Elsevier

Biological Control

Volume 56, Issue 2, February 2011, Pages 175-178
Biological Control

Potential risks of systemic imidacloprid to parasitoid natural enemies of a cerambycid attacking Eucalyptus

https://doi.org/10.1016/j.biocontrol.2010.08.007Get rights and content

Abstract

A community of insect herbivores has established on eucalyptus species in California following their introduction from Australia. A number of the species are under complete or partial biological control. A response to introduction of additional pest species into the complex has been the application of systemic insecticides to infested trees. Natural enemies that have been introduced to control the various pest species feed on the nectar of treated trees, and thus may be affected by these pesticides. In this study, Eucalyptus rudis trees were treated at label rates with the neonicotinoid systemic insecticide imidacloprid and nectar sampled at 5 months post-treatment during the spring bloom. The concentration of imidacloprid and its toxic metabolites in nectar was measured by ELISA at 660 ppb. Adults of the encyrtid egg parasitoid Avetianella longoi that were fed floral nectar collected from treated trees had significantly lower survival and reproductive fitness than adults fed nectar from untreated trees. In feeding bioassays, in which the adults were fed a range of concentrations of imidacloprid in sugar water, the LC50 for A. longoi was 212 ppb imidacloprid. Bioassays were also conducted with the braconid larval parasitoid, Syngaster lepidus. The LC50 for S. lepidus was 288 ppb imidacloprid. The insecticide appears to be concentrating in the nectar at higher levels than reported from other plant species and at concentrations exceeding the LC50 for two important parasitoids. If tree treatments become widespread as a result of continual introductions of new eucalypt herbivores, established biological control programs could be at significant risk.

Graphical abstract

The systemic neonicotinoid insecticide, imidacloprid, applied to the root zone of Eucalyptus and its toxic metabolites concentrate in floral nectar at 660 ppb. Adult parasitoids of Phoracantha semipunctata feed on nectar from Eucalyptus flowers. The LC50s of the egg parasitoid, Aventianella longoi, and the larval parasitoid, Syngaster lepidus, are 212 ppb and 288 ppb, respectively. Applications of the insecticide targeting other eucalypt herbivores have the potential to interfere with established biological control programs.

  1. Download : Download full-size image

Research highlights

► The concentration of imidacloprid and its toxic metabolites in nectar was 660 ppb. ► The LC50 for Avetianella longoi was 212 ppb imidacloprid. ► The LC50 for Syngaster lepidus was 288 ppb imidacloprid. ► A. longoi fed floral nectar from treated trees had lower survival and reproduction.

Introduction

Systemic insecticides are frequently thought to be more compatible with biological control than contact materials because natural enemies, feeding primarily on arthropod prey and not host plant tissues, have limited contact with the pesticides (Stapel et al., 2000). However, although natural enemies typically do not feed on foliage, many adult parasitoids feed on floral and extra-floral nectar. There is a growing body of evidence that suggests that systemic insecticides can not only contaminate nectar, but that natural enemies feeding on the nectar can be adversely affected (Cate et al., 1972, Stapel et al., 2000, Krischik et al., 2007).

Ecualyptus L’Heritier species were introduced into California in the middle of the 19th century for timber, windbreaks, and a variety of other uses (Doughty, 2000). For nearly 130 years, the trees remained free of introduced herbivores. However, beginning in 1984 the first of a community of herbivores was introduced into the state (Scriven et al., 1986, Paine and Millar, 2002). The list now includes at least 16 species in four different feeding guilds: 2 species of borers, 8 species of fluid-feeders, 3 species of foliage feeders, and 3 species of gall makers (Gill, 1998, TDP pers. obs.). Comprehensive efforts have been initiated to develop an integrated pest management program (Paine et al., 1995, Paine and Millar, 2005) that relies primarily on the use of cultural practices that promote host resistance (Hanks et al., 1999), host species selection (Hanks et al., 1993a, Hanks et al., 1993b, Hanks et al., 1995a, Hanks et al., 1995b), and biological control (Dahlsten et al., 1998, Dahlsten et al., 2005, Paine et al., 1993, Paine et al., 1997, Hanks et al., 1995a, Hanks et al., 1995b, Hanks et al., 2000).

The use of pesticides for the control of herbivores feeding on Eucalyptus spp. had been limited, in part because of the size of the trees, the wide dispersal of trees over large areas of unmaintained and landscaped land, and the limited availability of effective systemic insecticides. However, the introduction of red gum lerp psyllid, Glycaspis brimblecombei Moore (Hemiptera: Psyllidae), threatened the established integrated pest management program. Widespread and dense infestations of the insect resulted in the death of large numbers of trees in urban landscapes throughout California (Dahlsten et al., 2005). Although biological control programs were initiated very shortly after establishment of the psyllid, arborists and landscape managers responded to demands from their clientele for applications of systemic insecticides, particularly imidacloprid, as both curative and protective treatments of urban forest trees.

Complete or substantial biological control had been established against at least four important Eucalyptus herbivores (Phoracantha semipunctata (F.) (Coleoptera: Cerambycidae) [Hanks et al., 1995a, Hanks et al., 1995b], Gonipterus scutellatus (Coleoptera: Curculeonidae) [Hanks et al., 2000], Ctenarytaina eucalypti (Hemiptera: Psyllidae) [Dahlsten et al., 1998], and G. brimblecombei [Dahlsten et al., 2005]) and was the cornerstone of the integrated pest management program developed for the community of herbivores. However, widespread reliance on systemic treatments of imidacloprid for the control of the newly-introduced psyllids into that community could disrupt the biological control of other species if the insecticide accumulates in the floral nectar at levels that cause detrimental effects on adult natural enemies feeding on the nectar. The objective of the present study was to determine if imidacloprid accumulated in the nectar of treated Eucalyptus trees, to determine the toxicity of insecticide to adults of Avetianella longoi Siscaro (Hymentoptera: Encyrtidae) and Syngaster lepidus Brulle (Hymentoptera: Braconidae), parasitoids of P. semipunctata, and to determine if feeding on nectar collected from treated trees affected parasitoid reproductive fitness.

Section snippets

Insect colonies

Laboratory populations of the cerambycid beetle host, P. semipunctata, were initiated from individuals emerging from logs collected from established field populations in southern California. The colony was supplemented with additional individuals added to the laboratory populations each year. The procedures for rearing P. semipunctata are described in Hanks et al., 1993a, Hanks et al., 1993b. Briefly, adult beetles emerging from the colonies were collected daily and transferred to cylindrical

Imidacloprid in nectar

Trees treated with the label rate of imidacloprid accumulated insecticide in floral nectar at a pooled concentration of 286 ppb five months after application. The insecticide was not detected in nectar collected from untreated control trees. In addition to the imidacloprid, the ELISA also detected unidentified metabolites of imidacloprid that cross-react with the antibody used in the analysis. The combined imidacloprid and metabolite reading from the ELISA was 660 ppb.

Toxicity of imidacloprid

Adult A. longoi and S.

Discussion

Insecticide applications have long been recognized as contributing to significant disruptions to biological control of insect herbivores by natural enemies (Stern et al., 1959). Arthropod predators and parasitoids contact insecticide residues that are directly applied to plants, resulting in both increased mortality and behavioral effects (Stapel et al., 2000, Rebek and Sadof, 2003, Desneux et al., 2007, Grafton-Cardwell et al., 2008). Consequently rates of parasitism are reduced.

Systemic

Acknowledgments

We thank Sarah Allen for assistance in the field collections and Jocelyn Millar for this thoughtful review of the paper. The research was supported, in part, by grants from the CSREES/UC Invasive and Exotic Pest and Disease Program to TDP.

References (37)

  • R.W. Doughty

    The Eucalyptus: A Natural and Commercial History of the Gum Tree

    (2000)
  • D.J. Finney

    Probit Analysis

    (1971)
  • R.J. Gill

    Recently introduced pests of Eucalyptus

    California Plant Pest Disease Report

    (1998)
  • E.E. Grafton-Cardwell et al.

    Role of imidacloprid in integrated pest management of California citrus

    Journal of Economic Entomology

    (2008)
  • L.M. Hanks et al.

    Phoracantha semipunctata F. (Coleoptera: Cerambycidae), a serious pest of Eucalyptus in California: Biology and laboratory rearing procedures

    Annals of the Entomological Society of America

    (1993)
  • L.M. Hanks et al.

    Host species preference and larval performance in the wood-boring beetle Phoracantha semipunctata F

    Oecologia (Berlin)

    (1993)
  • L.M. Hanks et al.

    Variation among Eucalyptus species in resistance to eucalyptus longhorned borer in Southern California

    Entomologia Experimentalis et Applicata

    (1995)
  • L.M. Hanks et al.

    Biology and host relations of Avetianella longoi. (Hymenoptera: Encyrtidae), an egg parasitoid of the eucalyptus longhorned borer (Coleoptera: Cerambycidae)

    Annals of the Entomological Society of America

    (1995)
  • View full text