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Male-Produced Pheromone of Spathius agrili, A Parasitoid Introduced For The Biological Control Of The Invasive Emerald Ash Borer, Agrilus planipennis

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Abstract

The braconid wasp, Spathius agrili, has been released in the U.S. as a biocontrol agent for the invasive emerald ash borer (Coleoptera: Buprestidae: Agrilus planipennis), a destructive pest of ash trees (Fraxinus spp.). We identified and synthesized seven male-specific volatile compounds. Three of these, dodecanal, (4R,11E)-tetradecen-4-olide, and (Z)-10-heptadecen-2-one, were the key behaviorally active components in flight tunnel bioassays. Male specificity was demonstrated by gas chromatographic comparison of male and female volatile emissions and whole body extracts. Identifications were aided by coupled gas chromatographic-mass spectrometric (GC-MS) analysis, microchemical reactions, NMR, chiral GC analysis, and GC and MS comparison with authentic standards. Both the racemic and chiral forms of the γ-lactone, as well as both E- and Z-isomers were synthesized. Flight tunnel behavioral tests showed positive male and female S. agrili responses to both natural pheromone and synthetic blends, with upwind flight and landing on the source. Large field-cage tests, using yellow sticky traps baited with pheromone, captured approximately 50 % of the released male and female wasps in 24-h periods. The use of pheromone-baited traps in the field could simplify the current detection method for determining parasitoid establishment (i.e., laboriously felling and peeling ash trees for recovery of S. agrili from infested EAB larvae).

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References

  • Analytical Software. 1998. Statistix for Windows User’s Manual. Analytical Software, Tallahassee, Florida.

  • Attygalle, A. B. 1998. Microchemical techniques, pp. 207–294, in J. G. Millar and K. F. Haynes (eds.), Methods in Chemical Ecology, Volume 1, Chemical Methods. Kluwer, Boston.

    Chapter  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Baker, K. V., Brown, J. M., Hughes, N., Skarnulis, A. J., and Sexton, A. 1991. Mechanical activation of magnesium turnings for the preparation of reactive Grignard reagents. J Org Chem 56:698–703.

    Article  CAS  Google Scholar 

  • Bartelt, R. J., Schaner, A. M., and Jackson, L. L. 1989. Aggregation pheromone components in Drosophila mulleri. A chiral ester and an unsaturated ketone. J Chem Ecol 15:399–411.

    Article  CAS  Google Scholar 

  • Bartelt, R. J., Dowd, P. F., Plattner, R. D., and Weisleder, D. 1990. Aggregation pheromone of driedfruit beetle. Carpophilus hemipterus: Wind-tunnel bioassay and identification of two novel tetraene hydrocarbons. J Chem Ecol 16:1015–1039.

    Article  CAS  Google Scholar 

  • Bauer, L.S., Liu, Houping, Gao, Ruitong, Zhao, and Tonghai. 2006. Egg and larval parasitoids of emerald ash borer from China: potential for biocontrol in North America, pp. 48-49, in V. Mastro, R. Reardon, and G. Parra (comps). Proceedings of the 2005 emerald ash borer research and technology development meeting; 2005 September 26-27; Pittsburgh, PA. FHTET-2005-16. Morgantown, WV: U.S. Department of Agriculture, Forest Service, Forest Health Technology Enterprise Team.

  • Bauer, L.S., Liu, Houping, and Miller, D. 2009. Emerald ash borer biological control: rearing, releasing, establishment, and efficacy of parasitoids, pp. 7-8, in K. A. McManus, K. W. Gottschalk (eds.). Proceedings. 20th U.S. Department of Agriculture interagency research forum on invasive species 2009; 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.

  • Bauer, L.S., Gould, J., Duan, J., and Ulyshen, M. 2011. Emerald ash borer biological control, pp. 70-73, in K. A. McManus, K. W. Gottschalk (eds.). Proceedings. 21st U.S. Department of Agriculture interagency research forum on invasive species 2010; 2010 January 12-15; Annapolis, MD. Gen. Tech. Rep. NRS-P-75. Newtown Square, PA: U.S. Department of Agriculture, Forest Service, Northern Research Station.

  • Bloch, R. and Brillet, C. 1991. Selective oxidation of primary-secondary diols to lactones catalyzed by tetrapropylammonium perruthenate. Synlett 1991:829–830.

    Article  Google Scholar 

  • Collatz, J., Tolasch, T., Johannes, L., and Steidle, M. 2009. Mate finding in the parasitic wasp Cephalonomia tarsalis (Ashmead): more than one way to a female’s heart. J Chem Ecol 35:761–768.

    Article  PubMed  CAS  Google Scholar 

  • Cooperband, M., Cossé, A., Hartness, A., and Mastro, V.C. 2011. Color preferences of Spathius agrili, a parasitoid of emerald ash borer. Poster presentation at: 2011 Emerald Ash Borer research and technology development meeting; 2011 October 12-13; Wooster, OH.

  • Cossé, A. A., Bartelt, R. J., James, D. G., and Petroski, R. J. 2001. Identification of a female-specific, antennally active volatile compound of the currant stem girdler. J Chem Ecol 27:1841–1853.

    Article  PubMed  Google Scholar 

  • Cossé, A. A., Petroski, R. J., Zilkowski, B. W., Lelito, J. P., and Gould, R. J. 2011. Pheromones of Spathius agrili and S. floridanus: Exotic and native parasitoids of the invasive emerald ash borer. Poster presented at: 27th Meeting of the International Society of Chemical Ecology, 24-28 July 2011; Vancouver, B.C., Canada.

  • El-Sayed, A. M., Gödde, J., and Arn, H. 1999. Sprayer for quantitative application of odor stimuli. Environ Entomol 28:947–953.

    Google Scholar 

  • El-sayed, A.M. 2011. The Pherobase: Database of Pheromones and Semiochemicals. (http://www.pherobase.com)

  • Emerald Ash Borer Info 2011. (http://emeraldashborer.info)

  • Haack, R. A., Jendek, E., Liu, H., Marchant, K. R., Petrice, T. R., Poland, T. M., and Ye, H. 2002. The emerald ash borer: A new exotic pest in North America. Newsletter Michigan Entomol Soc 47:1–5.

    Google Scholar 

  • Hijfte, L. V., Little, R. D., Petersen, J. L., and Moeller, K. D. 1987. Intramolecular 1,3-diyl trapping reactions. Total synthesis of (±)-hypnophilan and (±)-coriolin. Formation of the trans-fused bicycle[3.3.0]octane ring system. J Org Chem 52:4647–4661.

    Article  Google Scholar 

  • James, D. G., Petroski, R. J., Cossé, A. A., Zilkowski, B. W., and Bartelt, R. J. 2003. Bioactivity, synthesis, and chirality of the sex pheromone of currant stem girdler, Janus integer. J Chem Ecol 29:2189–2199.

    Article  PubMed  CAS  Google Scholar 

  • Keeling, C., Plettner, E., and Slessor, K. N. 2004. Hymenopteran Semiochemicals. Topics Curr Chem 239:133–177.

    Article  CAS  Google Scholar 

  • Kuklev, D. V. and Smith, W. L. 2006. Chemical C2-elongation of polyunsaturated fatty acids. Chem Phys Lipids 144:172–177.

    Article  PubMed  CAS  Google Scholar 

  • Leal, W. S., Kuwahara, S., Ono, M., and Kubota, S. 1996. (R, Z)-7,15-hexadecadien-4-olide, sex pheromone of the yellowish elongate chafer, Heptophylla picea. Bioorg Med Chem 4:315–321.

    Article  PubMed  CAS  Google Scholar 

  • de Marques, F. A., McElfresh, J. S., and Millar, J. G. 2000. Kováts retention indexes of monounsaturated C12, C14, and C16 alcohols, acetates and aldehydes commonly found in lepidopteran pheromone blends. J Braz Chem Soc 11:592–599.

    Article  CAS  Google Scholar 

  • Miyashita, M., Yoshikoshi, A., and Grieco, P. A. 1977. Pyridinium-p-toluenesulfonate. A mild and efficient catalyst for the tetrahydro-pyranylation of alcohols. J Org Chem 42:3772–3774.

    Article  CAS  Google Scholar 

  • Paddon-Jones, G. C., Moore, C. J., Breckneil, D. J., König, W. A., and Kitching, W. 1997. Synthesis and absolute stereochemistry of Hagen’s-gland lactones in some parasitic wasps (Hymenoptera: Braconidae). Tett Lett 38:3479–3482.

    Article  CAS  Google Scholar 

  • Petroski, R. J. 2003a. Preparation of monotetrahydropyranylated short-chain symmetrical diols. Syn Commun 33:3251–3259.

    Article  CAS  Google Scholar 

  • Petroski, R. J. 2003b. Oxidation of monotetrahydropyranylated short-chain symmetrical diols. Syn Commun 33:3243–3250.

    Article  CAS  Google Scholar 

  • Quimio, G. M. and Walter, G. H. 2000. Swarming, Delayed Sexual Maturation of Males, and Mating Behavior of Fopius arisanus (Sonan) (Hymenoptera: Braconidae). J Insect Behav 13:797–813.

    Article  Google Scholar 

  • Ray, A.M., Swift, I.P., McElfresh, J.S., Alten, R.L., and Millar, J.G. 2011. (R)-Desmolactone, female-produced sex pheromone component of Desmocerus californicus, a longhorned beetle in the subfamily Lepturinae. Presentation presented at: 27th Meeting of the International Society of Chemical Ecology, 24-28 July 2011; Vancouver, B.C., Canada.

  • Ruther, J., Stahl, L. M., Steiner, S., Garbe, L. A., and Tolasch, T. 2007. A male sex pheromone in a parasitic wasp and control of the behavioral response by the female’s mating status. J Exp Biol 210:2163–2169.

    Article  PubMed  CAS  Google Scholar 

  • Schaner, A. M. and Jackson, L. L. 1992. (Z)-10-heptadecen-2-one and other 2-ketones in the aggregation pheromone blend of Drosophila martensis, D. buzzatii, and D. serido. J Chem Ecol 18:53–64.

    Article  CAS  Google Scholar 

  • Trost, B. M., Ball, Z. T., and Jőge 2002. A chemoselective reduction of alkynes to (E)-alkenes. J Am Chem Soc 124:7922–7923.

    Article  PubMed  CAS  Google Scholar 

  • WILEY 2005. Wiley. Spectral Library, [CD-ROM], 7th ed. Wiley, New York.

    Google Scholar 

  • Williams, H. J., Wong, M., Wharton, R. A., and Vinson, S. B. 1988. Hagen's gland morphology and chemical content analysis for three species of parasitic wasps (Hymenoptera: Braconidae). J Chem Ecol 14:1727–1736.

    Article  CAS  Google Scholar 

  • Willy, W. E., McKean, D. R., and Garcia, B. A. 1976. Conversion of alkyl chlorides to bromides, selective reactions of mixed bromochloroalkanes, and halogen exchange. Bull Chem Soc Jpn 49(7):1989–1995.

    Article  CAS  Google Scholar 

  • Yang, Z. Q., Strazanac, J. S., Marsh, P. M., Van Achterberg, C., and Choi, W. Y. 2005. First recorded parasitoid from China of Agrilus planipennis: A new species of Spathius (Hymenoptera: Braconidae: Doryctinae). Ann Entomol Soc Am 98:636–642.

    Article  Google Scholar 

  • Yang, Z. Q., Wang, X. Y., Gould, J. R., Reardon, R. C., Zhang, Y. N., Liu, G. J., and Liu, E. S. 2010. Biology and behavior of Spathius agrili, a parasitoid of the emerald ash borer, Agrilus planipennis, in China. J Ins Sci 10:1–13.

    Google Scholar 

  • Zilkowski, B. W., Bartelt, R. J., Cossé, A. A., and Petroski, R. J. 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  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Kyle Schmitt for technical assistance (USDA/ARS/Natl. Center for Agricultural Utilization Research, Peoria, IL). We are grateful for financial support from the U.S. Department of Agriculture, Forest Service, and Animal & Plant Health Inspective Service (APHIS). Mention of trade names or commercial products in this article is solely for the purpose of providing specific information, and does not imply recommendation or endorsement by the U.S. Department of Agriculture. USDA is an equal opportunity provider and employer.

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Authors and Affiliations

  1. USDA-ARS, Natl. Center for Agricultural Utilization Research, 1815 N. University St, Peoria, IL, 61604, USA

    Allard A. Cossé, Richard J. Petroski, Bruce W. Zilkowski & Karl Vermillion

  2. USDA-APHIS-PPQ, Emerald Ash Borer - Biological Control, 5936 Ford Court Suite 200, Brighton, MI, 48116, USA

    Jonathan P. Lelito

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

    Miriam F. Cooperband & Juli R. Gould

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  1. Allard A. Cossé
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  2. Richard J. Petroski
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  3. Bruce W. Zilkowski
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  4. Karl Vermillion
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  5. Jonathan P. Lelito
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  6. Miriam F. Cooperband
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  7. Juli R. Gould
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Correspondence to Allard A. Cossé.

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Cossé, A.A., Petroski, R.J., Zilkowski, B.W. et al. 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, 389–399 (2012). https://doi.org/10.1007/s10886-012-0101-2

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