Antennal Responses of the Western Pine Beetle, Dendroctonus Brevicomis
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378.qxd 10/30/2007 6:36 PM Page 209 Chemoecology 17: 209–221 (2008) 0937-7409/07/040209-13 CHEMOECOLOGY © Birkhäuser Verlag, Basel, 2007 DOI 10.1007/s00049-007-0378-8 Antennal responses of the western pine beetle, Dendroctonus brevicomis (Coleoptera: Curculionidae), to stem volatiles of its primary host, Pinus ponderosa, and nine sympatric nonhost angiosperms and conifers William P. Shepherd1, Dezene P. W. Huber2, Steven J. Seybold3, and Christopher J. Fettig4 1Southern Pine Beetle: Ecology, Behavior, and Management, Southern Research Station, USDA Forest Service, 2500 Shreveport Highway, Pineville, LA 71360 USA 2Natural Resources and Environmental Studies Institute, Ecosystem Science and Management Program, University of Northern British Columbia, 3333 University Way, Prince George, BC V2N 4Z9 Canada 3Chemical Ecology and Management of Forest Insects, Pacific Southwest Research Station, USDA Forest Service, 720 Olive Drive, Ste. D., Davis, CA 95616 USA 4Chemical Ecology and Management of Forest Insects, Pacific Southwest Research Station, USDA Forest Service, 1107 Kennedy Place, Ste 8, Davis, CA 95616 USA Summary. Stem volatile extracts from ten trees that are verbenone was identified from a number of nonhost sympatric with the western pine beetle, Dendroctonus brevi- conifers; and chalcogran was identified from P. tremuloides. comis LeConte (Coleoptera: Curculionidae) were assayed The number of nonhost volatile chemicals that D. brevi- by gas chromatographic-electroantennographic detection comis encounters and is capable of detecting, and the diver- analysis (GC-EAD). The extracts were from the primary sity of sources from which they emanate, highlight the host, ponderosa pine, Pinus ponderosa Dougl. ex Laws. complexity of the olfactory environment in which D. brevi- (Pinaceae); two nonhost angiosperms, California black oak, comis forages. This provides a basis for further work related Quercus kelloggii Newb. (Fagaceae), and quaking aspen, to chemically-mediated aspects of foraging in this insect and Populus tremuloides Michx. (Salicaceae); and seven non- perhaps other coniferophagous bark beetles, and highlights host conifers, white fir, Abies concolor (Gord. & Glend.) the need to consider foraging context in the design and Lindl. ex Hildebr. (Pinaceae), incense cedar, Calocedrus implementation of semiochemical-based management tac- decurrens (Torr.) Florin (Cupressaceae), Sierra lodgepole tics for tree protection. pine, P. contorta murrayana Grev. & Balf. (Pinaceae), Jeffrey pine, P. jeffreyi Grev. & Balf. (Pinaceae), sugar pine, Key words. Insecta – Coleoptera – Curculionidae – P. lambertiana Dougl. (Pinaceae), Douglas-fir, Pseudotsuga Scolytinae – chemical ecology – dispersal – kairomone – menziesii (Mirb.) Franco (Pinaceae), and mountain hemlock, optimal foraging – pheromone – synomone Tsuga mertensiana (Bong.) Carr. (Pinaceae). Sixty-four compounds were identified from the ten trees, 42 of which elicited antennal responses in D. brevicomis, usually in both sexes. In addition, several synthetic compounds, including a Introduction number of the antennally-active compounds from the extracted trees and some bark beetle pheromone compo- After spending the entire immature portion of their life cycle nents, elicited antennal responses in a manner similar to that under the bark of a host tree, newly emerged adult bark beetles observed with the extracts. Of the antennally-active com- (Coleoptera: Curculionidae) leave the protection of the brood pounds known to be present in trees sympatric with D. bre- host and search for a new host in which to reproduce vicomis, only geraniol was unique to its host. Four (Rudinsky 1962). The diverse mixture of trees present in the antennally-active compounds were found in the host and in foraging area of most bark beetles, combined with the rela- other conifers; five compounds were found only in nonhost tively narrow host range of many of these insects (Wood 1982) conifers; eight compounds were found in either or both of and the high costs associated with mistakes (Atkins 1966), the nonhost angiosperms; eight compounds were found in implies that they should be able to detect and respond to olfac- either or both of the angiosperms and in nonhost conifers, tory cues from potential hosts and nonhosts in their foraging but not in the host; and 19 were found in both the host and area in order to successfully and efficiently locate new hosts. in angiosperms and/or nonhost conifers. Several bark beetle Since foraging adult bark beetles maintain very limited energy pheromone components were found in the stem volatile reserves (Atkins 1969) and are highly susceptible to predation extracts. Conophthorin was identified from both nonhost (Stephen & Dahlsten 1976; Dahlsten 1982) and abiotic condi- angiosperms; exo-brevicomin was identified in A. concolor; tions (McMullen & Atkins 1962; Gries et al. 1989) during dis- persal, there are clear advantages to discriminating among Correspondence to: Dezene Huber, email: [email protected] hosts and nonhosts from a distance. 378.qxd 10/30/2007 6:36 PM Page 210 210 W. P. Shepherd et al. CHEMOECOLOGY The ability of coniferophagous bark beetles to detect that other antennally-active compounds have not yet been and respond to volatiles known to emanate from host and tested in the field against this insect. In addition, it is possi- nonhost trees has been well-researched for a number of ble that some nonhost conifer volatiles (NCVs) may also be species (Lanne et al. 1987; Byers 1995; Zhang & Schlyter behaviorally-active in this insect. In order to determine 2004; Seybold et al. 2006). There is significant evidence accurately which compounds might play a role in this that coniferophagous bark beetles are capable of responding insect’s foraging behavior, we explored D. brevicomis in flight to complex mixtures of synthetic nonhost antennal responses to the stem volatiles of its primary host, angiosperm volatiles (NAVs) (Dickens et al. 1992; Wilson to the stem volatiles of seven nonhost conifers and two non- et al. 1996; Borden et al. 1997; Byers et al. 1998; Deglow host angiosperms, and to 23 synthetic plant volatiles and & Borden 1998a,b; Poland et al. 1998; Huber et al. 1999; bark beetle pheromone components. The results of this 2000a,b; 2001; Zhang et al. 1999a,b; 2000; 2001; 2002; study provide a comprehensive list of plant-derived com- Poland & Haack 2000; Huber 2001; Huber & Borden pounds that may be further tested for their behavioral effects 2001a,b; 2003; Jactel et al. 2001; Zhang 2001; 2003; Zhang on this important forest pest (Miller & Keen 1960; Furniss & Schlyter 2003; Fettig et al. 2005). Although foraging bark & Carolin 1977). beetles also land on and directly test hosts and nonhosts by taste or close-range olfaction (Elkinton & Wood 1980; Moeck et al. 1981), the ability to detect and avoid nonhosts Materials and Methods without landing reduces the likelihood of negative inter- actions between foraging bark beetles and various general- Collection and handling of beetles and host/nonhost material ist predators and parasitoids that may be associated with Western pine beetle, D. brevicomis, and its primary host, P. pon- the surface of nonhost trees (Stephen & Dahlsten 1976; derosa, were collected from one site in California (Table 1). Five Dahlsten 1982). Exploitation of this flight behavior in these nonhost trees were also collected from this site, whereas three economically- and ecologically-important insects has other nonhost trees were collected from a second site in California recently been studied by using NAVs and other antiaggre- (Table 1). The final nonhost, T. mertensiana, was collected from Alaska (Table 1) for other purposes, but was included in the study gants to reduce attack on single trees and in forest stands because although its high elevation distribution is largely allopatric (Wilson et al. 1996; Borden et al. 1998; 2003; Huber & with D. brevicomis, there are potential zones of sympatry in Borden 2001b; Jakuš et al. 2003; Zhang & Schlyter 2004; California, Oregon, Washington, and British Columbia (Burns & Fettig et al. 2007). Honkala 1990). Although some NAVs appear to be antennally-active in Larval, pupal, and adult D. brevicomis in outer bark and phloem were collected from standing P. ponderosa by falling trees a number of coniferophagous bark beetles (Huber et al. and transporting ~1 m stem sections to the Chemical Ecology and 2000b), there is enough variability in both antennal and Management of Forest Insects Laboratory in Davis, California behavioral responses (Dickens et al. 1992; Wilson et al. where they were placed into wooden emergence cages (Browne 1996; Borden et al. 1997; Byers et al. 1998; Deglow & 1972). Insects emerged into jars containing moist paper towels at 4°C and were immediately sorted by sex based on the presence of Borden 1998a,b; Poland et al. 1998; Huber et al. 1999; the female mycangium and protuberances on the male frons (Wood 2000a,b; 2001; Zhang et al. 1999a,b; 2000; 2001; 2002; 1982). Beetles were shipped regularly in September through Schlyter et al. 2000; Poland & Haack 2000; Huber 2001; November 2005 by overnight mail on ice to the Southern Research Zhang 2001; 2003; Huber & Borden 2001a,b; 2003; Jactal Station in Pineville, Louisiana for GC-EAD analyses. et al. 2001; Zhang & Schlyter 2003; Fettig et al. 2005) to The stems of host and nonhost trees for collection of volatiles were harvested and sectioned into 2 m lengths for transportation justify the use of detailed coupled gas chromatographic- to the