission http://www.forestry.gov.uk/pdf/FCPN014.pdf/FILE/FCPN014.pdf
  53. Wheeler BD (1995) Introduction: restoration and wetlands. In: Wheeler BD, Shaw SC, Fojt WJ, Robertson RA (eds) Restoration of temperate wetlands. John Wiley & sons, Chichester, pp 1–18Google Scholar
  54. Williams CD, Dillon AB, Harvey CD, Hennessy R, McNamara L, Griffin CT (2013a) Control of a major pest of forestry, Hylobius abietis, with entomopathogenic nematodes and fungi using eradicant and prophylactic strategies. For Ecol Manag 305:212–222CrossRefGoogle Scholar
  55. Williams CD, Dillon AB, Girling RD, Griffin CT (2013b) Organic soils promote the efficacy of entomopathogenic nematodes, with different foraging strategies, in the control of a major forest pest: a meta-analysis of field trial data. Biol Control 65:357–364CrossRefGoogle Scholar
  56. Williams CD, Dillon AB, Ennis D, Hennessy R, Griffin CT (2015) Differential susceptibility of pine weevil, Hylobius abietis (Coleoptera: Curculionidae), larvae and pupae to entomopathogenic nematodes and death of adults infected as pupae. Biocontrol 60:537–546CrossRefGoogle Scholar
  57. Wilson MJ, Ehlers R-U, Glazer I (2012) Entomopathogenic nematode foraging Strategies–is Steinernema carpocapsae really an ambush forager? Nematology 14:389–394CrossRefGoogle Scholar
  58. Wilson MJ, Wilson DJ, Rodgers A, Gerard PJ (2016) Developing a strategy for using entomopathogenic nematodes to control the African black beetle (Heteronychus arator) in New Zealand pastures and investigating temperature constraints. Biol Control 93:1–7CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of BiologyMaynooth UniversityMaynooth, Co. KildareIreland
  2. 2.TeagascOak Park Research CentreCo. CarlowIreland
  3. 3.School of Natural Sciences and PsychologyLiverpool John Moores UniversityLiverpoolUK
  4. 4.Coillte Forest, Hartnetts CrossMacroom, Co. CorkIreland
  5. 5.E-nema GmbHSchwentinentalGermany
  6. 6.Institute of BiologyUniversity of NeuchâtelNeuchâtelSwitzerland

Personalised recommendations