Skip to main content
SpringerLink
Log in

Female-Produced Sex Pheromone of Tetrastichus planipennisi, a Parasitoid Introduced for Biological Control of the Invasive Emerald Ash Borer, Agrilus planipennis

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

The Asian eulophid wasp Tetrastichus planipennisi is being released in North America as a biocontrol agent for the emerald ash borer (Agrilus planipennis), a very destructive invasive buprestid beetle that is devastating ash trees (Fraxinus spp.). We identified, synthesized, and tested a female-produced sex pheromone for the wasp. The key component eliciting behavioral responses from male wasps in flight tunnel bioassays was identified as (6S,10S)-(2E,4E,8E)-4,6,8,10-tetramethyltrideca-2,4,8-triene. Female specificity was demonstrated by gas chromatographic (GC) comparison of male and female volatile emissions and whole body extracts. The identification was aided by coupled gas chromatography/mass spectrometry analysis, microchemical reactions, NMR, GC analyses with a chiral stationary phase column, and matching GC retention times and mass spectra with those of synthetic standards. The tetramethyl-triene hydrocarbon was synthesized as a mixture of two enantiomeric pairs of diastereomers, and as the pure insect-produced stereoisomer. In flight-tunnel bioassays, males responded to both the natural pheromone and the chiral synthetic material by upwind flight and landing on the source. In contrast, the mixture of four stereoisomers was not attractive, indicating that one or more of the “unnatural” stereoisomers antagonized attraction. Field trials, using yellow pan traps baited with natural pheromone, captured significantly more male wasps than control traps over a four week trial. The identified pheromone could increase the efficiency and specificity of the current detection methods for Tetrastichus planipennisi and aid in the determination of parasitoid establishment at release sites.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Scheme 1
Scheme 2
Scheme 3
Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abell K, Poland T, Cossé A, Bauer L (2015) Trapping techniques for emerald ash borer and its introduced parasitoids, pp. 113–127, in Van Driesche RG, Reardon RC (eds.), Biology and Control of Emerald Ash Borer. U.S. Department of Agriculture, Forest Service, Forest Health Technology Enterprise Team, Morgantown, WV. FHTET-2014-09. Available at: https://www.nrs.fs.fed.us/pubs/49295

  • Ayasse M, Paxton RJ, Tengo J (2001) Mating behavior and chemical communication in the order Hymenoptera. Annu Rev Entomol 46:31–78

    Article  CAS  Google Scholar 

  • Bartelt RJ (1999) Sap Beetles. In: Hardie J, Minks AK (eds) Pheromones of non-lepidopteran insects associated with agricultural plants. CABI Publishing, New York, pp 69–89

    Google Scholar 

  • Bartelt RJ, Dowd PF, Plattner PD, Weisleder D (1990) Aggregation pheromone of dried fruit beetle, Carpophilus hemipterus: wind-tunnel bioassay and identification of two novel tetraene hydrocarbons. J Chem Ecol 16:1015–1039

    Article  CAS  Google Scholar 

  • Bauer LS, Liu HP, Miller DL, Gould J (2008) Developing a biological control program for emerald ash borer (Agrilus planipennis), an invasive ash pest in North America. Newsl Michigan Entomol Soc 53:38–39

    Google Scholar 

  • Bauer LS, Liu H, Miller D (2009) Emerald ash borer biological control: rearing, releasing, establishment, and efficacy of parasitoids, pp. 7–8, in McManus KA, Gottschalk KW (eds.). Proceedings. 20th U.S. Department of Agriculture interagency research forum on invasive species; 2009 January 13–16; Annapolis, MD. Gen. Tech. Rep. NRS-P-51. Newtown Square, PA: U.S. Department of Agriculture, Forest Service, Northern Research Station. Available at: https://www.nrs.fs.fed.us/pubs/34330

  • Bauer LS, Gould J, Duan J, Hansen J, Cossé A, Miller D, Abell K, Van Driesche R, Lelito J, Poland T (2012) Sampling methods for recovery of exotic emerald ash borer parasitoids after environmental release, pp. 2–5, in McManus KA, Gottschalk KW (eds.). Proceedings. 22nd U.S. Department of Agriculture interagency research forum on invasive species; 2011 January 10–13; Annapolis, MD. Gen. Tech. Rep. NRS-P-92. Newtown Square, PA: U.S. Department of Agriculture, Forest Service, Northern Research Station. Available at: http://nrs.fs.fed.us/pubs/39810

  • Bauer LS, Duan JJ, Gould J (2014) Emerald ash borer (Agrilus planipennis Fairmaire) (Coleoptera: Buprestidae), pp. 189–209, in Van Driesche R, Reardon R. (eds.). The Use of Classical Biological Control to Preserve Forests in North America. U.S. Department of Agriculture, Forest Service, Forest Health Technology Enterprise Team, Morgantown, WV. FHTET-2013-02. Available at: http://www.fs.fed.us/foresthealth/technology/pdfs/FHTET-2013-2.pdf

  • Bauer LS, Duan JJ, Gould JR, Van Driesche R (2015) Progress in the classical biological control of Agrilus planipennis Fairmaire (Coleoptera: Buprestidae) in North America. Can Entomol 147:300–317

  • Bauer L, Hansen J, Gould J (2016) Yellow Pan Traps: A Simple Method for Trapping Parasitoids Released for Biological Control of the Emerald Ash Borer. Available at: https://www.nrs.fs.fed.us/disturbance/invasive_species/eab/local-resources/downloads/YPT_Method20160304.pdf

  • Bray AM, Bauer LS, Poland TM, Haack RA, Cognato AI, Smith JJ (2011) Genetic analysis of emerald ash borer (Agrilus planipennis Fairmaire) populations in Asia and North America. Biol Invasions 13:2869–2887

    Article  Google Scholar 

  • Cooperband MF, Hartness A, Lelito JP, Cossé AA (2013) Landing surface color preferences of Spathius agrili (Hymenoptera: Braconidae), a parasitoid of emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae). J Insect Behav 26(5):721–729

    Article  Google Scholar 

  • Cossé AA, Petroski RJ, Zilkowski BW, Vermillion K, Lelito JP, Cooperband MF, Gould JR (2012) Male-produced pheromone of Spathius agrili, a parasitoid introduced for the biological control of the invasive emerald ash borer, Agrilus planipennis. J Chem Ecol 38(4):389–399

    Article  Google Scholar 

  • Duan JJ, Bauer LS, Abell KJ, Lelito JP, Van Driesche R (2013) Establishment and abundance of Tetrastichus planipennisi (Hymenoptera: Eulophidae) in Michigan: potential for success in classical biocontrol of the invasive emerald ash borer (Coleoptera: Buprestidae). J Econ Entomol 106:1145–1154

    Article  Google Scholar 

  • Duan JJ, Bauer LS, Van Driesche RG (2017) Emerald ash borer biocontrol in ash saplings: the potential for early stage recovery of north American ash trees. Forest Ecol Manag 394:64–72

    Article  Google Scholar 

  • Duan JJ, Bauer LS, Van Driesche RG, Gould JR (2018) Progress and challenges of protecting north American ash trees from the emerald ash borer using biological control. Forests 9:1–17

    Google Scholar 

  • Duan JJ, Van Driesche RG, Crandall RS, Schmude JM, Rutledge CE, Slager BH, Gould JR, Elkinton JS (2019) Establishment and early impact of Spathius galinae (Hymenoptera: Braconidae) on emerald ash borer (Coleoptera: Buprestidae) in the northeastern United States. J Econ Entomol 112(5):2121–2130

    Article  Google Scholar 

  • El-Sayed AM, Godde J, Arn H (1999) Sprayer for quantitative application of odor stimuli. Environ Entomol 28:947–953

    Article  Google Scholar 

  • Emeraldashborer Info (2020) (http://emeraldashborer.info)

  • Evans DA, Ennis MD, Mathre DJ (1982) Asymmetric alkylation reactions of chiral imide enolates. A practical approach to the enantioselective synthesis of α-substituted carboxylic acid derivatives. J Am Chem Soc 104:1737–1739

    Article  CAS  Google Scholar 

  • Federal Register (2007) Availability of an environmental assessment for the proposed release of three parasitoids for the biological control of the emerald ash borer (Agrilus planipennis) in the continental United States. Fed Regist 72:28947–28948 (http://www.regulations.gov/#!docketDetail;D=APHIS-2007-0060)

    Google Scholar 

  • Federal Register (2015) Availability of an environmental assessment for field release of the parasitoid Spathius galinae for the biological control of the emerald ash borer (Agrilus planipennis) in the contiguous United States. Fed. Regist. 2015, 80: 7827–7828. (https://www.regulations.gov/ docket?D=APHIS-2014-0094)

  • Geerdink D, Buter J, van Beek TA, Minnaard AJ (2014) Asymmetric total synthesis of a putative sex pheromone component from the parasitoid wasp Trichogramma turkestanica. Beilstein J Org Chem 10:761–766

    Article  Google Scholar 

  • Gould JR, Bauer LS, Duan JJ, Williams D, Liu H (2015) History of emerald ash borer biological control. pp. 83–95. In: Van Driesche RG, Reardon RC (eds.), Biology and Control of Emerald Ash Borer. U.S. Department of Agriculture, Forest Service, Forest Health Technology Enterprise Team, Morgantown, WV. FHTET-2014-09. Available at: https://www.nrs.fs.fed.us/pubs/49321

  • Haack RA, Jendek E, Liu H, Marchant KR, Petrice TR, Poland TM, Ye H (2002) The emerald ash borer: a new exotic pest in North America. Newsletter Michigan Entomol Soc 47:1–5 Available at: https://www.nrs.fs.fed.us/pubs/1858

    Google Scholar 

  • Haack RA, Baranchikov Y, Bauer LS, Poland TM (2015) Emerald ash borer biology and invasion history, pp. 1–13, in Van Driesche RG, Reardon R (eds.). The Biology and Control of Emerald Ash Borer. USDA FS FHTET 2014–09

  • Heath RR, Sonnet PE (1980) Technique for in situ coating of Ag+ onto silica gel in HPLC columns for the separation of geometrical isomers. J Liq Chromatogr 3:1129–1135

    Article  CAS  Google Scholar 

  • Hooie HA, Wiggins GJ, Lambdin PL, Grant JF, Powell SD, Lelito JP (2015) Native parasitoids and recovery of Spathius agrili from areas of release against emerald ash borer in eastern Tennessee, USA. Biocontrol Sci Tech 25:345–351

    Article  Google Scholar 

  • Jin Y, Roberts FG, Coates RM (2007) Stereoselective isoprenoid chain extension with acetoacetate dianion: (E,E,E)-geranylgeraniol from (E,E)-farnesol. Org Synth 84:43–57

    Article  CAS  Google Scholar 

  • Kasun ZA, Gao X, Lipinski RM, Krische MJ (2015) Direct generation of triketide stereopolyads via merged redox-construction events: Total synthesis of (+)-zincophorin methyl ester. J Am Chem Soc 137:8900–8903

    Article  CAS  Google Scholar 

  • Keeling C, Plettner E, Slessor KN (2004) Hymenopteran Semiochemicals. Top Curr Chem 239:133–177

    Article  CAS  Google Scholar 

  • Lister T, Perkins MV (2004) Total synthesis of a hemiacetal polypropionate from Siphonaria australis. Aus J Chem 57:787–797

    Article  CAS  Google Scholar 

  • Liu HP, Bauer LS, Gao RT, Zhao TH, Petrice TR, Haack RA (2003) Exploratory survey for the emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae), and its natural enemies in China. Great Lakes Entomol 36:191–204

    Google Scholar 

  • Liu HP, Bauer LS, Miller DL, Zhao TH, Gao RT, Song L, Luan Q, Jin R, Gao C (2007) Seasonal abundance of Agrilus planipennis (Coleoptera: Buprestidae) and its natural enemies Oobius agrili (Hymenoptera: Encyrtidae) and Tetrastichus planipennisi (Hymenoptera: Eulophidae) in China. Biol Control 42:61–71

    Article  Google Scholar 

  • Mapbiocontrol (2020) Available at: http://www.mapbiocontrol.org/2020

  • NIST (2017) NIST Standard Reference Database Number 173, National Institute of Standards and Technology, Gaithersburg MD, 20899

  • Tröger A, Van Beek TA, Huigens ME, Silva IMMS, Posthumus MA, Francke W (2014) Structure elucidation of female-specific volatiles released by the parasitoid wasp Trichogramma turkestanica (Hymenoptera: Trichogrammatidae). J Organomet Chem 10:767–773

    Google Scholar 

  • Ulyshen MD, Duan JJ, Bauer LS, Fraser I (2010) Suitability and accessibility of immature Agrilus planipennis (Coleoptera: Buprestidae) stages to Tetrastichus planipennisi (Hymenoptera: Eulophidae). J Econ Entomol 103:1080–1085

    Article  Google Scholar 

  • USDA–APHIS/ARS/FS (2019) 2020. Emerald ash borer biological control release and recovery guidelines. USDA–APHIS–ARS-FS, Riverdale, Maryland. Available at: https://www.aphis.usda.gov/plant_health/plant_pest_info/emerald_ash_b/downloads/EAB-FieldRelease-Guidelines.pdf

  • Wang Q, Deredas D, Huynh C, Schlosser M (2003) Sequestered alkyllithiums: why phenyllithium alone is suitable for betaine-ylide generation. Chem Eur J 9:570–574

    Article  CAS  Google Scholar 

  • Wiley (2007) Wiley. Spectral library, [CD-ROM], 7th edn. Wiley, New York

    Google Scholar 

  • Yang Z, Strazanac JS, Yanxia Y, Xaioyi W (2006) A new species of emerald ash borer parasitoid from China belonging to the genus Tetrastichus Haliday (Hymenoptera: Eulophidae). Proc Entomol Soc Wash 108:550–558

    Google Scholar 

  • Zilkowski BW, Bartelt RJ, Cossé AA, Petroski RJ (2006) Male-produced aggregation pheromone compounds from the eggplant flea beetle (Epitrix fuscula): identification, synthesis, and field biossays. J Chem Ecol 32:2543–2558

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Karl Vermillion for the NMR analysis (USDA/ARS/NCAUR, Peoria, IL). We thank Robert Bartelt (USDA/ARS/NCAUR, Peoria, IL, retired) for very helpful suggestions towards the structure determination. We thank Miriam Cooperband (USDA/APHIS/PPQ, Otis Laboratory, MA) for the statistical analysis. We are grateful for financial support from the U.S. Department of Agriculture, Forest Service, and Animal & Plant Health Inspective Service (APHIS).

Author information

Authors and Affiliations

  1. USDA, APHIS, PPQ, Otis Laboratory, 1398 W. Truck Rd., Buzzards Bay, MA, 02542-1329, USA

    Allard A. Cossé

  2. USDA/ARS/Nat. Center for Agricultural Utilization Research, 1815 N. University St., Peoria, IL, 61604, USA

    Allard A. Cossé & Bruce W. Zilkowski

  3. Department of Entomology, University of California, Riverside, 3401 Watkins Drive, Riverside, CA, 92521, USA

    Yunfan Zou & Jocelyn G. Millar

  4. USDA Forest Service, Northern Research Station, 3101 Technology Blvd., Ste. F, Lansing, MI, 48910, USA

    Leah Bauer & Therese Poland

Authors
  1. Allard A. Cossé
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bruce W. Zilkowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yunfan Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jocelyn G. Millar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Leah Bauer
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Therese Poland
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Allard A. Cossé.

Ethics declarations

Disclaimer

This article reports the results of research only. Mention of a proprietary product does not constitute an endorsement or a recommendation by the U.S. Department of Agriculture (USDA) for its use. This research was supported [in part] by the intramural research program of the USDA Agricultural Research Service and the USDA Animal and Plant Health Inspection Service, Plant Protection and Quarantine. USDA is an equal opportunity provider and employer.

Electronic Supplementary Material

ESM 1

(DOCX 131 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cossé, A.A., Zilkowski, B.W., Zou, Y. et al. Female-Produced Sex Pheromone of Tetrastichus planipennisi, a Parasitoid Introduced for Biological Control of the Invasive Emerald Ash Borer, Agrilus planipennis. J Chem Ecol 46, 508–519 (2020). https://doi.org/10.1007/s10886-020-01188-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-020-01188-0

Keywords

Search

Navigation