Abstract
Halyomorpha halys (Stål) (Pentatomidae), called the brown marmorated stink bug (BMSB), is a newly invasive species in the eastern USA that is rapidly spreading from the original point of establishment in Allentown, PA. In its native range, the BMSB is reportedly attracted to methyl (E,E,Z)-2,4,6-decatrienoate, the male-produced pheromone of another pentatomid common in eastern Asia, Plautia stali Scott. In North America, Thyanta spp. are the only pentatomids known to produce methyl 2,4,6-decatrienoate [the (E,Z,Z)-isomer] as part of their pheromones. Methyl 2,4,6-decatrienoates were field-tested in Maryland to monitor the spread of the BMSB and to explore the possibility that Thyanta spp. are an alternate host for parasitic tachinid flies that use stink bug pheromones as host-finding kairomones. Here we report the first captures of adult and nymph BMSBs in traps baited with methyl (E,E,Z)-2,4,6-decatrienoate in central Maryland and present data verifying that the tachinid, Euclytia flava (Townsend), exploits methyl (E,Z,Z)-2,4,6-decatrienoate as a kairomone. We also report the unexpected finding that various isomers of methyl 2,4,6-decatrienoate attract Acrosternum hilare (Say), although this bug apparently does not produce methyl decatrienoates. Other stink bugs and tachinids native to North America were also attracted to methyl 2,4,6-decatrienoates. These data indicate there are Heteroptera in North America in addition to Thyanta spp. that probably use methyl 2,4,6-decatrienoates as pheromones. The evidence that some pentatomids exploit the pheromones of other true bugs as kairomones to find food or to congregate as a passive defense against tachinid parasitism is discussed.
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Aldrich, J. R., Blum, M. S., Lloyd, H. A., and Fales, H. M. 1978. Pentatomid natural products: chemistry and morphology of the III–IV dorsal abdominal glands of adults. J. Chem. Ecol. 4:161–172.
Aldrich, J. R., Kochansky, J. P., and Abrams, C. B. 1984a. Attractant for a beneficial insect and its parasitoids: pheromone of the predatory spined soldier bug, Podisus maculiventris (Hemiptera: Pentatomidae). Environ. Entomol. 13:1031–1036.
Aldrich, J. R., Kochansky, J. P., Lusby, W. R., and Sexton, J. D. 1984b. Semiochemicals from a predaceous stink bug, Podisus maculiventris (Hemiptera: Pentatomidae). J. Wash. Acad. Sci. 74:39–46.
Aldrich, J. R., Lusby, W. R., Kochansky, J. P., and Abrams, C. B. 1984c. Volatile compounds from the predatory insect, Podisus maculiventris (Hemiptera: Heteroptera: Pentatomidae): male and female metathoracic scent gland and female dorsal abdominal gland secretions. J. Chem. Ecol. 10:561–568.
Aldrich, J. R. 1985. Pheromone of a true bug (Hemiptera-Heteroptera): attractant for the predator, Podisus maculiventris, and kairomonal effects, pp. 95–119, in T. E. Acree, and D. M. Soderlund (eds.). Semiochemistry: Flavors and Pheromones. Walter de Gruyter, Berlin.
Aldrich, J. R. 1988a. Chemical ecology of the Heteroptera. Annu. Rev. Entomol. 33:211–238.
Aldrich, J. R. 1988b. Chemistry and biological activity of pentatomoid sex pheromones., pp. 417–431, in H. G. Cutler (ed.). Biologically Active Natural Products for Potential Use in Agriculture. American Chemical Society, Washington, D.C.
Aldrich, J. R., Lusby, W. R., Marron, B. E., Nicolaou, K. C., Hoffmann, M. P., and Wilson, L. T. 1989. Pheromone blends of green stink bugs and possible parasitoid selection. Naturwissenschaften 76:173–175.
Aldrich, J. R., Hoffmann, M. P., Kochansky, J. P., Lusby, W. R., Eger, J. E., and Payne, J. A. 1991. Identification and attractiveness of a major pheromone component for Nearctic Euschistus spp. stink bugs (Heteroptera: Pentatomidae). Environ. Entomol. 20:477–483.
Aldrich, J. R., Numata, H., Borges, M., Bin, F., Waite, G. K., and Lusby, W. R. 1993. Artifacts and pheromone blends from Nezara spp. and other stink bugs (Heteroptera: Pentatomidae). Z. Naturforsch. [C] 48:73–79.
Aldrich, J. R. 1995. Chemical communication in the true bugs and parasitoid exploitation., pp. 318–363, in R. T. Cardé, and W. J. Bell (eds.). Chemical Ecology of Insects. Chapman & Hall, New York.
Aldrich, J. R. and Zhang, A. 2002. Kairomone strains of Euclytia flava (Townsend), a parasitoid of stink bugs. J. Chem. Ecol. 28:1565–1582.
Aldrich, J. R., Khrimian, A., Zhang, A., and Shearer, P. W. 2006. Bug pheromones (Hemiptera: Heteroptera) and tachinid fly host-finding. Denisia 19:1015–1031.
Arnaud Jr., P. H. 1978. A Host–Parasite Catalog of North American Tachinidae (Diptera). United States Department of Agriculture, Washington, D.C.
Chen, X., Gottlieb, L., and Millar, J. G. 2000. Highly stereoselective syntheses of the sex pheromone components of the southern green stink bug Nezara viridula (L.) and the green stink bug Acrosternum hilare (Say). Synthesis 269–272.
Çokl, A., and Virant-Doberley, M. 2003. Communication with substrate-borne signals in small plant-dwelling insects. Annu. Rev. Entomol. 48:29–50.
Cullen, E. M., and Zalom, F. G. 2005. Relationship between Euschistus conspersus (Hem., Pentatomidae) pheromone trap catch and canopy samples in processing tomatoes. J. Appl. Entomol. 129:505–514.
Eger, J. E., and Ables, J. R. 1981. Parasitism of Pentatomidae by Tachinidae in South Carolina and Texas. Southwest. Entomol. 6:28–33.
Endo, N., Wada, T., Nishiba, Y., and Sasaki, R. 2006. Interspecific pheromone cross-attraction among soybean bugs (Heteroptera): does Piezodorus hybneri (Pentatomidae) utilize the pheromone of Riptortus clavatus (Alydidae) as a kairomone? J. Chem. Ecol. 32:1605–1612.
Evans, H. E. 1957. Ethological studies on digger wasps of the genus Astata (Hymenoptera, Sphecidae). J. N. Y. Entomol. Soc. 65:159–185.
Fitzgerald, T. D., St. Clair, A. D., Daterman, G. E., and Smith, R. G. 1973. Slow release plastic formulation of the cabbage looper pheromone cis-7-dodecenyl acetate: release rate and biological activity. Environ. Entomol. 2:607–610.
Gibson, R. M., Aspbury, A. S., and Mcdaniel, L. L. 2002. Active formation of mixed-species grouse leks: a role for predation in lek evolution? Proc. R. Soc. Lond. B Biol. Sci. 269:2503–2507.
Hamilton, W. D. 1971. Geometry for the selfish herd. J. Theor. Biol. 31:295–311.
Hoebeke, E. R., and Carter, M. E. 2003. Halyomorpha halys (Stal) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proc. Entomol. Soc. Wash. 105:225–237.
Jones, W. A., Shepard, B. M., and Sullivan, M. J. 1996. Incidence of parasitism of pentatomid (Heteroptera) pests of soybean in South Carolina with a review of studies in other states. J. Agric. Entomol. 13:243–263.
Khrimian, A. 2005. The geometric isomers of methyl-2,4,6-decatrienoate, including pheromones of at least two species of stink bugs. Tetrahedron 61:3651–3657.
Khrimian, A., Shearer, P. W., Zhang, A., Hamilton, D. W., and Aldrich, J. R. 2006. Field responses of the invasive brown marmorated stink bug, Halyomorpha hayls (Stål) to geometric isomers of methyl 2,4,6-decatrienoate. J. Chem. Ecol., in press.
Mcbrien, H. L., and Millar, J. G. 1999. Phytophagous bugs., pp. 277–304, in R. J. Hardie, and A. K. Minks (eds.). Pheromones of Non-lepidopteran Insects Associated with Agricultural Plants. CAB International Publishing, Wallingford.
Mcbrien, H. L., Millar, J. G., Gottlieb, L., Chen, X., and Rice, R. E. 2001. Male-produced sex attractant pheromone of the green stink bug, Acrosternum hilare (Say). J. Chem. Ecol. 27:1821–1839.
Mcbrien, H. L., Cokl, A., and Millar, J. G. 2002a. Comparison of substrate-borne vibrational signals of two congeneric stink bug species, Thyanta pallidovirens and T. custator accerra (Heteroptera: Pentatomidae). J. Insect Behav. 15:715–738.
Mcbrien, H. L., Millar, J. G., Rice, R. E., Mcelfresh, J. S., Cullen, E., and Zalom, F. G. 2002b. Sex attractant pheromone of the red-shouldered stink bug Thyanta pallidovirens: a pheromone blend with multiple redundant components. J. Chem. Ecol. 28:1797–1818.
Mcpherson, J. E. 1982. The Pentatomoidea of northeastern North America with Emphasis on the Fauna of Illinois. Southern Illinois University Press, Carbondale.
Mehta, C., and Patel, N. 2003. StatXact 6: Statistical Software for Exact Nonparametric Inference. Cytel Software, Cambridge.
Mendel, Z., Assael, F., and Dunkelblum, E. 2004. Kairomonal attraction of predatory bugs (Heteroptera: Anthocoridae) and brown lacewings (Neuroptera : Hemerobiidae) to sex pheromones of Matsucoccus species (Hemiptera : Matsucoccidae). Biol. Control 30:134–140.
Millar, J. 1998. Rapid and simple isolation of zingiberene from ginger essential oil. J. Nat. Prod. 61:1025–1026.
Millar, J. G. 1997. Methyl (2E,4Z,6Z)-deca-2,4,6-trienoate, a thermally unstable, sex-specific compound from the stink bug Thyanta pallidovirens. Tetrahedron Lett. 38:7971–7972.
Millar, J. G., Rice, R. E., Steffan, S. A., Daane, K. M., Cullen, E., and Zalom, F. G. 2001. Attraction of female digger wasps, Astata occidentalis Cresson (Hymenoptera: Sphecidae) to the sex pheromone of the stink bug Thyanta pallidovirens (Hemiptera: Pentatomidae). Pan-Pac. Entomol. 77:244–248.
Millar, J. G., Mcbrien, H. L., Ho, H.-Y., Rice, R. E., Cullen, E., Zalom, F. G., and Üokl, A. 2002. Pentatomid bug pheromones in IPM: possible applications and limitations. Int. Org. Biol. Control Bull. 25:241–250.
Mooring, M. S., and Hart, B. L. 1992. Animal grouping for protection from parasites: selfish herd and encounter-dilution effects. Behaviour 123:173–193.
Moraes, M. C. B., Laumann, R. A., Sujii, E. R., Pires, C. S. S., Borges, M., and Millar, J. G. 2005. Sex attractant pheromone from the neotropical red-shouldered stink bug, Thyanta perditor (F.). J. Chem. Ecol. 31:1415–1427.
Pereira, W., Elpino-Campos, A., Del-Claro, K., and Machado, G. 2004. Behavioral repertory of the neotropical harvestman Ilhaia cuspidata (Opiliones, Gonyleptidae). J. Arachnol. 32:22–30.
Pfannenstiel, R. S., Hunt, R. E., and Yeargan, K. V. 1995. Orientation of a hemipteran predator to vibrations produced by feeding caterpillars. J. Insect Behav. 8:1–9.
Sant’ana, J., Bruni, R., Abdul-Baki, A. A., and Aldrich, J. R. 1997. Pheromone-induced movement of nymphs of the predator Podisus maculiventris (Heteroptera: Pentatomidae). Biol. Control 10:123–128.
Schoene, W. J. 1933. Economic status of the green stink bug with reference to the succession of its wild hosts. J. Agric. Res. 46:863–866.
Stireman, J. O., O’hara, J. E., and Wood, D. M. 2006. Tachinidae: evolution, behavior, and ecology. Annu. Rev. Entomol. 51:525–555.
Sugie, H., Yoshida, M., Kawasaki, K., Noguchi, H., Moriya, S., Takagi, K., Fukuda, H., Fujiie, A., Yamanaka, M., Ohira, Y., Tsutsumi, T., Tsuda, K., Fukumoto, K., Yamashita, M., and Suzuki, H. 1996. Identification of the aggregation pheromone of the brown-winged green bug, Plautia stali Scott (Heteroptera: Pentatomidae). Appl. Entomol. Zool. 31:427–431.
Tada, N., Yoshida, M., and Sato, Y. 2001a. Monitoring of forecasting for stink bugs in apple. 2. The possibility of forecasting with aggregation pheromone. Ann. Rep. Plant Prot. North Jpn. 52:227–229.
Tada, N., Yoshida, M., and Sato, Y. 2001b. Monitoring of forecasting for stink bugs in apple. 1. Characteristics of attraction to aggregation pheromone in Iwate Prefecture. Ann. Rep. Plant Prot. North Jpn. 52:224–226.
Warnaar, F. 1977. Deca-2,4,6-trienoic acid, a new conjugated fatty acid, isolated from the latex of Euphorbial pucherrima Willd. Lipids 12:707–710.
Warnaar, F. 1981. Conjugated fatty acids from latex of Euphorbia lathyris. Phytochemistry 20:89–91.
Watt, P. J., and Chapman, R. 1998. Whirligig beetle aggregations: what are the costs and the benefits? Behav. Ecol. Sociobiol. 42:179–184.
Wcislo, W. T. 1984. Gregarious nesting of a digger wasp a “selfish herd” response to a parasitic fly (Hymenoptera: Sphecidae; Diptera: Sacrophagidae). Behav. Ecol. Sociobiol. 15:157–160.
Wilbur, D. A. 1939. Mass flights of the pentatomid, Thyanta custator (Fabr.) in Kansas. J. Kans. Entomol. Soc. 12:77–80.
Yasuda, T. 2000. Role of semiochemicals in prey-locating behavior of a generalist predatory stink bug, Eocanthecona furcellata (Wolff) (Heteroptera: Pentatomidae). Jpn. Agric. Res. Q. 34:15–20.
Zhang, Q. H., and Aldrich, J. R. 2004. Attraction of scavenging chloropid and milichiid flies (Diptera) to metathoracic scent gland compounds of plant bugs (Heteroptera: Miridae). Environ. Entomol. 33:12–20.
Acknowledgements
We thank T. J. Henry, Systematic Entomology Laboratory (SEL), USDA-ARS, Beltsville, MD, and David Rider, North Dakota State University, Fargo, for identification of pentatomid species, and Norman Woodley, SEL, for identification of tachinids. We are also grateful to Peter Shearer, Rutgers University, Agricultural Research & Extension Center, Bridgeton, NJ, for supplying H. halys, and to John Reese, Department of Entomology, Kansas State University, Manhattan, for helpful discussions and assistance with field work.
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Aldrich, J.R., Khrimian, A. & Camp, M.J. Methyl 2,4,6-decatrienoates Attract Stink Bugs and Tachinid Parasitoids. J Chem Ecol 33, 801–815 (2007). https://doi.org/10.1007/s10886-007-9270-9
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DOI: https://doi.org/10.1007/s10886-007-9270-9