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Unusual Macrocyclic Lactone Sex Pheromone of Parcoblatta

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Unusual Macrocyclic Lactone Sex Pheromone of Parcoblatta Unusual macrocyclic lactone sex pheromone of PNAS PLUS Parcoblatta lata, a primary food source of the endangered red-cockaded woodpecker Dorit Eliyahua,b,1,2, Satoshi Nojimaa,b,1,3, Richard G. Santangeloa,b, Shannon Carpenterc,4, Francis X. Websterc, David J. Kiemlec, Cesar Gemenoa,b,5, Walter S. Leald, and Coby Schala,b,6 aDepartment of Entomology and bW. M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, NC, 27695; cDepartment of Chemistry, College of Environmental Science and Forestry, State University of New York, Syracuse, NY 13210; and dDepartment of Entomology, University of California, Davis, CA 95616 AUTHOR SUMMARY Wood cockroaches in the genus for highly sensitive NMR ex- Parcoblatta, comprising 12 spe- periments, we turned to a home- cies endemic to North America, made preparative GC apparatus are highly abundant in south- (4). In this procedure, each ap- eastern pine forests and repre- plication of an extract into the sent an important prey of the GC column was followed by endangered red-cockaded collection of the pheromone as woodpecker, Picoides borealis. it eluted out of the column. The The broad wood cockroach, procedure we developed allows Parcoblatta lata, is among the the accumulation of successive largest and most abundant of trappings of the pheromone the wood cockroaches, consti- from multiple GC separations. tuting >50% of the biomass of Finally, the trap, containing less the woodpecker’s diet (1). Be- Fig. P1. Field trapping of Parcoblatta species using synthetic than 2 μg of the pheromone, was parcoblattalactone loaded in rubber septa dispensers. The septa were cause reproduction in red- positioned in the center of adhesive-coated traps vertically attached to transferred directly into an cockaded woodpeckers is af- pine trees, and trapping was conducted overnight in a mixed pine- NMR microcapillary tube, using fected dramatically by seasonal hardwood forest at Lake Johnson, Wake County, NC. Six transects of only about 7 μL of solvent. This and spatial changes in arthropod the five treatments were set with traps 12–15 m apart. To evaluate the sample was flown immediately prey availability, monitoring P. species specificity of their sex pheromonal signal, lures baited with from North Carolina State Uni- lata populations could serve as volatile collections of virgin P. lata females were included also. versity to the State University of a useful index of habitat suit- New York in Syracuse, NY for ability for woodpecker conservation and forest management hand-delivery directly to the NMR instrument. The spectra we efforts. Current efforts to assess habitat quality and prey avail- obtained were remarkably clean and permitted us to propose the ability entail exceptional investment in broad-scale monitoring structure of the pheromone as (4Z,11Z)-oxacyclotrideca-4,11- with nonselective traps such as burlap bands on trees or card- dien-2-one [synonym, (3Z,10Z)-dodecadienolide], which we board, pitfall, and light traps. A synthetic sex pheromone of named “parcoblattalactone” because of its origin from Parco- P. lata, a major prey, holds promise as an important economically blatta and its macrocyclic lactone structure. This compound was and ecologically sound tool to monitor the quality and suit- synthesized and was confirmed unambiguously to be the same as ability of foraging habitats for red-cockaded woodpeckers. We the natural pheromone by comparing the two NMR spectra. describe here the identification, synthesis, and confirmation of The male cockroach, however, is the best judge whether we the chemical structure of this pheromone. successfully deciphered its sexual communication code. We first Our previous analysis showed that the sex pheromone is pro- tested the synthetic parcoblattalactone by monitoring the elec- duced in the anterior seven segments of sexually mature virgin trophysiological responses of isolated antennae of adult male females (2). We extracted 1,400 virgin females in hexane, and, ECOLOGY while separating the extract by gas chromatography (GC), we also coupled the effluent of the GC to an isolated male antenna, Author contributions: D.E., S.N., F.X.W., D.J.K., C.G., W.S.L., and C.S. designed research; D.E., which was used as a biological detector (electroantennographic S.N., R.G.S., S.C., F.X.W., D.J.K., W.S.L., and C.S. performed research; S.N., S.C., and F.X.W. contributed new reagents/analytic tools; D.E., S.N., F.X.W., D.J.K., W.S.L., and C.S. analyzed detection; GC-EAD) (3). Sensilla on the male antennae house data; and D.E., S.N., R.G.S., S.C., F.X.W., D.J.K., C.G., W.S.L., and C.S. wrote the paper. highly specialized receptors that are exquisitely sensitive to the The authors declare no conflict of interest. female pheromone. GC-EAD analyses revealed four electro- This article is a PNAS Direct Submission. physiologically active compounds. We concentrated on the most Freely available online through the PNAS open access option. abundant compound, which also stimulated strong behavioral CHEMISTRY 1 responses (upwind running and correct choice in a two-choice D.E. and S.N. contributed equally to this work. 2 maze) from males. Analysis by GC coupled to a mass spec- Present address: Center for Insect Science, University of Arizona, Tucson, AZ 85721. trometer (GC-MS) showed that this compound did not match 3Present address: Shin-Etsu Chemical Co., Ltd. Tokyo, Japan. any of the hundreds of thousands of compounds in the MS li- 4Present address: Department of Chemistry, Yale University, New Haven, CT 06520. brary. Although it gave us important clues as to the molecular 5Present address: Departament de Producció Vegetal i Ciència Forestal, Universitat de formula and its molecular weight, MS was not sufficient to de- Lleida, Lleida, Spain. cipher the full chemical structure. Likewise, infrared spectros- 6To whom correspondence should be addressed. E-mail: [email protected]. copy coupled to the GC yielded some more clues but not the full See full research article on page E490 of www.pnas.org. structure. To obtain a tiny amount of absolutely pure pheromone Cite this Author Summary as: PNAS 10.1073/pnas.1111748109. www.pnas.org/cgi/doi/10.1073/pnas.1111748109 PNAS | February 21, 2012 | vol. 109 | no. 8 | 2705–2706 Downloaded by guest on September 24, 2021 P. lata, Parcoblatta virginica,andParcoblatta pennsylvanica that The Parcoblatta species complex, consisting of 12 species en- were freshly collected in the same pine forest in Raleigh, NC. demic to North America, constitutes excellent material for future Both P. lata and P. virginica responded to as little as ∼0.1 ng of the studies of premating reproductive isolation. The compound we pheromone, but P. pennsylvanica antennae responded only isolated from P. lata attracted males of some other Parcoblatta to very large amounts of parcoblattalactone. These results were species but not others. This observation suggests that Parcoblatta confirmed with traps baited with parcoblattalactone that we species likely use species-specific multicomponent pheromone deployed overnight in a mixed pine-hardwood forest in Raleigh. blends, as do many other insects. Some species that were not Sticky traps baited with 10, 100, and 1,000 ng parcoblattalactone attracted to parcoblattalactone may have greater fidelity to their attracted large numbers of adult males of four Parcoblatta species, multicomponent pheromone blend, or they may use a different most commonly P. lata, P. virginica,andP. caudelli,butnota major component, not parcoblattalactone, in their pheromone single P. pennsylvanica, even though that species was clearly found blend. Interestingly, however, P. virginica and P. caudelli males in this forest (Fig. P1). No immature Parcoblatta were found also were attracted to volatile emissions of P. lata females that on any of the traps; one or two adult females were trapped in contained the full blend of pheromone components. This un- some traps but were found equally in baited and unbaited traps. usual observation suggests that other species-isolating mecha- These results show that parcoblattalactone can attract not nisms may operate in this genus, such as temporal and spatial partitioning of sexual activity of different species within the only P. lata but also several other Parcoblatta species, empha- fi sizing its utility in monitoring several endemic wood cockroach forest. Parcoblatta females also may use species-speci c contact sex pheromones to elicit courtship only from conspecific males. species in red-cockaded woodpecker habitats. This macrocyclic lactone is a previously unidentified natural product and a pre- 1. Hanula JL, Lipscomb D, Franzreb KE, Loeb SC (2000) Diet of nestling red-cockaded viously unknown pheromonal structure for cockroaches, high- woodpeckers at three locations. J Field Ornithol 71:126–134. lighting the great chemical diversity that characterizes olfactory 2. Gemeno C, Snook K, Benda N, Schal C (2003) Behavioral and electrophysiological communication in cockroaches—each long-range sex phero- evidence for volatile sex pheromones in Parcoblatta wood cockroaches. J Chem Ecol 29: fi 37–54. mone identi ed to date from different genera belongs to a dif- 3. Nojima S, Schal C, Webster FX, Santangelo RG, Roelofs WL (2005) Identification of the ferent chemical class. As innovative natural product chemists, sex pheromone of the German cockroach, Blattella germanica. Science 307:1104–1106. cockroaches have undergone adaptive radiations in their sexual 4. Nojima S, Kiemle DJ, Webster FX, Apperson CS, Schal C (2011) Nanogram-scale communication signals, producing highly diverse and often preparation and NMR analysis for mass-limited small volatile compounds. PLoS ONE 6: e18178. unique sexual attractants and consequently fashioning relatively 5. Gemeno C, Schal C (2004) Sex pheromones of cockroaches. Advances in Insect Chemical “private” channels of olfactory communication (5). Ecology, eds Cardé RT, Millar JG (Cambridge Univ Press, Cambridge, UK), pp 179–247. 2706 | www.pnas.org/cgi/doi/10.1073/pnas.1111748109 Eliyahu et al.
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