Elsevier

Forest Ecology and Management

Volume 380, 15 November 2016, Pages 242-251
Forest Ecology and Management

Inundative pest control: How risky is it? A case study using entomopathogenic nematodes in a forest ecosystem

https://doi.org/10.1016/j.foreco.2016.08.018Get rights and content

Highlights

  • Entomopathogenic nematodes (EPN) are used to control developing pine weevil in stumps.

  • We assessed direct and indirect risks associated with EPN use in forest ecosysytems.

  • We review establishment, dispersal, host range, direct & indirect non-target effects.

  • Risks were minimal in comparison to other studies and compared to chemical control.

Abstract

Entomopathogenic nematodes (EPN) are globally important inundative biological control agents. Their widespread use makes environmental risk assessment important, but very few comprehensive post-application risk assessments have been conducted for EPN. We apply a rigorous risk analysis procedure to the use of EPN applied in a forest ecosystem to suppress the large pine weevil (Hylobius abietis). In this synthesis, we provide a quantitative evaluation of five risk categories: (a) establishment, (b) dispersal, (c) host range, (d) direct non-target effects and (e) indirect non-target effects. A low level of risk was identified (35–51 out of a possible total of 125). Species exotic to the clear-fell forest ecosystem (Steinernema carpocapsae and Heterorhabditis downesi) were accorded a lower overall risk status than native species and strains (Steinernema feltiae), largely as a result of their shorter persistence in the target environment. We conclude that EPN are a low risk viable alternative control for pine weevil compared to the higher risk conventional control using pyrethroid or neonicotinoid insecticides.

Section snippets

Inundative control with EPN and the potential associated risks

Entomopathogenic nematodes (EPN) are lethal insect pathogens that are commercially produced as inundative control agents and used in various regions of the world against a variety of pests (Kaya and Gaugler, 1993, Shapiro-Ilan et al., 2006, Grewal, 2012). There are two genera (Steinernema Travassos, 1927 and Heterorhabditis Poinar, 1976: Nematoda: Rhabditidae), both of which have global natural distributions (except Antarctica) and are used in biological control (Kaya and Gaugler, 1993, Stuart

Large pine weevil control: Target pest, environment and control agents

The large pine weevil is a major forestry pest in 15 European countries, including Ireland and the UK (Långström & Day, 2004). This insect threatens an estimated 3.4 million hectares of forests and would cause up to €140 million in annual damages if not controlled (Långström & Day, 2004). Larvae feed and develop under the bark of stumps and roots of recently dead conifers for one or more years (Leather et al., 1999). Emerging adults feed on the bark of seedlings that are planted to restock such

Natural distribution of entomopathogenic nematode species used for pine weevil control

Organisms exotic to a particular environment may pose risks that differ in quality and scale from those posed by indigenous organisms (Simberloff and Stiling, 1996, van Lenteren et al., 2003, Clercq et al., 2011, van Lenteren, 2012). Ehlers and Hokkanen (1996) recommended that, unlike the release of indigenous EPN, the release of exotic EPN species (but not exotic strains of indigenous species) should be regulated due to greater potential risk. Thus, a discussion of the risks posed by EPN must

Risk categories for inundative control agents

Several methods to standardise risk assessment procedures for inundative control agents have been proposed (van Lenteren et al., 2003, Babendreier et al., 2005, Mills et al., 2006). To meet the criteria for risk assessment of introduced biological control agents recommended by the Organisation for Economic Co-operation and Development (OECD, 2003), van Lenteren et al. (2003) proposed a method of calculating a numerical index based on five risk categories. This method allows for a categorical

Establishment

In inundative biological control, long-term persistence and establishment of the applied control agent in the target environment is not a desired outcome (Bathon, 1996, van Lenteren et al., 2003). Control agents are applied in large numbers to cause an immediate, but usually transient, reduction in the pest population. EPN have the potential to persist in the soil after application since the applied IJs are the non-feeding, stress-tolerant ‘dauer’ stage; in addition, they may recycle and

Conclusions and risk evaluation

Both exotic and indigenous EPN trialled against the large pine weevil persisted in the soil for up to four years after application (Dillon et al., 2008a, Harvey and Griffin, 2016), but the evidence suggests that persistence was driven by recycling through the target pest as intended. Consequently, EPN levels decreased to background levels (for an indigenous strain) or undetectable levels (for exotic species/strains) along with the natural decrease in pest population (Torr et al., 2007, Dillon

Acknowledgments

CDH was funded by the EPA STRIVE programme (project 2007-PhD-B-6) and CDW was funded by INTERREG IVA (IMPACT Project), co-funded by the Department of Agriculture, Food and the Marine (DAFM). Field trials were conducted under licence from the Pesticide Control Service of DAFM.

References (114)

  • A.B. Dillon et al.

    Environmental safety of entomopathogenic nematodes – Effects on abundance, diversity and community structure of non-target beetles in a forest ecosystem

    Biol. Control

    (2012)
  • M.S. Eng et al.

    Phoresy of the entomopathogenic nematode Heterorhabditis marelatus by a non-host organism, the isopod Porcellio scaber

    J. Invertebr. Pathol.

    (2005)
  • P.S. Grewal et al.

    Thermal adaptation of entomopathogenic nematodes: Niche breadth for infection, establishment, and reproduction

    J. Therm. Biol.

    (1994)
  • P.S. Grewal et al.

    Dauer juvenile longevity and stress tolerance in natural populations of entomopathogenic nematodes: is there a relationship?

    Int. J. Parasitol.

    (2002)
  • C.D. Harvey et al.

    The impact of entomopathogenic nematodes on a non-target, service-providing longhorn beetle is limited by targeted application when controlling forestry pest Hylobius abietis

    Biol. Control

    (2012)
  • P.O. Hedgren

    Early arriving saproxylic beetles (Coleoptera) and parasitoids (Hymenoptera) in low and high stumps of Norway spruce

    For. Ecol. Manage.

    (2007)
  • A.K. Hodson et al.

    Ecological influence of the entomopathogenic nematode, Steinernema carpocapsae, on pistachio orchard soil arthropods

    Pedobiologia

    (2012)
  • R. Jabbour et al.

    Soil and habitat complexity effects on movement of the entomopathogenic nematode Steinernema carpocapsae in maize

    Biol. Control

    (2008)
  • M. Jonsell et al.

    Diversity of saproxylic beetle species in logging residues in Sweden – comparisons between tree species and diameters

    Biol. Conserv.

    (2007)
  • A.M. Koppenhofer et al.

    Effect of soil type on infectivity and persistence of the entomopathogenic nematodes Steinernema scarabaei, Steinernema glaseri, Heterorhabditis zealandica, and Heterorhabditis bacteriophora

    J. Invertebr. Pathol.

    (2006)
  • Lawrence A. Lacey et al.

    Interactions of two idiobiont parasitoids (Hymenoptera: Ichneumonidae) of codling moth (Lepidoptera: Tortricidae) with the entomopathogenic nematode Steinernema carpocapsae (Rhabditida: Steinernematidae)

    J. Invertebr. Pathol.

    (2003)
  • E.E. Lewis et al.

    Behavioral ecology of entomopathogenic nematodes

    Biol. Control

    (2006)
  • L.C. Millar et al.

    Interaction between endemic and introduced entomopathogenic nematodes in conventional-till and no-till corn

    Biol. Control

    (2001)
  • J.P. Parkman et al.

    Dispersal of Steinernema scapterisci (Rhabditida: Steinernematidae) after inoculative applications for mole cricket (Orthoptera: Gryllotalpidae) control in pastures

    Biol. Control

    (1993)
  • A.E. Pye et al.

    Neoaplectana carpocapsae: Infection and reproduction in large pine weevil larvae, Hylobius abietis

    Exp. Parasitol.

    (1978)
  • J.A. Rosenheim et al.

    Intraguild predation among biological-control agents: theory and evidence

    Biol. Control

    (1995)
  • D.I. Shapiro-Ilan et al.

    Application technology and environmental considerations for use of entomopathogenic nematodes in biological control

    Biol. Control

    (2006)
  • D. Simberloff et al.

    Risks of species introduced for biological control

    Biol. Conserv.

    (1996)
  • R.J. Stuart et al.

    Patchiness in populations of entomopathogenic nematodes

    J. Invertebr. Pathol.

    (1994)
  • R.L. Anderson

    Toxicity of fenvalerate and permethrin to several nontarget aquatic invertebrates

    Environ. Entomol.

    (1982)
  • D. Babendreier et al.

    Methods used to assess non-target effects of invertebrate biological control agents of arthropod pests

    Biocontrol

    (2005)
  • B.I.P. Barratt et al.

    Post-release evaluation of non-target effects of biological control agents

  • H. Bathon

    Impact of entomopathogenic nematodes on non-target hosts

    Biocontrol Sci. Technol.

    (1996)
  • A. Battisti

    Effects of entomopathogenic nematodes on the spruce web-spinning sawfly Cephalcia arvensis Panzer and its parasitoids in the fields

    Biocontrol Sci. Technol.

    (1994)
  • R.P. Blackshaw

    A survey of insect parasitic nematodes in Northern Ireland

    Ann. Appl. Biol.

    (1988)
  • B. Boag et al.

    Distribution and prevalence of the entomopathogenic nematode Steinernema feltiae in Scotland

    Ann. Appl. Biol.

    (1992)
  • E. Brockerhoff et al.

    Plantation forests and biodiversity: oxymoron or opportunity?

    Biodivers. Conserv.

    (2008)
  • P. Clercq et al.

    Benefits and risks of exotic biological control agents

    Biocontrol

    (2011)
  • Dillon, A.B., 2003. Biological control of the large pine weevil, Hylobius abietis L., (Coleoptera: Curculionidae) using...
  • A.B. Dillon et al.

    Establishment, persistence, and introgression of entomopathogenic nematodes in a forest ecosystem

    Ecol. Appl.

    (2008)
  • M.J. Downes et al.

    Dispersal behaviour and transmission strategies of the entomopathogenic nematodes Heterorhabditis and Steinernema

    Biocontrol Sci. Technol.

    (1996)
  • E.A.J. Duffy

    A Monograph of the Immature Stages of British and Imported Timber Beetles (Cerambycidae)

    (1953)
  • L.W. Duncan et al.

    Incidence of endemic entomopathogenic nematodes following application of Steinernema riobrave for control of Diaprepes abbreviatus

    J. Nematol.

    (2003)
  • R.-U. Ehlers et al.

    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.

    (1996)
  • D.E. Ennis et al.

    Simulated roots and host feeding enhance infection of subterranean insects by the entomopathogenic nematode Steinernema carpocapsae

    J. Invertebr. Pathol.

    (2012)
  • A. Everard et al.

    Competition and intraguild predation between the braconid parasitoid Bracon hylobii and the entomopathogenic nematode Heterorhabditis downesi, natural enemies of the large pine weevil, Hylobius abietis

    Bull. Entomol. Res.

    (2009)
  • S. Forst et al.

    Xenorhabdus and Photorhabdus spp.: Bugs that kill bugs

    Annu. Rev. Microbiol.

    (1997)
  • R. Georgis et al.

    A steinernematid nematode in the web-spinning larch sawfly, Cephalcia lariciphila (Wachtl)

    Plant. Pathol.

    (1979)
  • R. Georgis et al.

    A neoaplectanid nematode in the larch sawfly Cephalcia lariciphila (Hymenoptera: Pamphiliidae)

    Ann. Appl. Biol.

    (1981)
  • P.S. Grewal

    Entomopathogenic nematodes as tools in integrated pest management

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