Repellency and Toxicity of ponderosae Hopkins (Coleoptera: Scolytidae) by the Host Monoterpene Myrcene

Brian M. Shirley and Stephen Cook

Seed orchards produce high-quality seed from selected tree genotypes. In the intermountain west, Conophthorus ponderosae Hopkins (Coleoptera: Scolytidae) is a pest in seed orchards of ponderosa pine, Pinus ponderosa (Laws). The effect of myrcene as a deterrent to cone attack by C. ponderosae in a ponderosa

pine seed orchard was examined. Two factors were considered, timing of cone cluster attack and average brood production per cone cluster. There was a delayed Downloaded from https://academic.oup.com/wjaf/article/22/4/241/4717750 by guest on 01 October 2021 attack by C. ponderosae on cones treated with vials of myrcene attached at the base of cone clusters. During both 2003 and 2004, final brood production per cone was not affected significantly by the presence of myrcene. During 2003, brood production was influenced by the timing of attack, with later attacks resulting in fewer brood adults per cone cluster. The toxicity of myrcene to adult C. ponderosae was examined in a laboratory and compared with that of ABSTRACT (ϩ)-␣-pinene, another host-produced monoterpene that acts as a synergist for the male attractant pheromone pityol. Keywords: Conophthorus ponderosae, monoterpene, ponderosa pine, repellency, myrcene, toxicity

onifer seed orchards are used to produce high-quality seed nisms of the tree. The girdling also causes seed abortion, but the from selected tree genotypes. Because the orchards are ex- cones of ponderosa pine typically remain attached to the stem. After Cpensive to establish and require intensive management, successfully attacking a cone, female C. ponderosae release a male-at- there is little tolerance for damage to the seed crop. In Idaho, the tractant sex pheromone, pityol (Birgersson et al. 1995). Typically, ponderosa pine cone , Conophthorus ponderosae Hopkins (Co- from 2 to 21 eggs are deposited in the gallery created by the female, leoptera: Scolytidae), can be a pest in both ponderosa pine [Pinus with the average being approximately 7 eggs per cone (Williamson ponderosa (Laws)] and western white pine [Pinus monticola (Doug- et al. 1966, Kinzer et al. 1970). Both parents usually remain in the las)] seed orchards (Wood 1982). C. ponderosae typically causes little cone throughout the brood development period (Wood 1982). No damage in natural pine stands (Schenk and Goyer 1967). For exam- published data are available on actual brood production per cone, ple, a study conducted over a wide area of north Idaho reported which should be lower than the number of eggs laid because of such damage to the cone crop of 9% by Conophthorus monticolae (equals factors as predation, parasitism, and competition among the devel- C. ponderosae) in natural stands of western white pine, P. monticola oping larvae. Douglas (Williamson et al. 1966). However, C. ponderosae was ob- Many scolytid use a combination of chemical and visual served destroying 24.8% of the potential seed crop of ponderosa cues to locate their respective host trees and for intraspecific com- pine over a 4-year period in New Mexico (Kinzer et al. 1970). A munication (Raffa 2001). The chemical cues used by scolytids are closely related (Conophthorus resinosae Hopkins) with a life often aggregation or sex pheromones that are frequently synergized history similar to that of C. ponderosae can reduce seed production by the presence of tree monoterpenes. Rappaport et al. (2000) de- by up to 90% in cultivated red pine stands (de Groot and Zylstra termined some of the chemical cues used by male C. ponderosae to 1995). Because of this potentially high level of seed mortality, or- locate mates. Male C. ponderosae exhibit a positive response to the chard managers frequently used insecticides such as carbofuran for female-produced sex pheromone pityol (Rappaport et al. 2000). control of C. ponderosae populations (DeBarr et al. 1982, Valenti et Male attraction to pityol is enhanced or diminished in the presence al. 1990). However, because of the impact of carbofuran on nontar- of specific host- and beetle-produced compounds. For example, get organisms and other negative environmental affects, it is no adding 4-allylanisole to a pityol-baited trap reduces trap catch of longer used against Conophthorus spp. male beetles, indicating some form of interruption in the beetle During the spring and early summer, adult C. ponderosae emerge communication system (Rappaport et al. 2000). Adding the tree- from cones attacked the previous year and disperse to locate new produced compound myrcene to pityol-baited traps also reduces host cones (Wood 1982). Female beetles initiate attacks near the trap catches (Shirley 2005). Similar reduction in trap catches has stem at the base of second-year cones. During the attack process, the been observed for other Conophthorus spp. when conophthorin is female girdles the cone, effectively cutting off the defensive mecha- added to traps (Birgersson et al. 1995, Pierce et al. 1995, de Groot et

Received April 26, 2006; accepted October 17, 2006. Brian M. Shirley ([email protected]), Department of Forest Resources, College of Natural Resources, University of Idaho, Moscow, ID 83844-1133. Stephen Cook ([email protected]), Department of Forest Resources, College of Natural Resources, University of Idaho, Moscow, Idaho 83844-1133. We thank Sanford Eigenbrode and Elwood Hart for their valuable input and the Bureau of Land Management for the use of their seed orchard. We also appreciate the valuable comments from two anonymous reviewers. The research was supported in part by the Inland Empire Tree Improvement Cooperative and the University of Idaho. Copyright © 2007 by the Society of American Foresters.

WEST.J.APPL.FOR. 22(4) 2007 241 al. 1998). However, pityol predominantly attracts male beetles, and examine the impact of the myrcene treatment on mean C. pondero- it is unclear what effect any of these compounds may have on female sae brood production per cone. The C. ponderosae broods in two beetles. Of the three compounds identified as potential repellents to untreated clusters of cones attacked by C. ponderosae were parasit- C. ponderosae, myrcene is produced by host trees, and it has been ized by Cephalonomia conophthori Evans (Hymenoptera: Bethyli- demonstrated to be toxic to other scolytid species (Cook and Hain dae) (Shirley et al. 2004). Because the objective of this study was to 1988, Raffa and Smalley 1995). Many host-produced monoter- determine the effects of myrcene on C. ponderosae brood produc- penes are toxic to herbivores, but the level of toxicity is not tion, only cones that had been attacked by C. ponderosae and that consistent across compounds (Cook and Hain 1988, Raffa and were without evidence of predation or parasitism were used in this Smalley 1995, Zou and Cates 1997, Wallin and Raffa 2000). An- analysis. There were 12 treated clusters and 11 untreated clusters other host monoterpene that is also toxic to several species of sco- with attack and no evidence of parasitism. lytids, ␣-pinene (Cook and Hain 1988, Raffa and Smalley 1995), To examine the effect of the attack period on brood production, has also been demonstrated to be a synergist for pityol in attracting the data were reclassified into two periods from the original four, male Conophthorus spp. (Rappaport et al. 2000, de Groot et al. based on the peak time period of beetle capture in pityol-baited traps 1998). within the orchard (Figure 1). The first three sample periods (May The overall objective of this study was to examine the impact of 9–June 23) were combined into a single period, which was the time myrcene on female C. ponderosae when they are attacking host cones period in which the highest daily trap catch of C. ponderosae oc- Downloaded from https://academic.oup.com/wjaf/article/22/4/241/4717750 by guest on 01 October 2021 and on subsequent, within-cone brood production. In addition, the curred. The remaining sample period coincided with the period of toxicity of myrcene to adult C. ponderosae was examined and com- the lowest number of male C. ponderosae trapped, and became the pared with the toxicity of ␣-pinene. new period 2. The reclassification of time periods enabled us to examine the data based on the biology of the beetle. The sample size Materials and Methods for the new analysis had 17 clusters for attack period 1 and 8 clusters In 2003 and 2004, fieldwork was conducted from May to July in for attack period 2 (again, parasitized cones were not included in this the Russell Barr seed orchard in north-central Idaho. The orchard is analysis). Differences between the two periods were compared using owned and operated by the Bureau of Land Management and is Student’s t-test. All statistical analyses were conducted using SAS located on the eastern shore of the Salmon river in Idaho County, Institute (2002). approximately 10 km south of Whitebird, Idaho. The seed orchard During 2004, 20 individual ponderosa pines were selected, and was established in 1977. P. ponderosa is the only species of conifer the control and myrcene treatments were applied to clusters in each present within the orchard. Trees are irrigated and pruned regularly tree and monitored as in 2003. However, during 2004, myrcene to prevent damage to the trees by the frequent prescribed fires ap- treatments were replaced at intervals of approximately 3 week (i.e., plied to the orchard (approximately every 2–3 years). The grasses at the time of cone inspection). The myrcene treatments were re- and forbs growing around the trees are mown frequently (approxi- placed to ensure a continuous presence of myrcene throughout the mately every 2–3 weeks) throughout the growing season. flight season, and the monitoring dates were set earlier to ensure that During 2003, 18 individual ponderosa pine trees with a mini- the myrcene was present prior to any beetles’ flight. There were three mum distance of 20 m between trees were selected for use in this monitoring periods during 2004: April 15–May 14, May 15–June experiment. Each tree had multiple cone clusters in the lower can- 4, and June 5–24. There was not a trapping study being conducted opy, and clusters were more than 2 m apart. The cone clusters on in the orchard during 2004, so we were unable to correlate the each tree were used as pairs and randomly assigned one of two periods of attack with the flight of male C. ponderosae. All cone treatments. One cluster per tree had a slow-release (275 mg/day at clusters were collected at the end of the last period, and each cone 23° C) vial of myrcene (Phero Tech, Inc., Delta, British Columbia, was placed in an individual paper bag to allow the brood to complete Canada) attached to it, and the second cluster was used as a non- development. The cones were dissected on August 24, and the num- treated control. A total of 36 clusters (18 pairs) were used during ber of brood per cone was determined as in 2003. Adults that were 2003. The limbs containing the respective cone clusters were extracted from the cones were subsequently used in the toxicity tests marked, and cones were monitored for attack by C. ponderosae at described below. approximately 2-week intervals throughout the flight season. The Statistical analyses were conducted similarly to those for the vials were placed in the trees on May 9, and there were four moni- 2003 data; however, because there were three time periods, a general toring periods: May 9–23, May 23–June 6, June 6–23, and June linear model was used for comparison of brood per cluster by time 23–July 6). period. As with the 2003 data, only cones that had been attacked by At the end of the flight period (mid-July), cones were collected C. ponderosae were used in the analysis. There were 15 treated cone and placed in individual paper bags to allow any brood present clusters and 20 untreated cone clusters that were attacked by C. within the cones to complete development. The length of each cone ponderosae, and there was no evidence of parasitism in any of the 35 was measured, and any natural enemies that were in the cone or the clusters. rearing bag were collected and identified. Cones were dissected in The toxicity of myrcene (90% pure; Sigma-Aldrich, Steinheim, the laboratory, and the number of brood per cone was determined. Switzerland) and (ϩ)-␣-pinene (97% pure; Sigma-Aldrich) to adult No more than two adult beetles were ever present within the parent C. ponderosae was examined in 2004. The C. ponderosae adults used galleries, and beetles found inside the original attack gallery were not for the test were extracted from ponderosae pine cones collected at counted as brood, but were assumed to be parents. the Russell Barr seed orchard as described above. Additional C. The proportion of cones attacked by C. ponderosae was compared ponderosae adults were extracted from cones that were from the same among treatments and time periods. Total C. ponderosae brood per seed orchard but were not part of the repellency experiment. Indi- attacked cone was examined to determine the effect of the myrcene vidual beetles were placed in glass vials capped with perforated alu- treatment and the time of attack. A Student’s t-test was conducted to minum foil and maintained away from host volatiles for 1 day at

242 WEST.J.APPL.FOR. 22(4) 2007 Downloaded from https://academic.oup.com/wjaf/article/22/4/241/4717750 by guest on 01 October 2021

Figure 1. Average number of male C. ponderosae trapped per day (؎SEM) in nine traps baited with the sex pheromone pityol plus the monoterpene ␣-pinene during four sampling periods.

22.5° C. The beetles were randomly assigned among treatments, There were 154 C. ponderosae adult beetles collected from the 23 with five beetles per treatment. Five glass vials containing individual clusters (63 cones) that were attacked and that did not have natural beetles were placed in a large glass jar (1.1 l) with filter paper rounds enemies present within them during 2003. In addition, 36 adult (diameter, 5.5 cm) taped to the inside of the jar. Terpene treatments Cephalonomia conophthori Evans (Hymenoptera: Bethylidae), a were applied to the filter paper using a micropipette, and the jars parasitoid of C. ponderosae, were collected from two cones (Shirley et were sealed. The treatments were as follows: filter paper alone (con- al. 2004). The two cones with the parasitoids present were not trol); myrcene or ␣-pinene in doses of 10, 25, 50, and 75 parts per included in the analysis; both cones were untreated and attacked million (ppm). The filter paper alone (0 ppm) treatment had 8 during attack period one. There was not a significant difference (t ϭ replicates; the 10-, 25-, and 50-ppm treatments had 5 replicates 2.09; df ϭ 21: [p Ͼ t] ϭ 0.1551) between the C. ponderosae brood each; and the 75-ppm treatments were replicated 3 times (total n ϭ produced in untreated control clusters versus myrcene-treated clus- 220 adult C. ponderosae). The jars with the beetles were maintained ters by the end of the season (Table 1). However, cones attacked by at 22.5° C, and mortality was measured daily for four consecutive C. ponderosae during the first period (6 weeks: May 3–June 23) days. Probit analysis was conducted for data on days 2, 3, and 4 to produced significantly more (t ϭ 2.04; df ϭ 21: [p Ͼ t] ϭ 0.0213) estimate the concentration of each tested monoterpene at which brood per cone than did cones attacked during the second period (3 50% mortality of C. ponderosae adults occurred (LC50). In addition, weeks: June 24–July 16). the time to 50% C. ponderosae adult population mortality (LT50) Similar to the 2003 results, the proportion of cone clusters at- was estimated for each treatment dose using probit analysis. All tacked by C. ponderosae was consistently higher on untreated clusters statistical analyses were conducted using SAS Institute (2002). than on clusters treated with myrcene during 2004 (Figure 2b). Clusters in both treatments were attacked during each period, but Results there was a difference in the proportion of attack for each period by Repellency Trials treatment. By June 7, 82% of the nontreated clusters had been During 2003, the proportion of cone clusters attacked by C. attacked versus 41% of the myrcene-treated clusters. Untreated con- ponderosae was consistently higher for untreated clusters versus clus- trols were attacked most heavily during the first sample period, ters treated with myrcene (Figure 2a). There were no C. ponderosae whereas the treated clusters were attacked at the same rate for the attacks on the myrcene-treated clusters during the first 2-week pe- first and third periods, with a small reduction in attack during the riod versus 44% attack on nontreated clusters. By the end of the second period. second period, 17% of the myrcene-treated clusters had been at- There were 92 adult C. ponderosae collected from the 35 clusters tacked compared with 67% of the nontreated clusters during the (54 cones) that were part of the experiment during 2004. No pred- same period. Further, the highest proportion of myrcene-treated ators or parasitoids were observed in the attacked cones. Over the cone clusters was attacked during the last sampling period, when total summer, there was no significant difference (t ϭ 2.03; df ϭ 33: more than 60% of the attack of treated clusters occurred. In com- [p Ͼ t] ϭ 0.1979) in C. ponderosae brood production between parison, nearly 90% of the attack on untreated clusters occurred myrcene-treated cone clusters and untreated cone clusters (Table 2). during the first two sampling periods. There was also no significant difference (F ϭ 1.34; df ϭ 2, 32: [p Ͼ

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Figure 2. Cumulative proportion of P. ponderosa clusters with and without myrcene present that were attacked by C. ponderosae during four consecutive sample periods in 2003 (a) and during three consecutive sample periods in 2004 (b).

Table 1. Mean brood production (؎SEM) of C. ponderosae per attacked P. ponderosa cone during 2003, by treatment and attack period (period 1, May 3 to June 23; period 2, June 24 to July 16).

Period 1 Period 2 Total Treatment n Brood/cone n Brood/cone na Brood/cone Control 11 5.83 Ϯ 1.22 1 1 12 5.80 Ϯ 0.84 Myrcene 4 3.96 Ϯ 1.84 7 1.33 Ϯ 0.85 11 2.29 Ϯ 1.23 Total 15 4.86 Ϯ 0.82 8 1.32 Ϯ 0.68

a Mean number of cones per cluster for controls, 1.58 Ϯ 0.82. Mean number of cones per cluster for myrcene-treated cones, 1.18 Ϯ 0.64

244 WEST.J.APPL.FOR. 22(4) 2007 Table 2. Mean brood production (؎SEM) of C. ponderosae per attacked P. ponderosa cone during 2004, by treatment and attack period (period 1, April 15 to May 14; period 2, May 15 to June 4; period 3, June 5 to June 24).

Period 1 Period 2 Period 3 Total Treatment n Brood/cone n Brood/cone n Brood/cone na Brood/cone Control 16 4.00 Ϯ 0.89 1 1.00 3 2.00 Ϯ 2.00 20 1.95 Ϯ 0.83 Myrcene 7 7.43 Ϯ 1.87 3 1.33 Ϯ 4.30 5 2.00 Ϯ 1.64 15 3.53 Ϯ 1.14 Total 23 3.30 Ϯ 0.81 4 2.00 Ϯ 2.31 8 1.00 Ϯ 0.81

a Mean number of cones per cluster for controls, 1.20 Ϯ 0.64. Mean number of cones per cluster for myrcene-treated cones, 1.27 Ϯ 0.68

␣ ؉ ؎ Table 3. Survival (percent SEM) of C. ponderosae adults and the estimated LT50 for C. ponderosae exposed to ( )- -pinene or myrcene at various concentrations (initial survival was 100%).

Days after exposure

a b, c c, d Tr Con n 1234LT50 95% CI C 0 40 100 100 100 100

Ap 10 25 100 100 100 96 Ϯ 2.2 Downloaded from https://academic.oup.com/wjaf/article/22/4/241/4717750 by guest on 01 October 2021 25 25 100 100 96 Ϯ 2.2 92 Ϯ 4.5 13.24 50 25 92 Ϯ 2.7 68 Ϯ 2.7 60 Ϯ 3.5 52 Ϯ 2.7 6.16 2.99–10.46 75 15 47 Ϯ 15 27 Ϯ 23 0 0 1.25 0.66–3.08 My 10 25 92 Ϯ 4.5 92 Ϯ 4.5 92 Ϯ 4.5 92 Ϯ 4.5 3.61 25 25 96 Ϯ 2.2 80 Ϯ 6.1 80 Ϯ 6.1 76 Ϯ 6.1 3.18 0–36.48 50 25 80 Ϯ 4.2 60 Ϯ 4.2 50 Ϯ 5.7 35 Ϯ 9.4 1.25 0–5.38 75 15 60 Ϯ 8.7 13.3 Ϯ 2.9 0 0 1.25 0.27–2.75

a Tr, treatment; Con, concentration of the tested monoterpene (ppm); C, control; Ap, (ϩ)-␣-pinene; My, myrcene. b The number of days to 50% mortality of the population of C. ponderosae at a specific dose. Table cells without values had insufficient mortality during the observation periods. c LT50 and 95% CI values were calculated using the Probit analysis described in SAS Institute (2002). d For table cells without values, confidence intervals were not calculated due to the low mortality during the observation periods. f] ϭ 0.2772) in brood production by time period; however, similar over time. The 2004 experiment accounted for this possible deple- to 2003, there were fewer brood per cluster the later the clusters were tion by replacing the myrcene vials at intervals of approximately 3 attacked in the season. weeks (when C. ponderosae attacks started to occur on the treated cones in 2003). During 2004, C. ponderosae attack rates similar to Toxicity Trials 2003 were reached by the end of the season even with the replace- ␣ The LT50 for C. ponderosae exposed to -pinene was not signif- ment of the myrcene treatment. This suggests that myrcene, al- icantly different from the LT50 for C. ponderosae exposed to myrcene though effective at preventing attack of cones by C. ponderosae early at any of the exposure concentrations (Table 3). Rearing C. pondero- in the season, loses effectiveness later in the season. It is important to sae outside the natural setting is extremely difficult to do. Because of note that the population of beetles in this orchard is very high, this, the sample sizes for the toxicity study were small [n ϭ 5 adult C. frequently resulting in virtually no seed production, as evidenced by ponderosae per replicate; total n ϭ 15 (75 ppm), 25 (10, 25, and 50 the high rate of attack reported here. At such high C. ponderosae ppm), and 40 (0 ppm)], which probably contributed to the large infestation levels, competition for host cones could become high confidence intervals. enough to reduce the sensitivity of the female C. ponderosae to myrcene. There was not a statistically significant difference between the Discussion brood production of treated and untreated cones during either 2003 The proportion of cone clusters from each treatment (untreated or 2004. One possible explanation for the lack of differences is that and myrcene-treated) eventually attacked by C. ponderosae during environmental cues other than semiochemicals are important to C. both years of the study was similar (2003: untreated, 78%, and ponderosae in locating hosts and mates or that other tree volatiles ϩ ␣ myrcene-treated, 61%; 2004: untreated, 94%, and myrcene- [( )- -pinene] that are released at the time of attack reduce the treated, 71%). However, the proportion of clusters attacked by C. negative response of the males to the presence of myrcene. Another ponderosae that were treated with myrcene never equaled the pro- possibility is that once beetles have mated, a treatment on the out- portion of untreated clusters that were attacked in either year of the side of the cone does not affect brood production or survival within study. In addition, most of the C. ponderosae attacks on the the cone. myrcene-treated clusters occurred later in the season than did at- The time of attack by female C. ponderosae was the only factor tacks on the untreated clusters. The similar final attack rate suggests measured that appeared to affect brood production in the success- that all clusters in the study were suitable hosts. If the clusters are all fully attacked cones. There was a significant difference in the brood suitable, the delayed attack suggests that the myrcene was initially production of cones attacked early versus late in the season during deterring attack of the cones by C. ponderosae females. 2003, with cones attacked later having lower brood production. During 2003, a single application of myrcene was used, and vials During 2004, there was also a decrease in brood production if attack were noted to be visibly dry at the end of the experiment. The occurred later in the season. Female C. ponderosae can re-emerge increase in C. ponderosae attack of the treated clusters later in the from attacked cones after ovipositing and attack a second cone study was possibly due to the depletion of the myrcene in the vials (Wood 1982). This late re-emergence and attack of additional cones

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␣ ؉ ؎ Figure 3. Estimated concentration ( 95% CI) for 50% population mortality (LC50)ofC. ponderosae exposed to myrcene and ( )- -pinene. may partially account for the observed decreases in brood later in the Literature Cited season. Females re-emerging from cones could have lower energy BIRGERSSON, G., G.L. DEBARR,P.DE GROOT, M.J. DALUSKY, H.D. PIERCE, J.H.J. reserves because of the energy expended laying eggs in the previous BORDEN,G.MEYER,W.FRANCKE, K.E. ESPELIE, AND C.W. BERISFORD. 1995. cone and may not produce more eggs. The trend of reduced egg Pheromones in white pine cone beetle, Conophthorus coniperda (schwarz) laying potential after a previous attack has been shown in other (Coleoptera: Scolytidae). J. Chem. Ecol. 21:143–167. COOK, S.P., AND F.P. HAIN. 1988. Toxicity of host monoterpenes to Dendroctonus scolytid species (Wagner et al. 1981). frontalis and Ips calligraphus (Coleoptera: Scolytidae). J. Entomol. Sci. Although not significantly different, the LC50 of myrcene to C. 23:287–292. ϩ ␣ ponderosae was consistently lower than the LC50 of ( )- -pinene DEBARR, G.L., L.R. BARBER, AND A.H. MAXWELL. 1982. Use of carbofuran for control of eastern white pine cone and seed . For. Ecol. Manag. 4:1–18. (Figure 3). The estimated LT50 of the two compounds to the beetles DE GROOT, P., AND B.F. ZYLSTRA. 1995. Factors affecting capture of male red pine was not statistically significant, but the LT50 of myrcene was con- ϩ ␣ cone beetles, Conophthorus resinosae Hopkins (Coleoptera: Scolytidae), in stantly shorter than the LT50 values of ( )- -pinene, with the ex- pheromone traps. Can. Entomol. 127:851–858. ception of the 75-ppm treatment, where the LT50 values for the two DE GROOT, P., G.L. DEBARR, AND G. BIRGERSSON. 1998. Field bioassays of synthetic compounds were identical (Table 3). There were large confidence pheromones and host monoterpenes for Conophthorus coniperda (Coleoptera: Scolytidae). Environ. Entomol. 27:382–387. intervals associated with both the LT50 and LC50 estimates, proba- bly because of the relatively small sample sizes. Although beetles KINZER, H.G., B.J. RIDGILL, AND J.G. WATTS. 1970. Biology and cone attack behavior of Conophthorus ponderosae (Coleoptera: Scolytidae) in southern New were maintained for 1 day prior to monoterpene exposure to limit Mexico. Ann. Entomol. Soc. Am. 63:795–798. physical problems and little to no mortality occurred in the controls, PIERCE, H.D.J., P. DE GROOT, J.H. BORDEN,S.RAMASWAMY, AND A.C. some error may also have been introduced by physically removing OEHLSCHLAGER. 1995. Pheromones in red pine cone beetle, Conophthorus beetles from the cones rather than waiting for them to emerge. More resinosae Hopkins, and its synonym, C. banksianae McPherson (Coleoptera: study and replication are needed to accurately assess the toxicity of Scolytidae). J. Chem. Ecol. 21:169–185. RAFFA, K.F. 2001. Mixed messages across multiple trophic levels: The ecology of bark myrcene to C. ponderosae. beetle communication systems. Chemoecology 11:49–65. Myrcene shows promise for use in an integrated pest manage- RAFFA, K.F., AND E.B. SMALLEY. 1995. Interaction of pre-attack and induced ment system for managing populations of C. ponderosae in seed monoterpenes concentrations in host conifer defense against -fungal orchards. In this orchard, myrcene caused a disruption of attack by complexes. Oecologia 102:285–295. RAPPAPORT, N., J.D. STEIN, D.R.M.A. ARTURO,G.DEBARR,P.DE GROOT, AND S. the female beetles on the host cone, at least early in the flight season. MORI. 2000. Responses of Conophthorus spp. (Coleoptera: Scolytidae) to There was also a reduction in brood production in cones attacked behavioral chemicals in field trials: A transcontinental perspective. Can. Entomol. later in the summer. However, there was not a significant reduction 132:925–937. in brood production based solely on the presence of myrcene. Re- SAS INSTITUTE. 2002. PROC user’s manual, version 7th Ed. SAS Institute, Cary, NC. ducing the brood production in an orchard setting could be bene- SCHENK, J.A., AND R.A. GOYER. 1967. Cone and seed insects of western white pine in northern Idaho. J. For. 65:186–187. ficial in reducing the residual beetle populations to an acceptable SHIRLEY, B. 2005. Potential for using monoterpenes in an integrated pest management level, such that dependence on pesticides for control could also be program for Conophthorus ponderosae (Coleoptera: Scolytidae). MSc thesis, Univ. reduced. Idaho, Moscow, ID. 51 p.

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