Periodic outbreaks of spruce budworm (SBW) affect large areas of ecologically and economically important conifer forests in North America, causing tree mortality and reduced forest productivity. Host resistance against SBW has been linked to growth phenology and the chemical composition of foliage, but the underlying molecular mechanisms and population variation are largely unknown. Using a genomics approach, we discovered a β-glucosidase gene, Pgβglu-1, whose expression levels and function underpin natural resistance to SBW in mature white spruce (Picea glauca) trees. In phenotypically resistant trees, Pgβglu-1 transcripts were up to 1000 times more abundant than in non-resistant trees and were highly enriched in foliage. The encoded PgβGLU-1 enzyme catalysed the cleavage of acetophenone sugar conjugates to release the aglycons piceol and pungenol. These aglycons were previously shown to be active against SBW. Levels of Pgβglu-1 transcripts and biologically active acetophenone aglycons were substantially different between resistant and non-resistant trees over time, were positively correlated with each other and were highly variable in a natural white spruce population. These results suggest that expression of Pgβglu-1 and accumulation of acetophenone aglycons is a constitutive defence mechanism in white spruce. The progeny of resistant trees had higher Pgβglu-1 gene expression than non-resistant progeny, indicating that the trait is heritable. With reported increases in the intensity of SBW outbreaks, influenced by climate, variation of Pgβglu-1 transcript expression, PgβGLU-1 enzyme activity and acetophenone accumulation may serve as resistance markers to better predict impacts of SBW in both managed and wild spruce populations.
Laboratory rearing of spruce budworm, Choristoneura fumiferana, in conjunction with field rearing, gravimetric analyses, a transfer experiment, and foliage chemical analyses at six dates during the period of budworm feeding activity indicated that the age of balsam fir, Abies balsamea, trees (70-year-old mature trees or 30-year-old juvenile trees) affected tree suitability for the spruce budworm via the chemical profile of the foliage. Insects reared on old trees had greater survival and pupal weight, shorter development times, and caused more defoliation than those reared on young trees. Young trees were more suitable for the development of young larvae (instars 2-5), while old trees were more suitable for the development of older, sixth-instar larvae. These results were confirmed by the laboratory transfer experiment. Young larvae fed foliage from young trees had higher relative growth rates (RGR), digestibility (AD), and efficiency of conversion of ingested foliage (ECI) than those fed foliage from old trees. These differences appeared to be related to the high N:tannins ratio, and the high contents of P present in young trees during the development of the young larvae. Old larvae fed foliage from old trees had higher relative growth rates, relative consumption rates (RCR), and digestibility of the foliage than those fed foliage from young trees. The high digestibility of the foliage of old trees was compensated for by a lower efficiency of conversion of digested food (ECD), which in turn resulted in no significant effect of tree age on the efficiency of conversion of ingested foliage by old larvae. The low relative consumption rate of old larvae fed foliage from young trees appeared to be related to the low N:tannins ratio, and the high contents of bornyl acetate, terpinolene, and °-3-carene present in young trees during the budworm sixth instar. Variations in these compounds in relation to tree age may serve as mechanisms of balsam fir resistance to spruce budworm by reducing the feeding rate of sixth instar larvae.
Variation in insect herbivory can lead to population structure in plant hosts as indicated by defence traits. In annual herbaceous, defence traits may vary between geographic areas but evidence of such patterns is lacking for long-lived species. This may result from the variety of selection pressures from herbivores, long distance gene flow, genome properties, and lack of research. We investigated the antagonistic interaction between white spruce (Picea glauca) and spruce budworm (SBW, Choristoneura fumiferana) the most devastating forest insect of eastern North America in common garden experiments. White spruces that are able to resist SBW attack were reported to accumulate the acetophenones piceol and pungenol constitutively in their foliage. We show that levels of these acetophenones and transcripts of the gene responsible for their release is highly heritable and that their accumulation is synchronized with the most devastating stage of SBW. Piceol and pungenol concentrations negatively correlate with rate of development in female SBW and follow a non-random geographic variation pattern that is partially explained by historical damage from SBW and temperature. Our results show that accumulation of acetophenones is an efficient resistance mechanism against SBW in white spruce and that insects can affect population structure of a long-lived plant.
Phenolic compounds are apparently important in the defence mechanisms of conifers. To test the hypothesis that phenolic compounds in resistant white spruce [Picea glauca (Moench) Voss (Pinaceae)] impart resistance against spruce budworm [Choristoneura fumiferana (Clemens) (Lepidoptera: Tortricidae)], we performed aqueous extractions of current-year shoots of white spruce that were tolerant of varying levels of budworm defoliation. High-performance liquid chromatographic profiles of water extracts of P. glauca needles differed between resistant and susceptible trees. Further nuclear magnetic resonance analyses identified two phenolic glucosides in susceptible white spruce, picein [3-(b-D-glucosyloxy)-hydroxy-acetophenone] and pungenin [3-(b-D-glucosyloxy)-4-hydroxy-acetophenone], and two phenolics in resistant white spruce, pungenol (3¢,4¢-hydroxy-acetophenone) and piceol (4¢-hydroxyacetophenone). We focused on the performance of spruce budworm when piceol and pungenol were added to the diet. These two compounds significantly reduced larval survival, retarded development, and reduced pupal mass. Food consumption by sixth-instar spruce budworms was affected by a combination of the phenolic compounds. These results suggest that the two phenolic compounds reduce the pressure of spruce budworm herbivory on specific host tree phenotypes. Thus, the mechanism of defence in P. glauca apparently reflects a strategy of constitutive resistance.
1. Four groups of spruce budworm larvae, Choristoneura fumiferana, of the same physiological stage (at the beginning of diapause) were exposed to natural temperatures, starting in July, August, September and October. Post-diapause emergence and certain metabolites were monitored throughout the overwintering period.2. Larval exposure to high temperatures for long periods before winter had a significant effect on temperature requirements for subsequent diapause development and apparently caused a certain amount of mortality, especially for those larvae that entered diapause earlier in the season.3. Substantial loss of lipid and glycogen reserves was related to intensity of high temperature exposure during the pre-winter period, which in turn was associated with the timing of diapause initiation.4. Patterns of glycerol accumulation during the winter were also influenced by temperature conditions in the early phase of diapause development.5. Among several possible mortality factors, an extended cool period in spring was suggested as a potential cause of overwintering mortality, which was closely associated with a deficiency in energy reserves caused by high temperature exposure before winter.6. These results stress the significant impact of pre-winter conditions on the overwintering process and highlight the importance of an ecophysiological approach to insect overwintering biology.
Summary 1.The abundance and performance of the Eastern Spruce Gall Adelgid, Adelges abietis, was evaluated on young, open-grown trees of White Spruce, Picea glauca, whose growth rates had been increased through fertilization or decreased through root-pruning. 2. In general, gall densities were highest on control trees and on mid-crown branches. Reduced galling success on fertilized trees was largely due to higher overwintering mortality of first-generation nymphs. Foliar magnesium, total tannin and total phenol contents were positively, and nitrogen and total monoterpene contents negatively, related to gall density and/or galling success. 3. Although short shoots were more abundant, shoot length was parabolically related to gall density. There was a non-significant parabolic trend between shoot size and galling success and volume. The number and average size of A. abietis females emerging from galls were positively related to gall volume, and realized fecundity was positively correlated to female size. Consequently, fitness was approximately twice as high for nymphs colonizing intermediate-sized than small or large shoots. 4. These results do not support the plant vigour or plant stress hypotheses. The results do, however, agree with predictions of the modified plant stress hypothesis for sucking insects. It is speculated that Adelges abietis lacks the necessary resources for successful gall formation on small shoots and is unable to produce a stimulus large enough to induce gall formation on large shoots. Key-words: Adelges abietis, insect-plant interactions, parabolic plant module size-galler abundance relationship, phenols, tanninsFunctional Ecology (1999) 13, [859][860][861][862][863][864][865][866][867] 859 DeBruyn 1994;Björkman 1997). Studies examining the relationship between insect performance and plant chemistry have also reported varying results (Tija & Houston 1975;Zucker 1982;Waring & Price 1990;Hartley & Lawton 1992;Waring & Cobb 1992;Bryant et al. 1993;Hartley & Jones 1997). Nevertheless, these studies generally found a positive relationship between insect performance and plant nitrogen content, and a negative relationship to secondary compounds (e.g. total phenols, tannins and monoterpenes).This study was carried out to determine the relationship between the abundance and performance of the shoot-galling Eastern Spruce Gall Adelgid Adelges abietis (L.) and the growth rate and foliar chemistry of White Spruce, Picea glauca (Moench) Voss. Tree growth and foliar chemistry were manipulated by fertilization and root pruning. We tested the predictions that gall abundance and galler performance would be higher on fast-growing trees (Plant Vigour hypothesis) with low C/N ratios than on slowgrowing trees with high C/N ratios, as well as the alternative prediction that gall abundance and galler performance would be highest on the slowest-growing, stressed trees (Plant Stress and Modified Plant Stress hypotheses). To obtain an estimate of fitness associated with the colonization of different-sized shoots we ...
Two field studies were carried out to determine the influence of Abies balsamea foliage age on the preference and performance of larvae of Neodiprion abietis, a specialist Diprionid sawfly. Preference was determined by examining N. abietis defoliation on all age classes of foliage. Performance was estimated using larval survival, cocoon weights and the percentage of adults that were females. Neodiprion abietis preference for, and performance on, current-year foliage was very low, peaked on 2 or 3-year-old foliage, and declined on older foliage. Thus, sawfly feeding preference was adaptive. However, survival and cocoon weight were highest when sawflies were allowed to feed on all age classes of foliage, demonstrating that an insect specialist may perform better when feeding on several age classes of foliage from a single host plant species. These results indicate that either different larval instars have different nutritional requirements, or that food mixing provides the best diet, permitting the herbivore to obtain needed nutrients while avoiding ingestion of toxic doses of secondary metabolites. In addition, our results suggest that limited availability of varied foliage has more negative consequences for N. abietis females than for males, as the percentage of survivors that were females decreased when juvenile mortality was high. Our results emphasize the importance of considering non-linear changes in foliar quality as leaves age on herbivore preference and performance, and demonstrate how a herbivore can use this variability to maximize its fitness.
A white spruce, Picea glauca (Moench) Voss (Pinaceae), plantation in southern Quebec was found to contain two distinct types of trees, the first resistant and the second susceptible to attack by spruce budworm, Choristoneura fumiferana (Clemens) (Lepidoptera: Tortricidae). To identify the mechanisms of white spruce resistance to spruce budworm, we studied the role of epicuticular waxes, comparing (i) the foliar chemistry of susceptible and resistant trees and (ii) the feeding pattern of larvae at first contact with the foliage. Needles collected from resistant trees contained concentrations of the monoterpenes α-pinene and myrcene that were 307% and 476%, respectively, above those found in needles collected from susceptible trees. Although there were no significant differences in probing behaviour, significantly fewer larvae transitioned from probing to feeding on resistant needles; this led to fewer feeding bouts as well as a significantly shorter first meal. Removal of waxes increased the number of individuals transitioning from probing to feeding on resistant needles; this led to more feeding bouts. Our results demonstrate that monoterpenes influence the pattern of feeding of spruce budworm larvae as well as playing an important role in white spruce resistance.
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