Biologically Active Natural Products - American Chemical Society

Chapter 28

Chemistry and Biological Activity of Pentatomoid Sex Pheromones Jeffrey R. Aldrich

Downloaded by CORNELL UNIV on May 19, 2017 | http://pubs.acs.org Publication Date: November 28, 1988 | doi: 10.1021/bk-1988-0380.ch028

Insect and Nematode Hormone Laboratory, Beltsville Agricultural Research Center, Agricultural Research Service, U.S. Department of Agriculture, Beltsville, MD 20705

The Pentatomoidea include devastating pests, as well as beneficial predators. In the pest, Nezara viridula, males liberate a long-range attractant pheromone containing a trans-epoxide of (Z)-α-bisabolene as the major component, and in Eurygaster integriceps, vanillin and ethyl acrylate from males attract nearby females after the bugs migrate to wheat fields. Males of an African cotton pest, Sphaerocoris annulus, emit a blend of (Z)- and (E)-4,8-nonadienal, (Z)-4-nonenal, and nonanal that is probably an attractant pheromone. In the cottonseed-feeding Tectacoris diophthalmus, males that have not found females produce a crystalline deposit of 3,5-dihydroxy-4-pyrone which may be an aphrodisiac and/or an attractant. Pheromones attractive to flying adults have been identified from male predaceous pentatomids (Asopinae) in the genus Podisus and artificially mimicked; R-(+)-α-terpineol, (E)-2-hexenal, and benzyl alcohol for P. maculiventris, S-(+)-linalool, (E)-2-hexenal, and benzyl alcohol for P. fretus. Antipodes of chiral monoterpenols are inactive but not inhibitory, and the pheromones are not mutually inhibitory. A complex of parasitoids use these pheromones to locate hosts. Males of 5 other asopine species that prey upon pestiferous beetles yield pheromones comprised of 6,10,13-trimethyltetradecanol and/or the isovalerate ester of this alcohol. On t h e n i g h t o f October 14, 1939, a high school f o o t b a l l game i n Kansas was invaded by s t i n k bugs: " S p e c t a t o r s were f i r s t made aware of t h e i r presence by t h e d i n caused by the w h i r r i n g o f w i n g s . . . T h e band l o c a t e d i n the b e s t l i g h t e d p o r t i o n o f the stands had t o move i m m e d i a t e l y . The o f f e n s i v e s t i n k b u g smell permeated the neighborhood, e s p e c i a l l y a f t e r s p e c t a t o r s and p l a y e r s had c r u s h e d This chapter not subject to U.S. copyright Published 1988 American Chemical Society

Cutler; Biologically Active Natural Products ACS Symposium Series; American Chemical Society: Washington, DC, 1988.


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the bugs w i t h t h e i r shoes and c l o t h i n g . By the time the game was o v e r . . . t h e bugs were from 1 1/2 t o 3 1/2 inches d e e p " U ) . This b i z a r r e account of a Thyanta s p e c i e s i n d i c a t e s t h a t pentatomids, a l i a s s t i n k bugs, are not o n l y c h e m i c a l l y v i l e , but a l s o v a g i l e . The Pentatomidae and a l l i e d groups such as s h i e l d bugs ( S c u t e l l e r i d a e ) comprise the s u p e r f a m i l y Pentatomoidea. T h e i r s t i n k s are t y p i c a l l y m i x t u r e s of n - a l k a n e s , Cg, C Q , and C^o a l k - 2 - e n a l s , 4 - o x o - a l k e n a l s and, Tn a d u l t s , a l k e n y l a c e t a t e s . These o d o r i f e r o u s s e c r e t i o n s are e x p e l l e d from t h o r a c i c glands i n a d u l t s and abdominal glands i n immatures when the i n s e c t s are a t t a c k e d [2). B e s i d e s t h e i r n o t o r i o u s chemical f o r t i f i c a t i o n , pentatomoids c h a r a c t e r i s t i c a l l y possess h y p o d e r m i c - 1 i k e mouthparts w i t h which they p i e r c e and suck the sap of d e v e l o p i n g f r u i t s o r , i n the case of p r e d a t o r y s p e c i e s , the b l o o d of p r e y . The most v a l u a b l e p o r t i o n of a crop may be s e v e r e l y damaged and exposed t o d i s e a s e , y e t the i n i t i a l i n j u r y i s often inconspicuous. T h i s s u b t l e a s s a u l t , combined w i t h the m o b i l i t y of a d u l t bugs, make pentatomoids d i f f i c u l t to d e t e c t and c o n t r o l . A t f i r s t r e s e a r c h e r s i n search of sex pheromones f o r H e t e r o p t e r a suspected t h a t s t i n k gland e s t e r s were a t t r a c t a n t s ( 3 ) . However, i n the Pentatomoidea (and probably most H e t e r o p t e r a ) thTs i s not so. In f a c t , the chemical barrage from the s t i n k glands confounds the task of i s o l a t i n g the t r u e sex pheromones. I t i s now e v i d e n t t h a t a v a r i e t y o f pheromone glands have e v o l v e d i n d e p e n d e n t l y i n male pentatomoids. In some of the predaceous s t i n k bugs ( A s o p i n a e ) , m a l e - s p e c i f i c pheromone glands are e x t r a o r d i n a r i l y l a r g e and produce copious amounts of s e c r e t i o n . Though l e s s than a t e n t h of the over 2500 s p e c i e s o f Pentatomidae are predaceous, the extreme r e l i a n c e of asopines on pheromones has f a c i l i t a t e d r e s e a r c h on these s p e c i e s . T h e r e f o r e , the sex pheromone c h e m i s t r y and b i o l o g i c a l a c t i v i t y of Asopinae w i l l be d i s c u s s e d f i r s t as a framework f o r the ensuing d i s c u s s i o n s of the meager data f o r s c u t e l l e r i d and phytophagous pentatomid sex pheromones. Data on the u s u r p a t i o n of pentatomoid sex pheromones and l a r v a l s t i n k g l a n d s e c r e t i o n s by p a r a s i t o i d s as h o s t - f i n d i n g kairomones are a l s o included. Asopinae Males i n the genera P o d i s u s , A l c a e o r r h y n c h u s , and Z i c r o n a have huge pheromone glands opening underneath the wings (4,ÇJ~. A w e l l - f e d P o d i s u s male may c o n t a i n over a m i l l i g r a m of pheromone i n h i s d o r s a l abdominal glands (DAGs) and can s e l e c t i v e l y r e l e a s e the f r a g r a n t s e c r e t i o n to c a l l a mate (6). In the two s y m p a t r i c s p e c i e s of P o d i s u s t h a t have been i n v e s t i g a t e d , m a c u l i v e n t r i s ( c a l l e d the s p i n e d s o l d i e r bug) and £ . f r e t u s , the DAG s e c r e t i o n s each c o n t a i n ( E ) - 2 - h e x e n a l ( I ) and benzyl a l c o h o l ( I I ) as major c o n s t i t u e n t s , but d T f f e r i n t h e i r major monoterpenol component ( F i g u r e 1 ) . j*-( + ) - a - T e r p i n e o l (V) i s the p r i n c i p a l monoterpenol i n the pheromone o f the s p i n e d s o l d i e r bug and S - ( + ) - l i n a l o o l ( I I I ) i s the predominant terpene i n t h e T r e t u s pheromone but, i n t e r e s t i n g l y , the major monoterpenol of each s p e c i e s occurs as a minor c o n s t i t u e n t i n i t s s i b l i n g s p e c i e s ' pheromone ( Λ 8 ) . Other minor components ( and C^g normal h y d r o c a r b o n s , U ) - a - b i s a b o l e n e ( X V I I ) , and a t r a n s - e p o x i d e ( X V I I I ) o f the s e s q u i t e r p e n e hydrocarbon ( 4 4 ) . The l a t t e r compound was the predominant component and the s t e r e o c h e m i s t r y of the n a t u r a l p r o d u c t was a s s i g n e d based on the b i o a s s a y a c t i v i t i e s of s y n t h e t i c diastereomers (44). Southern green s t i n k bug males from t h e U.S. r e l e a s e XVIII (and/or the a n t i p o d e ) and the c i s - i s o m e r XIX (15%) (and/or the a n t i p o d e ) , p l u s the C13 (2.3%) and ( ^ 9 (7.4%) a l k a n e s , and 1.4% n e r o l i d o l ( V I I ) ( 4 2 ) . Male N. v i r i d u l a from F r a n c e resemble the U.S. s t r a i n of the bug i n e m i t t i n g both X V I I I and XIX ( c a . 2:1 r a t i o ) ( 4 4 ) . T h e r e f o r e , i t appears t h a t d i f f e r e n t pheromone s t r a i n s of ÎN. v i r i d u l a e x i s t ( 4 2 ) . C o n c l u d i n g Remarks Males of many predaceous s t i n k bugs have m a s s i v e , w e l l - d e f i n e d e x o c r i n e glands t h a t s e c r e t e a t t r a c t a n t pheromones. Some p l a n t - f e e d i n g s c u t e l l e r i d s a l s o have obvious pheromone-1ike glands as do the Asopinae ( 2 0 ) , but i n most phytophagous pentatomoids e x o c r i n e gland c e l l s are s c a t t e r e d i n the c u t i c u l a r e p i d e r m i s and t h e i r excess i n males i s o n l y apparent upon h i s t o l o g i c a l e x a m i n a t i o n (39). In s p e c i e s l a c k i n g pheromone glands t h a t can be d i s s e c t e d from the bugs, a e r a t i o n i s the b e s t method f o r pheromone i s o l a t i o n . T h i s approach i s f r a u g h t w i t h the d i f f i c u l t y of h e r d i n g bugs i n t o a s u i t a b l e apparatus w i t h o u t e l i c i t i n g a d e f e n s i v e chemical d i s c h a r g e . Moreover, pentatomoids f r e q u e n t l y h i b e r n a t e or a e s t i v a t e as a d u l t s b e f o r e r e p r o d u c i n g , and d i a p a u s i n g males o f v i r i d u l a (and p r o b a b l y males of o t h e r s p e c i e s ) do not produce pheromone ( 4 5 ) . N e v e r t h e l e s s , m a l e - s p e c i f i c blends have been i s o l a t e d v i a a i r b o r n e t r a p p i n g f o r economically important E u s c h i s t u s , Acrosternum, T h y a n t a , and M u r g a n t i a s p e c i e s ( A l d r i c h , J . R.; Hoffmann, M. P., unpublished data). S t i n k bug damage i s o f t e n u n p r e d i c t a b l e because pentatomoids are s t r o n g f l i e r s U ,46,47) t h a t h a p h a z a r d l y invade c r o p s . T h e r e f o r e , pheromone-baited t r a p s f o r p e s t s p e c i e s may be u s e f u l i n d e t e c t i n g i n c i p i e n t i n f e s t a t i o n s . Beyond t h i s now c o n v e n t i o n a l use o f pheromones, d e c i p h e r i n g the chemical communication systems of



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1985 F i g u r e 3. Nezara v i r i d u l a a d u l t s ( c u m u l a t i v e ) and t a c h i n i d p a r a s i t o i d s ( d a i l y ) caught i n t r a p s deployed i n L o u i s i a n a b a i t e d w i t h a i r b o r n e - t r a p p e d v o l a t i l e s from H. v i r i d u l a males l a b o r a t o r y - r e a r e d i n M a r y l a n d . ( R e p r i n t e d from r e f . 42.)



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harmful and beneficial pentatomoids could lead to improved biological control in a variety of ways. Nezara vjridula has recently invaded the Sacramento Valley in California (32). The knowledge that at least some parasitoids home in on the Nezara attractant pheromone and that this pheromone differs between geographically isolated populations, may temper decisions as to where to seek parasitoids for establishment in California (Hoffmann, M. P., University of California at Davis, personal communication, 1987). A novel use for synthetic pheromones of the southern green stink bug and other exotic pentatomoid pests would be their implementation as artificial kairomones to collect the parasitoids needed for biological control. Similarly, synthetic pheromones of Asopinae might be used to collect exotic predators for biological control programs (17). Native asopines could be augmented and conserved in agroecosystems by the judicious application of artificial pheromones. This approach may be an economically favorable means to tap the vast reservoir of predaceous heteropterans, especially if attractants are discovered for more species from other taxa and found not to be mutually inhibitory. Better biocontrol through chemistry would be a propitious welcome to the next millennium. Acknowledgments The author thanks Dr. Larry Douglas, ARS Consulting Statistician, University of Maryland, for statistical analysis, and Susan Wilzer for technical assistance. Mention of commercial products does not constitute an endorsement by the U.S. Department of Agriculture. Literature Cited 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12.

Wilbur, D. A. J. Kans. Entomol. Soc. 1939, 12, 77-80. Aldrich, J. R. Ann. Rev. Entomol. 1988, 33, 211-38. Aldrich, J. R. In Semiochemistry: Flavors and Pheromones; Acree, T. E.; Soderlund, D. M., Eds.; de Gruyter: Berlin, 1985; pp 95-119. Aldrich, J. R.; Blum, M. S.; Lloyd, H.; Fales, H. M. J. Chem. Ecol. 1978, 4, 161-72. Dupuis, C. Bull. Soc. Nat. (Paris) 1952, 7, 1-4. Aldrich, J. R.; Kochansky, J. P.; Abrams, C. B. Environ. Entomol. 1984, 13, 1031-6. Aldrich, J. R.; Lusby, W. R.; Kochansky, J. P. Experientia 1986, 42, 583-5. Rudmann, Α. Α.; Aldrich, J. R. J. Chromatogr. 1987, 407, 324-9. Evans, E. W. Ecology 1982, 63, 147-58. McPherson, J. E. The Pentatomoidea (Hemiptera) of Northeastern North America; Southern Illinois University Press: Carbondale, 1982. Turnipseed, S.; Kogan, M. In Natural Enemies of Arthropods in Soybean; Pitre, H. Ν., Ed.; South Carolina Agr. Exp. Stn.: Southern Cooperative Series Bull No. 285, 1983; pp 1-6. Aldrich, J. R.; Lusby, W. R.; Kochansky, J. P.; Abrams, C. B. J. Chem. Ecol. 1984, 10, 561-8.



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13. Aldrich, J. R.; Kochansky, J. P.; Lusby, W. R.; Sexton, J. D. J. Wash. Acad. Sci. 1984, 74, 39-46. 14. Orr, D. B.; Russin, J. S.; Boethel, D. J. Can. Entomol. 1986, 118, 1063-72. 15. Eger Jr., J. E.; Ables, J. R. Southwestern Entomol. 1981, 6, 28-33. 16. Ward, J. P.; VanDorp, D. A. Recueil 1969, 88, 989-93. 17. Aldrich, J. R.; Lusby, W. R. Comp. Biochem. Physiol. 1986, 85B, 639-42. 18. Clausen, C. P. Introduced Parasites and Predators of Arthropod Pests and Weeds: A World Review; U. S. Department of Agriculture, U. S. Government Print Office: Washington, DC, 1978; pp 23-6. 19. Aldrich, J. R.; Oliver, J. E.; Lusby, W. R.; Kochansky, J. P. Arch. Insect Biochem. Physiol. 1986, 3, 1-12. 20. Carayon, J. Ann. Soc. Entomol. Fr. 1984, 20, 113-34. 21. Oetting, R. D.; Yonke, T. R. Ann. Entomol. Soc. Am. 1975, 68, 659-62. 22. Evans, E. W.; Root, R. B. Ann. Entomol. Soc. Am. 1980, 73, 270-4. 23. Ubik, K.; Vrkoc, J.; Zdarek, J.; Kontev, C. Naturwissenschaften 1975, 62, 348. 24. Vrkoc, J.; Ubik, K.; Zdarek, J.; Kontev, C. Acta Entomol. Bohemoslov. 1977, 74, 205-6. 25. Zdarek, J.; Kontev, C. Acta Entomol. Bohemoslov. 1975, 72, 239-48. 26. Slater, J. Α.; Baranowski, R. M. How To Know The True Bugs; Wm. C. Brown Co.: Dubuque, Iowa, 1978; p 43. 27. Knight, D. W.; Staddon, B. W.; Thorne, M. J. Z. Naturforsch. Teil C 1985, 40, 851-3. 28. Staddon, B. W.; Thorne, M. J.; Knight, D. W. Aust. J. Zool. 1987, 35, 227-34. 29. Gough, A. J. E.; Hamilton, J. G. C.; Games, D. E.; Staddon, B. W. J. Chem. Ecol. 1985, 11, 343-52. 30. Hamilton, J. G. C., Gough, A. J. E.; Staddon, B. W.; Games, D. E. J. Chem. Ecol. 1985, 11, 1399-409. 31. Gough, A. J. E.; Games, D. E.; Staddon, B. W.; Knight, D. W.; Olagbemiro, T. O. Z. Naturforsch. Teil C 1986, 41, 93-6. 32. Hoffmann, M. P.; Wilson, L. T.; Zalom, F. G. California Agriculture 1987, 41, 4-6. 33. Mitchell, W. C.; Mau, R. F. L. J. Econ. Entomol. 1971, 64, 856-9. 34. Alcock, J. Psyche 1971, 78, 215-28. 35. Harris, V. E.; Todd, J. W. Entomol. Exp. Appl. 1980, 27, 117-26. 36. Moriya, S.; Shiga, M. Appl. Entomol. Zool. 1984, 19, 317-22. 37. Hibino, Y. J. Ethol. 1985, 3, 123-9. 38. Hibino, Y. J. Ethol. 1986, 4, 91-5. 39. Carayon, J. C. R. Acad. Sci. Ser. III 1981, 292, 867-70. 40. Borges, M.; Jepson, P. C.; Howse, P. E. Entomol. Exp. Appl. 1987, 44, 205-212. 41. Pavis, C.; Malosse, C. C. R. Acad. Sci. Ser. III 1986, 303, 273-6.


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42. Aldrich, J. R.; Oliver, J. E.; Lusby, W. R.; Kochansky, J. P.; Lockwood, J. A. J. Exp. Zool. 1987, 244, in press. 43. Pavis, C. Ph.D. Thesis, Universite de Paris-Sud Centre d'Orsay, France, 1986; pp 92-99. 44. Baker, R.; Borges, M.; Cooke, N. G.; Herbert, R. H. Chem. Commun. 1987, 414-16. 45. Brennan, B. M.; Chang, F.; Mitchell, W. C. Environ. Entomol. 1977, 6, 167-73. 46. Hokkanen, H. Ann. Entomol. Fenn. 1986, 52, 28-31. 47. Moriya, S. Appl. Entomol. Zool. 1987, 22, 19-24. 1,1988


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